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Algae & Phylum & Class & Family & Genus & Approach & Host localization & Zone & Ref \\
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Seaweed & 
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\DOI{10.5802/crchim.271}
\datereceived{2023-06-08}
\daterevised{2023-10-06}
\datererevised{2023-10-26}
\dateaccepted{2023-11-09}
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\dateposted{2024-04-04}
\begin{document}

\begin{noXML}

\CDRsetmeta{articletype}{review}

%\makeatletter
%\def\TITREspecial{\relax}
%\def\cdr@specialtitle@english{Chemical Ecology -- Chemical Mediation in the Environment}
%\def\cdr@specialtitle@french{\'Ecologie chimique -- M\'ediation chimique dans l'environnement}
%\makeatother

\title{A review on the chemical ecology of the Fucaceae holobionts:
from fundamental knowledge to applications{\vspace*{-3pt}}}

\alttitle{Revue de la litt\'{e}rature sur l'\'{e}cologie chimique de
l'holobionte des \textit{Fucaceae} : des connaissances fondamentales
aux applications}

\author{\firstname{Coralie} \lastname{Rousseau}\CDRorcid{0009-0005-8568-3449}\IsCorresp\IsEqualContrib}
\address{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}
\email[C. Rousseau]{coralie.rousseau@sb-roscoff.fr}


\author{\firstname{Gautier} \lastname{Demoulinger}\CDRorcid{0009-0003-0896-3995}\IsEqualContrib}
\address{Molecules of Communication and Adaptation of Microorganisms (MCAM, UMR 7245), National Museum of Natural History, CNRS, 75000 Paris, France}
\address{Plant Nutrition R\&D Department, Centre Mondial de l'Innovation of Groupe Roullier, 35400 Saint-Malo, France}


\author{\firstname{Sylvie} \lastname{Rousvoal}}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}


\author{\firstname{Delphine}~\lastname{Champeval}}
\addressSameAs{2}{Molecules of Communication and Adaptation of Microorganisms (MCAM, UMR 7245), National Museum of Natural History, CNRS, 75000 Paris, France}


\author{\firstname{Maurane} \lastname{Dolly}}
\addressSameAs{2}{Molecules of Communication and Adaptation of Microorganisms (MCAM, UMR 7245), National Museum of Natural History, CNRS, 75000 Paris, France}


\author{\firstname{Gurvan} \lastname{Michel}\CDRorcid{0000-0002-3009-6205}}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}


\author{\firstname{Fran\c{c}ois} \lastname{Thomas}\CDRorcid{0000-0003-1896-0774}}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}


\author{\firstname{Gabriel~V.}~\lastname{Markov}\CDRorcid{0000-0002-8566-7482}}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}


\author{\firstname{Philippe} \lastname{Potin}\CDRorcid{0000-0001-7358-6282}}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}


\author{\firstname{Simon M.} \lastname{Dittami}\CDRorcid{0000-0001-7987-7523}\IsCorresp}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}
\email[S. M. Dittami]{simon.dittami@sb-roscoff.fr}

\author{\firstname{Soizic} \lastname{Prado}\CDRorcid{0000-0002-8071-9642}\IsCorresp}
\addressSameAs{2}{Molecules of Communication and Adaptation of Microorganisms (MCAM, UMR 7245), National Museum of Natural History, CNRS, 75000 Paris, France}
\email[S. Prado]{soizic.prado@mnhn.fr}

\author{\firstname{Catherine}~\lastname{Leblanc}\CDRorcid{0000-0001-7149-0332}\IsCorresp}
\addressSameAs{1}{Integrative Biology of Marine Models (LBI2M, UMR 8227), Station Biologique de Roscoff, Sorbonne Universit\'{e}, CNRS, 29680 Roscoff, France}
\email[C. Leblanc]{catherine.leblanc@sb-roscoff.fr}

\author{\firstname{C\'{e}cile} \lastname{Le Guillard}\CDRorcid{0000-0002-1269-8640}\IsCorresp}
\addressSameAs{3}{Plant Nutrition R\&D Department, Centre Mondial de l'Innovation of Groupe Roullier, 35400 Saint-Malo, France}
\email[C. Le Guillard]{Cecile.LeGuillard@roullier.com}

\shortrunauthors

\begin{abstract}
In recent years, the use of brown seaweeds (Phaeophyceae) and
especially Fucaceae, has increased for a variety of applications
including food additives, nutraceuticals, cosmetics, and agriculture,
mainly because most edible brown algae contain valuable bioactive
compounds. However, the growing demand for some species, such as
\textit{Ascophyllum nodosum}, has become a major concern due to the
risk of overharvesting. Along with this increasing demand, there is
growing awareness of the intricate interactions between algal hosts and
their microbiota. The Fucaceae are of particular interest in this
regard, as several species exhibit specificity with regard to their
associated endophytic fungi. Many of these associated microbes produce
a wide range of bioactive compounds themselves and may contribute to
well-known properties previously attributed to the host. For some
compounds, an alternative to wild harvesting could be the production of
molecules of interest by organic synthesis or by biotechnological
production, e.g.,  in microbial cell factories incorporating
selected members of the algal microbiota. This requires in-depth
knowledge of the alga and its microbiota to recognize the origin and
the synthesis pathways of these bioactive compounds. This review
presents the current understanding of the Fucaceae and their associated
microbiota as sources of chemical compounds intended for diverse
applications.
{\vspace*{-2pt}}
\end{abstract}


\begin{altabstract}
Ces derni\`{e}res ann\'{e}es, l'utilisation des algues brunes
(\textit{Phaeophyceae}) et sp\'{e}cifiquement les \textit{Fucaceae}, a
augment\'{e} dans plusieurs domaines d'applications, incluant les
additifs alimentaires, les nutraceutiques, les cosm\'{e}tiques et
l'agriculture, principalement parce que la plupart des algues brunes
comestibles contiennent des compos\'{e}s bioactifs pr\'{e}cieux.
Toutefois, la demande croissante pour certaines esp\`{e}ces, comme
\textit{Ascophyllum nodosum}, est devenue une pr\'{e}occupation majeure
en raison du risque de surexploitation. D'autre part, les
interactions complexes entre les algues h\^{o}tes et leurs microbiotes
sont de plus en plus connues. Les \textit{Fucaceae} sont
particuli\`{e}rement int\'{e}ressantes \`{a} cet \'{e}gard, car
plusieurs esp\`{e}ces de cette famille sont associ\'{e}es de
mani\`{e}re stable \`{a} des champignons intracellulaires. Nombre de
ces microbes associ\'{e}s produisent eux-m\^{e}mes une large gamme de
compos\'{e}s bioactifs et peuvent contribuer aux propri\'{e}t\'{e}s
pr\'{e}c\'{e}demment attribu\'{e}es \`{a} l'h\^{o}te. Pour certains
compos\'{e}s, une alternative \`{a} la r\'{e}colte sauvage pourrait
\^{e}tre la production de mol\'{e}cules d'int\'{e}r\^{e}t par chimie de
synth\`{e}se ou par production biotechnologique, par exemple en
utilisant certains microbes s\'{e}lectionn\'{e}s du microbiote algal
comme des usines cellulaires microbiennes. Cela n\'{e}cessite une
connaissance approfondie de l'algue et de son microbiote afin de
reconna\^{i}tre l'origine et les voies de synth\`{e}se de ces
compos\'{e}s bioactifs. Cette revue pr\'{e}sente les connaissances
actuelles sur les \textit{Fucaceae} et leur microbiote associ\'{e} en
tant que sources de compos\'{e}s chimiques destin\'{e}s \`{a} diverses
applications.
\end{altabstract}

\thanks{SEABIOZ ANR project (AAPG2020,
ANR-20-CE43-0013),  ANRT and the Centre Mondial de l'Innovation of
the Groupe Roullier (Cifre grant number 2022/0938),  UMR 8227
of the Roscoff Biological Station (CNRS, Sorbonne University),  UMR
7245 of the National Museum of Natural History{\vspace*{-1pt}}}

\keywords{\kwd{Holobiont}
\kwd{Fucaceae}
\kwd{Bioactive compounds}
\kwd{Microbiota}} 


\altkeywords{\kwd{Holobionte}
\kwd{\textit{Fucaceae}} 
\kwd{Compos\'{e}s bioactifs}
\kwd{Microbiote}} 

\maketitle

\twocolumngrid

\end{noXML}


\section{Introduction}

Seaweeds are classified into three phylogenetically independent groups:
the red algae (Rhodophyta), the green algae (Chlorophyta), and the
brown algae (Phaeophyceae) \cite{bib1}. Within the class Phaeophyceae,
the order Fucales represents nine families and contains more than 500
described species, including the Fucaceae. The family Fucaceae
comprises six genera: \textit{Ascophyllum}, \textit{Silvetia},
\textit{Pelvetia, Hesperophycus}, \textit{Pelvetiopsis} and
\textit{Fucus}~\cite{bib2} (Figure~\ref{fig1}).



\begin{figure*}
{\vspace*{-2pt}}
\includegraphics{fig01}
{\vspace*{-2pt}}
\caption{\label{fig1}
Scheme showing the phylogenetic positions of Fucaceae genera and
picturing representative species from the main orders~(B) among the
brown algal lineage~(A).}
\end{figure*}

The life cycle of the Fucaceae is monogenetic and heteromorphic with
both diecious and monoecious species (Figure~\ref{fig2}). 

\begin{figure*}
\includegraphics{fig02}
{\vspace*{-1pt}}
\caption{\label{fig2}
Examples of life cycles in Fucales of dioecious (A) and monoecious (B)
species.}
{\vspace*{-2pt}}
\end{figure*}

Species of Fucaceae thrive mainly in the Northern Hemisphere in
foreshore rocky substrates exposed to the tides, known as the
intertidal zone (Table~\ref{tab1}). \textit{Pelvetia} is found in the
North-East Atlantic Ocean, the Arctic Ocean, and the North Sea.
\textit{Ascophyllum} and \textit{Fucus} are mainly present in the North
Atlantic Ocean, while \textit{Pelvetiopsis}, \textit{Silvetia},
\textit{Fucus}, and \textit{Hesperophycus} are found in the North
Pacific (Table~\ref{tab1}). The changing physicochemical factors of the
intertidal zone, such as salinity, solar radiation, tidal range, wave
exposure, and temperature influence the geographic distribution of
macroalgae. These factors also generate a local distribution pattern
such as the vertical zonation. \textit{Pelvetia canaliculata} is
usually found in the extreme upper intertidal zone, followed by
\textit{Fucus spiralis} and \textit{Fucus guiryi}. In the
mid-intertidal zone, \textit{Ascophyllum nodosum} prefers sheltered
rocky shores whereas \textit{Fucus vesiculosus} occurs on exposed
rocks. In the lower intertidal zone, \textit{Fucus serratus} is
commonly observed growing on sheltered rocks \cite{bib3,bib4}. 


\begin{table*}
\caption{\label{tab1}Distribution of the six genera from the Fucaceae family}
\begin{tabular}{cccc}
\thead
Genus  & Geographic region & Zone & References \\
\endthead 
\textit{Ascophyllum} & 
North Atlantic Ocean & 
Sheltered intertidal & \cite{bib5,bib6,bib7} \\

\textit{Fucus} & 
North Pacific, North Atlantic &
Mid-tidal to subtidal & \cite{bib8,bib9,bib10}  \\

\textit{Pelvetia} & 
\parbox[t]{5cm}{\centering North-East Atlantic, Arctic Ocean, North Sea} &
\parbox[t]{4.5cm}{\centering Sheltered extreme upper intertidal} 
& \cite{bib6,bib11}\vspace*{2pt} \\

\textit{Pelvetiopsis} & 
North Pacific, from South to North Canada &
Upper intertidal & \cite{bib12} \\

\textit{Silvetia} &  \parbox[t]{6.4cm}{\centering North Pacific, West
coast of North America, Coastlines of Japan, China and Korea} & 
Mid-tidal & \cite{bib6,bib12}\vspace*{2pt} \\

\textit{Hesperophycus} &  \parbox[t]{6.4cm}{\centering North Pacific,
from Santa Cruz, California to Islas San Benito, Baja California} &
Upper intertidal & \cite{bib13}\vspace*{2pt}
\botline
\end{tabular}
\end{table*}

Some members of the Fucaceae are considered ecosystem engineers
\cite{bib6,bib9,bib10} as they form diverse three-dimensional habitats
that serve as refuge for a wide range of micro- to macroscopic living
organisms~\cite{bib14,bib15}. Lastly, the Fucaceae are important for
the marine food web, and act as a source of food for a diverse array of
living organisms such as birds, mammals, and fishes~\cite{bib16}.

Beyond their ecological functions, the Fucaceae have been harvested by
humans for centuries, serving not only as sustenance for livestock and
humans, but also finding application in agriculture and as traditional
medicinal remedies~\cite{bib12}. Regarding the exploitation of
Fucaceae, to our knowledge there are no data available globally or at
the European level for this specific family. However, at least in some
regions, such as Brittany in France,  \textit{A. nodosum} and
\textit{Fucus spp.} are the main intertidal seaweed species exploited,
accounting for 80\% of the total amount of seaweed (6436 tons fresh
weight) harvested directly on the shore in 2021 by
professionals~\cite{bib17,bib18}. The strong local exploitation of
these two species of Fucaceae is consistent with their distribution in
the North Atlantic Ocean (Table~\ref{tab1}), as France is the second
largest producer after Norway in Europe. Globally, the majority of
these uses are based on the alga itself or its extracts. However, the
biosynthetic origin of the bioactive molecules within these extracts is
not yet fully known. Indeed, some of the compounds present in these
seaweed extracts may be derived from the seaweed itself or from its
microbiota (i.e., bacteria, archaea, viruses, fungi and other
eukaryotes found in the biofilm forming on the host surface but also
inside the host tissues).


The aim of this systematic review is to synthetize the current
knowledge on aspects of the biology and chemistry of the Fucaceae and
their associated microbiota. It will examine the chemical interactions
within the Fucaceae holobiont, i.e., the functional entity
resulting from the association of a host and its microbiota
\cite{bib19,bib20,bib21}, and will lead to a better understanding of
the ecological roles assumed by its different partners. This
fundamental knowledge on the chemical ecology of Fucaceae, i.e.,
chemically mediated interactions between the Fucaceae and associated
organisms, will also offer new perspectives on the application and
valorization of the Fucaceae holobiont. For instance, it could reveal
whether some microorganisms are necessary for the seaweed to produce
specific compounds of interest. It also helps us to understand to what
extent and how the environmental parameters affect the biosynthesis of
compounds within the holobiont in Nature. In the case of molecules
produced by a microorganism or a community of microorganisms itself, it
would be possible to consider a year-round production of the compound
of interest in a bioreactor, which would contribute to the sustainable
exploitation of the chemical diversity of Fucaceae holobionts. 

We will first review the applications of the Fucaceae (Section~\ref{sec2})
focusing on the European market, followed by reviewing the available
information regarding the algal microbiota and its influence on the
host, such as how fitness and the production of compounds of interest
are impacted (Section~\ref{sec3}). Lastly, we will focus on the compounds
produced by the associated microbiota and discuss their potential role
in the biology and ecology of the Fucaceae\unskip\break (Section~\ref{sec4}).


\section{Overview of the applications of Fucaceae}\label{sec2}


In Europe, the leading markets for seaweed-derived products are the
production of plant biostimulants for agriculture and the phycocolloid
industry. Thus, the main commercially exploited species are brown
seaweeds (more than 99\%), such as \textit{Alaria esculenta},
\textit{Laminaria hyperborea}, \textit{Laminaria digitata},
\textit{Saccharina latissima}, \textit{Undaria pinnatifida}, and
\textit{A. nodosum}, which belongs to Fucaceae~\cite{bib22}.
Regardless of the field of application, it is important to remember
that the chemical composition of a seaweed species and its extracts is
affected by, among others, the season and location of harvesting
\cite{bib23,bib24,bib25}. These factors must be considered since they
likely influence the biological activities of the commercial products
being manufactured. A general overview of the current uses of the
Fucaceae and Fucaceae-derived products is provided in the following
subsections according to the type of application. In addition,
promising results obtained at a laboratory scale are also presented,
suggesting other potential applications for Fucaceae in the coming
years.



\subsection{Food ingredients and additives}


In some regions of the world, the consumption of seaweed as food has
been, for many centuries, linked mostly to times of hardship, scarcity,
and famine. For instance, during the Irish Great Famine of 1845--1847,
seaweed became the `last resort' for the starving population, and
the Fucaceae \textit{P. canaliculata} was one of the seaweeds used
as a food source~\cite{bib26}. Nowadays, seaweeds are considered
valuable sources of food ingredients due to their content in minerals,
soluble and insoluble dietary fibers, proteins with well-balanced
essential amino acids, and fatty acids, among others. For instance,
\textit{Fucus spp.} are good sources of Na, K, Ca, Mg,
Fe, Cu, Zn, Mn, and I~\cite{bib27,bib28}. In Europe, more than 150
species of algae (i.e., microalgae, cyanobacteria, and seaweeds) are
consumed but only 30 species are approved by the Novel Food regulation
(EU) 2015/2283 for human consumption. Among these 30 species, brown
seaweeds are well represented, and species belonging to Fucaceae,
\textit{A. nodosum}, \textit{F. serratus}, \textit{F. spiralis}, and \textit{F.
vesiculosus} are the ones approved by the Novel Food regulation
\cite{bib22}. Several studies report the use of 
\textit{F.~vesiculosus} and to a lesser extent of \textit{A. nodosum} as
valuable food ingredients or food additives, mostly as a source of
phlorotannins and antioxidants, which prevent food spoilage resulting
from oxidative deterioration. These two families of compounds have
already been incorporated in many food types, as powders in bread or
more often as an aqueous or ethanolic extract in fish, fish-based
products, and dairy products. However, the incorporation of such
seaweed-based ingredients frequently compromises the organoleptic
profile of the final products~\cite{bib29}. Finally, the main food
additives based on brown seaweed are alginates and alginic acids
(E400), used as gelling and thickening agents in many food products.
European seaweeds contribute to 34\% of the world's alginate and
alginic acids supply, and, although it likely only makes up a small
proportion of the overall production (precise data are not available)
in comparison with other brown seaweeds (e.g., \textit{Laminaria
spp.}), \textit{A. nodosum} is one of the species processed by this
industry. Overall, Europe is the top food and pharma-grade alginate
producer in the world~\cite{bib5,bib22,bib29}.



\subsection{Human health and well-being}


The Fucaceae also have many benefits for human health and well-being,
such as specific phenolic compounds (phlorotannins), carotenoids
(fucoxanthin), polysaccharides and iodine~\cite{bib2,bib12,bib27}.
According to recent studies, \textit{A. nodosum}, \textit{F. vesiculosus},
and \textit{Silvetia compressa} extracts may help manage and
prevent metabolic syndrome and related disorders, which could be in
part attributed to prebiotic activities~\cite{bib30,bib31}.
Phlorotannins represent a unique and diverse class of phenolic
compounds exclusive to brown algae and are abundant in the Fucaceae
\cite{bib2}. Phlorotannin contents can reach up to 14\% and 12\% dry
weight in \textit{A. nodosum} and \textit{Fucus
spp.}, respectively~\cite{bib12}. It has been demonstrated
that phlorotannins possess numerous health benefits such as antioxidant
effects, antidiabetic properties, anti-inflammatory effects, and
antitumor properties~\cite{bib12}. Lopes et~al.\ 
have demonstrated that phlorotannin-rich extracts from
\textit{Fucus} species were able to inhibit
carbohydrate-metabolizing enzymes as well as the xanthine oxidase, an
enzyme usually overexpressed in patients with diabetes. These results
are encouraging for the incorporation of phlorotannin-rich extracts in
nutraceuticals or pharmaceuticals for glycemic control and
diabetes-related vascular disorders~\cite{bib32}. Brown seaweeds also
contain a range of polysaccharides (alginate and alginic acids,
fucose-containing sulphated polysaccharides (i.e., fucoidans and
ascophyllan), laminaran, or laminarin), but none of them are specific
to the Fucaceae. In fact, alginate is the predominant polysaccharide
component in the cell walls and intercellular matrix of all species of
brown seaweeds. Fucose-containing sulphated polysaccharides, such as
fucoidans, are also present in many other brown seaweeds, but unlike
alginate, which has a well-defined structure, the chemical structure
and composition of fucoidans depend to a large extent on the different
species in which they are found. For instance, the structure of
fucoidans from two Fucaceae species, \textit{A. nodosum} and
\textit{F. vesiculosus}, is different, illustrating the huge
structural variety of brown seaweed polysaccharides
\cite{bib33,bib34,bib35}. A wide range of beneficial activities are
associated to alginates, fucoidans, and laminarans, such as
antioxidant, antimicrobial, antitumor, anticoagulant, prebiotic,
immunostimulatory, and antidiabetic properties~\cite{bib36}. They are
also used for biomedical applications in biocompatible and
biodegradable materials, such as for wound-healing films (e.g.,
ALGICELL\texttrademark, SeaSorb$^{\text{\textregistered}}$), tissue
engineering, and drug delivery applications~\cite{bib37,bib38}.\looseness=1


\subsection{Cosmetics} 


Brown seaweeds, including the Fucaceae, produce a myriad of bioactive
compounds of interest that are used in cosmetic products as well as in
\mbox{thalassotherapy,} e.g., \textit{Fucus spp.} baths
\cite{bib39,bib40}. Over the last few decades, the ``marine
cosmetics'' industry has developed considerably, with many companies
exploiting the wide range of properties of seaweed, such as
\textit{Fucus spp.} and \textit{A. nodosum} for
``phycocosmetics''~\cite{bib41}. They produce and provide ingredients
for the cosmetics industry or develop their own commercial products
(e.g., NutraMara, R\'{i} Na Mara, Maiiro, Nuwen, Lessonia, Agrimer
cosmetic, Thalion). Alginate is used for its various rheological
properties (gelling agents, thickeners, emulsifiers) as well as for its
bioactivities (antioxidant, anticellulite, anti-inflammatory,
antiphotoaging and moisturizer), which are also described for fucoidans
and laminarans~\cite{bib40}. The phenolic compounds of Fucaceae
(i.e., the aforementioned phlorotannins) are incorporated into
cosmetics as antioxidant, anti-aging/antiwrinkling, anti-allergic,
whitening, or UV protective agents. For example, a recent study
demonstrated higher anti-aging activities of \textit{A. nodosum}
and \textit{F. serratus} fractions enriched in phenolic compounds
compared to the anti-aging activity of the tea flavonol
epigallocatechin gallate, which is a powerful antioxidant already
marketed for its anti-aging properties~\cite{bib42}. Another example
is a phlorotannin-enriched fraction from \textit{F. spiralis},
which exhibited a higher antioxidant ability (DPPH assay) in comparison
with the synthetic standard Butylated Hydroxytoluene (BHT). This
extract also exhibited a strong inhibition of collagenase and elastase
making \textit{F. spiralis} a promising species for dermatological
applications~\cite{bib43}. Finally, over the past ten years, the
safety of synthetic ingredients in cosmetic products has been
questioned. For instance, some synthetic preservatives such as parabens
are controversial. They are suspected to cause skin sensitization,
allergic dermatitis, as well as estrogenic and carcinogenic effects
(breast cancer and malignant melanoma)~\cite{bib44}. Due to their
antifungal and antibacterial activities, phenolic compounds of Fucaceae
are promising alternatives as natural cosmetics preservatives
\cite{bib40,bib45}.


More recently, seaweeds have been gaining attention as ingredients in
``cosmeceuticals'', which are cosmetic products claiming to have
medicinal or drug-like benefits~\cite{bib46}. Indeed, most of the
seaweed components and properties mentioned above for human health are
also valuable for the cosmetic\break industry.


\subsection{Agriculture}

\textit{Ascophyllum nodosum} and to a lesser extent species belonging
to \textit{Fucus} have been used for centuries by farmers from
coastal regions of the northern hemisphere to fertilize agricultural
land. These species are recognized for their rich macro- and
micro-nutrient content, essential for plant growth, making them
biofertilizers of choice. In the last few decades, they have also
been harvested to produce tailored extracts used as biostimulants for
plant growth and increased tolerance to abiotic stresses. These
properties have been linked to their rich content in minerals (e.g.,
potassium), plant hormones (e.g., auxins, cytokinins, and abscisic
acid), osmotic regulators (e.g., glycine betaines), phlorotannins,
bioactive carbohydrates (e.g., alginates, oligosaccharides)
\cite{bib5,bib47,bib48,bib49}. For instance, biostimulants made of
\textit{A. nodosum} extracts demonstrated significant benefits on
wheat, maize, tomato, sweet pepper, and grapevine crops
\cite{bib50,bib51,bib52,bib53,bib54,bib55}. Different companies around
the world, such as Acadian Seaplants Ltd., Maxicrop Ltd., and Timac
Agro have commercialized products derived from \textit{A. nodosum}
extracts~\cite{bib47}. The plant biostimulant market is continuously
growing and, according to some projections, the European demand for
seaweed-based biostimulants is projected to be worth up to
{\texteuro}1.8 billion by 2030~\cite{bib48,bib56}. Recent studies
have also demonstrated that \textit{A. nodosum} extracts could
potentially stimulate plant defenses against biotic stresses and be
used as an alternative to phytosanitary products to fight plant
pathogens like mildew~\cite{bib49,bib57}. These benefits also apply
to seaweed cultivation, which just like vascular plants are subjected
to diseases and epiphyte infestation. Notably, the use of commercial
biostimulants based on \textit{A. nodosum} extracts is being
explored for enhanced growth rate, and mitigation of epiphyte and
endophyte infestations during the cultivation of red seaweeds such as
\textit{Kappaphycus} sp.~\cite{bib58,bib59,bib60}.
However, the benefits of such \textit{A. nodosum}-based
biostimulants need to be further studied as the active compounds might
be dependent on environmental conditions, species and life stage
\cite{bib58,bib61}.


Brown seaweeds, in particular \textit{A. nodosum}, are also widely
used for livestock feed with positive effects on growth performance,
stress and pathogen resistance, and meat quality of the livestock
\cite{bib62}. The rich phenolic compounds in \textit{A. nodosum}
are one of the main factors promoting feed digestibility and animal
health in general. The \textit{A. nodosum}-based
Tasco$^{\text{\textregistered}}$ product from Acadian
Seaplants is one example of this~\cite{bib45}. Such effects have been
demonstrated in pigs~\cite{bib63,bib64} as well as poultry
\cite{bib65}, making animal feed a most promising short-term market
for seaweed use in Europe as it is projected to reach up to
{\texteuro}2.2 billion by 2030~\cite{bib56}. Finally, the aquaculture
industry is also an important market as it generates up to 50\% of the
world's fish production for human consumption. Here too, extracts of
Fucaceae, especially those from \textit{A. nodosum}, are promising
for the production of natural feed additive owing to their
antibacterial, antifungal, antibiotic, antioxidant activities and
phenolic compounds which could also be used as a natural cross-linker
for aquaculture food delivery systems, for examples as fish oil
microencapsulation~\cite{bib66,bib67,bib68}.



\subsection{Biomass availability and sustainability}


To sustain the growing demand for Fucaceae biomass of these different
markets, its source must be abundant and renewable. Countries
exploiting wild seaweed off the Atlantic coast have different
management practices according to the species being harvested 
\cite{bib5}. Even though the harvesting of \textit{A. nodosum} has
been considered to be economically sustainable for centuries in
Northern Europe, there are recent concerns about its environmental
impacts. A recent study recommended avoiding harvesting \textit{A.
nodosum} from the wild in Portugal because of the vulnerability and
ecological importance of this southernmost population in Europe
\cite{bib69}. In Eastern Canada, where the commercial exploitation of
\textit{A. nodosum} began in the late 1950s, studies evaluating the
impact of harvesting and management over 25 years concluded that
\textit{A. nodosum} harvesting is sustainable in this area, however
it needs to be closely monitored as environmental conditions are
changing~\cite{bib7,bib70,bib71}. In Alaska, the harvesting of
\textit{Fucus distichus} is also considered sustainable due to a
tailored management plan which takes into account the timing of
reproduction, the available biomass, and regrowth~\cite{bib72}. In
Europe, the harvesting of \textit{Fucus spp.} from wild
populations is permitted in some countries (i.e., Ireland, France) and
prohibited in others (i.e., Germany)~\cite{bib73}. In the future,
regardless of the Fucaceae species, local harvesting and monitoring
practices should be adapted to ensure sustainable management of wild
resources to avoid overharvesting at a global scale
\cite{bib7,bib69,bib70,bib71} and it may become necessary to
investigate different strategies for Fucaceae cultivation in coastal
and/or offshore waters~\cite{bib5,bib73}. 



\section{Seaweed and their microbiota, a complex holobiont}\label{sec3}

We believe that the microbiota of Fucaceae may contribute to finding
suitable responses to a sustainable commercial exploitation of these
seaweed species. As reviewed below, the Fucaceae microbiota is complex
and may contribute significantly to the health of the host alga but
also its chemical composition including the production of bioactive
compounds. A better understanding of the Fucaceae microbiota could lead
to the development of alternative production methods of compounds of
interest, for instance by directly synthesizing and/or producing the
compounds of interest from microbial culture.


Seaweed-associated microbiota have been studied from various
scientific perspectives and has revealed dynamic interactions between
symbionts and hosts. The bacterial composition of seaweed microbiota
has been shown to vary in terms of diversity and abundance,
according to host species~\cite{bib74,bib75,bib76}, and even
within the same species depending on host tissue type, age, health, and
host morphology
\cite{bib76,bib77,bib78,bib79,bib80,bib81,bib82,bib83,bib84,bib85,bib86}.
Furthermore, the environment plays a crucial role in microbial
composition and dynamics. For instance, spatial and temporal
differences~\cite{bib74,bib81,bib82,bib87,bib88}, as well as
temperature and salinity variations~\cite{bib89,bib90,bib91},
latitude \cite{bib92}, and ocean warming have been shown to influence
the microbiota of seaweeds~\cite{bib88}. Finally, the composition of
the microbiota differs profoundly from the surrounding water. Microbes
form diverse biofilms on the surface of the seaweeds, which constitutes
a highly selective habitat
\cite{bib74,bib76,bib78,bib83,bib92,bib93,bib94,bib95}.


As we acquire more information on the composition of seaweed-associated
microbiota, whether it is bacterial, fungal, or other, we also
gradually increase our awareness of the intricate interactions that
likely exist between algal hosts and their microbiota, as well as
between the different members of the microbiota. Seaweeds provide a
favorable environment for the proliferation of microorganisms and the
formation of biofilms, notably due to the presence of carbon-rich
constituents in their cell wall. These constituents serve as sources of
nutrients for members of the
microbiota~\cite{bib19,bib20,bib96,bib97,bib98,bib99,bib100}. On
the other hand, seaweeds may impede microbial growth and biofilm
formation through various mechanisms. Several brown seaweeds have, for
instance, been shown to react to elicitation with oligoguluronates
(oligosaccharides liberated during brown algal cell-wall degradation
that are perceived as signal), through oxidative bursts which could
serve as an algal defense against bacteria or other colonizers
\cite{bib101,bib102}. In this regard, the release of specific organic
compounds, such as halogenated or phenolics-related compounds, is
noteworthy, given that certain species of kelp (e.g.,
\textit{Nereocystis}, \textit{Macrocystis}, \textit{Laminaria},
\textit{Saccharina}) are known to feature a unique iodine-based defense
metabolism~\cite{bib103} and phlorotannins present in the Fucales
exhibiting antimicrobial properties~\cite{bib104}. To date, only
partial information exists on the response of bacteria to particular
algal defense compounds, such as in the model bacterium
\textit{Zobellia galactanivorans}, where L-2-haloacid dehalogenases
have been shown to increase bacterial tolerance to haloacetic acids
\cite{bib105}. One hypothesis~is that the selective pressure and the
resulting stability of associations have enabled the evolution of
stable, mutually beneficial interactions between hosts and their
microbiota. Several prominent model systems demonstrate the extent and
capacity of seaweed-dependent microbiota in all major algal lineages.
For instance, the green alga \textit{Ulva compressa} requires at least
two growth hormones from its bacterial symbionts---thallusin and a yet
unknown compound---to reach its normal growth and
morphology~\cite{bib106}. The red alga \textit{Delisea pulchra} is a
model system to study the emergence of dysbiosis in the algal biofilm,
but recent work has also shown that some members of the microbiota,
such as \textit{Phaeobacter} sp.\ BS52, may provide protection against
dysbiosis-related changes in the microbiota~\cite{bib107}. Lastly, in
the brown alga \textit{Ectocarpus subulatus}, the bacterial community
is essential during host acclimation to low salinity~\cite{bib90}.
Metatranscriptomic analyses suggest that the provision of vitamins
essential for growth and the regulation of dysbiotic behavior in the
bacterial community may be two important features explaining this
\cite{bib108}. Well-studied cases such as these are still an exception
in seaweeds, but it is plausible that such interactions are widespread
among multicellular eukaryotes and their \mbox{associated} microbiota. Despite
criticisms of the term due to the challenge of experimentally
demonstrating co-evolution and co-adaptation~\cite{bib109}, the
significance of host--microbiota interactions in most model systems is
now widely acknowledged.

Among seaweeds, Fucaceae are interesting in terms of their microbiota
because several species of this family are consistently associated with
endophytic fungi (see below for more details). Despite initial
groundbreaking research and recent heightened scientific interest in
the broader topic of host--microbe interactions, there are
still extensive gaps in our knowledge of the Fucaceae microbiota and
its interactions with its hosts. In the following section, we will
summarize the data currently available in this field and highlight key
gaps and challenges toward generating a holistic understanding of these
associations.


\subsection{The bacterial composition of Fucaceae holobionts}

Bacteria, comprising both epi- and endobacterial communities, are an
important component of the Fucaceae microbiota. Most information is
currently available for the genus \textit{Fucus} and especially for
\textit{F. vesiculosus} (Table~\ref{tab2}). In addition to
environmental factors affecting microbial \textit{Fucus spp.}
communities~\cite{bib76,bib87,bib89,bib92,bib110,bib111}, Parrot
et~al.~\cite{bib83} also described variations in the bacterial
communities according to different thallus parts of  the host. 

\begin{sidewaystable*}
\vsptwo
\caption{\label{tab2}Description of bacterial diversity of the Fucaceae from the
literature. Only the most abundant taxa are reported} 
\fontsize{7.3}{8.8}\selectfont
\tabcolsep=1pt
\begin{tabular}{ccccccccc}
\thead
Algae & Phylum & Class & Family & Genus & Approach & Host localization & Zone & Ref \\
\endthead
\morerows{4}{\parbox[t]{1.6cm}{\centering\textit{Ascophyllum nodosum}}}  & 
\parbox[t]{2.3cm}{\centering Firmicutes, 
Actinobacteria, 
Proteobacteria, 
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Bacilli, Actinomycetes,  
Gammaproteobacteria,} & 
\parbox[t]{2.9cm}{\centering Bacillaceaea,  
Nocardiaceae, 
Oceanospirillaceae} & 
\parbox[t]{3cm}{\centering \textit{Bacillus}, 
\textit{Rhodococcus}, 
\textit{Cobetia}, 
\textit{Pseudoalteromonas}} & 
Cultivable & Endophyte &
\parbox[t]{2cm}{\centering Roscoff, France and Oban, Scotland} &
\cite{bib117} 
\vspace*{6pt}\\
 & \parbox[t]{2.3cm}{\centering Proteobacteria, 
Bacteroidetes, 
Firmicutes} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria,  
Gammaproteobacteria  
Betaproteobacteria,  
Flavobacteriia} & 
\parbox[t]{2.9cm}{\centering Flavobacteriaceae,  
Oceanospirillaceae,  
Rhodobacteraceae} & 
\parbox[t]{3cm}{\centering \textit{Cobetia},  
\textit{Marinomonas},  
\textit{Pseudoalteromonas},  
\textit{Cellulophaga}} & 
Cultivable & Epiphyte & 
\parbox[t]{2cm}{\centering Roscoff, France} & 
\cite{bib75} 
\vspace*{6pt}\\
 & \parbox[t]{2.3cm}{\centering Proteobacteria, 
Bacteroidetes,  
Actinobacteria} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria, 
Bacteroidota,} & 
\parbox[t]{2.9cm}{\centering Flavobacteriaceae,  
Alteromonadaceae,  
Microbacteriaceae,  
Micrococcaceae} & 
\parbox[t]{3cm}{\centering\textit{Winogradskyella}, 
\textit{Marinobacter Microbacterium},  
\textit{Micrococcus}} & 
Cultivable & Epiphyte & 
\parbox[t]{2cm}{\centering Galway Bay, Ireland} & 
\cite{bib115} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria,  
Firmicutes,  
Bacteroidota,  
Cyanobacteria} &  &  &  & 
Metabarcoding & 
Epiphyte & 
\parbox[t]{2cm}{\centering Kerry, Ireland} & 
\cite{bib116}
\vspace*{6pt}\\
 & \parbox[t]{2.3cm}{\centering Proteobacteria,  
Planctomycetes,  
Actinobacteria,  
Verrucomicrobia,  
Cyanobacteria, 
Bacteroidetes,  
Firmicutes} &  &  &  & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering Galway Bay, Ireland} & 
\cite{bib115} 
\vspace*{6pt}\\
\morerows{5}{\parbox[t]{1.6cm}{\centering\textit{Fucus vesiculosus}}}  & 
\parbox[t]{2.3cm}{\centering Proteobacteria, 
Bacteroidetes,  
Verrucomicrobia,  
Cyanobacteria} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria, 
Alphaproteobacteria,}
&  &  & 
\parbox[t]{1.7cm}{\centering DGGE $+$ Metabarcoding} & Epiphyte & 
\parbox[t]{2cm}{\centering Kiel fjord} & 
\cite{bib87} 
\vspace*{6pt}\\
 & \parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes,  
Cyanobacteria,} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria,  
Gammaproteobacteria,  
Deltaproteobacteria}
&  &  & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering Kiel fjord} & 
\cite{bib120} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria,  
Flavobacteriia,  
Saprospiria} & 
\parbox[t]{2.9cm}{\centering Rhodobacteraceae,  
Flavobacteriaceae,  
Saprospiraceaea} &  & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering Kiel Bight, Western Baltic} & 
\cite{bib89} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria,  
Gammaproteobacteria,  
Flavobacteriia,  
Saprospiria} & 
\parbox[t]{2.9cm}{\centering Rhodobacteriaceae,  
Flavobacteriaceae, 
Saprospiraceaea} &  & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering Kiel Fjord} & 
\cite{bib118} 
\vspace*{6pt} \\
\tabtwosplittabular
 & \parbox[t]{2.3cm}{\centering Actinobacteria,  
Bacteroidetes,  
Firmicutes,  
Proteobacteria} & 
\parbox[t]{3.3cm}{\centering Flavobacteria, 
Bacilli,  
Actinobacteria,  
Alphaproteobacteria,  
Gammaproteobacteria,} &  &  & 
Cultivable & Epiphyte & 
\parbox[t]{2cm}{\centering Western Baltic Sea, Germany} & 
\cite{bib110} 
\vspace*{6pt}\\
 & \parbox[t]{2.3cm}{\centering Proteobacteria,  
Planctomycetota} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria, 
Planctomycetia, 
unclassified} & 
\parbox[t]{2.9cm}{\centering Rhodobacteraceae,  
Erythobacteraceaea, 
Hyphomonadaceaea} & 
\parbox[t]{3cm}{\centering \textit{Erythrobacter}, 
\textit{Altererythrobacter}, 
\textit{Roseobacter}} & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering B\"{u}lker Leuchtturm} & 
\cite{bib121} 
\vspace*{6pt}\\
\morerows{2}{\parbox[t]{1.6cm}{\centering \textit{Fucus vesiculosus}}}  & 
\parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes,  
Actinobacteria,  
Cyanobacteria} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria, 
Gammaproteobacteria,  
Flavobacteriia,  
Saprospirae,  
Actinobacteria} &  &  & 
Metabarcoding & Epiphyte & 
Baltic & 
\cite{bib88} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes,  
Verrucomicrobia} & 
\parbox[t]{3.3cm}{\centering Alphaproteobacteria,  
Gammaproteobacteria,  
Bacteroidia} & 
\parbox[t]{2.9cm}{\centering Rhodobacteraceae,  
Burkholderiaceae,  
Thiohalorhabdaceae,} & 
\parbox[t]{3cm}{\centering\textit{Granulosiccocus},  
\textit{Rubritalea},  
\textit{Rhodobacteraceaea\_NA},  
\textit{Pleurocapsa},  
\textit{Litorimonas},  
\textit{Blastopirellula}} & 
Metabarcoding & Mixed & 
\parbox[t]{2cm}{\centering Western and Eastern Atlantic Ocean} & 
\cite{bib92} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria,  
Bacteroidia,  
Alphaproteobacteria} &  &  & 
Metabarcoding & Mixed & 
\parbox[t]{2cm}{\centering Acadia National Park, United States} & 
\cite{bib76} 
\vspace*{6pt}\\ 
\morerows{1}{\parbox[t]{1.6cm}{\centering\textit{Fucus distichus}}} & 
\parbox[t]{2.3cm}{\centering Bacteroidota,  
Proteobacteria, 
Verrucomicrobia,} & 
\parbox[t]{3.3cm}{\centering Flavobacteriales, 
Alphaproteobacteria, 
Verrucomicrobiae, 
Saprospiria,  
Gammaproteobacteria} & 
\parbox[t]{2.9cm}{\centering Flavobacteriaceae,  
Rhodobacteraceae,  
Rubritaleaceae,  
Saprospiraceae, 
Thiohalorhabdaceae} &  & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering Calvert Island, British Columbia, Canada} & 
\cite{bib111} 
\vspace*{6pt}\\ 
 & \parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria, 
Bacteroidia, 
Alphaproteobacteria} &  &  & 
Metabarcoding & Mixed & 
\parbox[t]{2cm}{\centering Acadia National Park, United States} & 
\cite{bib76} 
\vspace*{6pt}\\ 
%\tabtwosplittabular
\morerows{1}{\parbox[t]{1.6cm}{\centering\textit{Fucus spiralis}}}  & 
\parbox[t]{2.3cm}{\centering Proteobacteria,  
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria,  
Alphaproteobacteria, 
Flavobacteriia,  
Sphingobacteriia} & 
\parbox[t]{2.9cm}{\centering Rhodobacteraceae,  
Halomonadaceae,  
Flavobacteriaceae} & 
\parbox[t]{3cm}{\centering\textit{Sulfitobacter}, 
\textit{Loktanella},  
\textit{Octadecabacter}} & 
Metabarcoding & Epiphyte & 
\parbox[t]{2cm}{\centering North Sea, Germany} & 
\cite{bib119} 
\vspace*{6pt}\\
& \parbox[t]{2.3cm}{\centering Proteobacteria, 
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria, 
Bacteroidia,  
Alphaproteobacteria} &  &  & 
Metabarcoding & Mixed & 
\parbox[t]{2cm}{\centering Acadia National Park, United States} & 
\cite{bib76} 
\vspace*{6pt}\\
\parbox[t]{1.6cm}{\centering\textit{Pelvetia canaliculata}} & 
\parbox[t]{2.3cm}{\centering Proteobacteria,  
Actinobacteria,  
Firmicutes,  
Bacteroidetes} & 
\parbox[t]{3.3cm}{\centering Gammaproteobacteria, 
Actinomycetes,  
Bacilli} & 
\parbox[t]{2.9cm}{\centering Pseudoalteromonadaceae,  
Nocardiaceae,  
Bacillaceaea,  
Oceanospirillaceae} & 
\parbox[t]{3cm}{\centering\textit{Pseudoalteromonas},  
\textit{Rhodococcus},  
\textit{Bacillus},  
\textit{Cobetia}} &
Cultivable & Endophyte & 
\parbox[t]{2cm}{\centering Roscoff, France and Oban, Scotland} & 
\cite{bib117} \vspace*{2pt}
\botline
\end{tabular}
\end{sidewaystable*}

The bacterial population of \textit{A. nodosum} was studied long
time ago by lab-based culturing~\cite{bib112} and electronic
microscopy~\cite{bib113}. Following this, coculture experiments in
axenic conditions with the endophytic fungus \textit{Mycophycias
ascophylli} suggested that bacteria protect \textit{A. nodosum}
from being digested by this fungus~\cite{bib114}. After a long gap,
the bacterial composition of \textit{A. nodosum} was further
described in 2015, but few studies are available to date. Two of them
\cite{bib115,bib116} describe the changes in the epibacterial
communities in response to stress, while two others focused on the
cultivable bacteria: Martin et~al.~\cite{bib75} describe the
polysaccharide-degrading activity of surface-attached bacteria, and
Tourneroche et~al.~\cite{bib117} sought to understand the role of
endobacteria in the quorum-sensing system. This latter study also
examined the cultivable microbiota of \textit{P. canaliculata},
constituting the only microbiota study in this genus so far
\cite{bib117}. To our knowledge, as of today, no microbial
analyses exist for \textit{Pelvetiopsis}, \textit{Silvetia}, and
\textit{Hesperophycus}.


A common point of the above studies was that
\textit{Proteobacteria} and \textit{Bacteroidetes} were
abundant. Furthermore, \textit{Firmicutes} and
\textit{Actinobacteria} were detected in six studies. One common
point among some of these studies is that the presence of several
members of the \textit{Rhodobacteraceae} was positively correlated
to abiotic stressors in the environment
\cite{bib78,bib88,bib89,bib118,bib119}. However, given the low
number of currently available datasets, it is difficult to conclude on
general trends, such as the recurring presence of core genera
systematically associated with Fucaceae. This would require sampling a
broader range of species and conditions and consistent taxonomic
assignment based on the same databases at the genus level. As
previously reported in green algae~\cite{bib93}, it is also likely
that there is a core set of bacterial functions consistently associated
with the microbiome despite profound taxonomic variability. Yet, this
can only be assessed to a limited extent based on 16S rRNA gene
metabarcoding data. Exploring these functions would require researchers
to include metagenomic approaches to complement metabarcoding
approaches and to provide genomic data for the uncultivable components
of the microbiota. Thus, even though the bacterial compartment is
arguably the best-studied part of the Fucaceae microbiota, much
research is still required to obtain a comprehensive picture.

\subsection{Fungal composition of Fucaceae holobionts}

Microscopic fungi asymptomatically colonize the tissues of healthy
seaweed. These algicolous fungi produce bioactive metabolites that are
able to kill pathogens or exhibit potent quorum-quenching abilities
\cite{bib117}, suggesting that their functions in the host might be
based on chemical signaling~\cite{bib122}.

The best-known symbiotic associations between Fucaceae and fungi have
been described in \textit{A. nodosum}. This seaweed hosts large
symbiotic communities including the fungus \textit{Mycophycias
ascophylli} belonging to Mycosphaerellaceae family (formerly
\textit{Mycosphaerella ascophylli} Cotton)
\cite{bib123,bib124,bib125,bib126,bib127}. This latter association was
previously designated as a mycophycobiosis by Kohlmeyer and Kohlmeyer
\cite{bib127} and was renamed by Garbary and Deckert as a
\mbox{``symbiotum''~\cite{bib125},} a term describing the relationship between
a photobiont and a mutualistic endophytic fungus \cite{bib128}. This
fungus is also present in the related Fucaceae \textit{P. caniculata}
(L.) and both brown seaweeds do not occur naturally without this
symbiotic fungus~\cite{bib126}. Observations with light microscopy show
that fungal hyphae are strongly attached to seaweed cell
walls~\cite{bib129}. Their greatest concentration has been observed in
receptacles, followed by plant apices, the main axis, and the
holdfast~\cite{bib95} and their abundance depends on the maturity of
tissue. Reproduction of the mycobiont occurs at the same time as
reproduction of the host~\cite{bib125}. \textit{Mycophycias ascophylli}
has been shown to impact host development, fitness and protection
against desiccation. It also secretes compounds that may deter
herbivores, increase the width of the thallus, and modify host
physiology under stressful environments by developing rhizoids for
better attachment to substrates~\cite{bib131,bib132,bib133}. These
observations suggest potential interest of some compounds produced by
this fungus for plant protection against abiotic stress. At present,
there are no ITS (Internal Transcribed Spacer) rDNA sequences available
for \textit{M. ascophylli} in GenBank or UNITE databases \cite{bib134}
but a partial sequence of the Large Subunit 28S rRNA gene is available
in the NBCI database~\cite{bib135}. More recently, Vallet
et~al.~\cite{bib122} isolated a similar fungus from \textit{A. nodosum}
and identified it as a member of the Sordariomycete class related to
\textit{Moheitopora} sp. This taxon was also identified in a recent
study exploring the diversity of fungal endophytes in \textit{P.
caniculata}~\cite{bib134}. 


Beyond this particular example, a number of studies have established
fungal cultures from other Fucaceae and revealed a wide diversity of
symbionts (Table~\ref{tab3}): eight strains were identified in \textit{P.
canaliculata}~\cite{bib122,bib126,bib134}, 46 in \textit{F. serratus}
\cite{bib136,bib137,bib138}, 32 in \textit{F.~vesiculosus}
\cite{bib121,bib137,bib139,bib140}, one in \textit{F. spiralis}
\cite{bib137}), 18 in \textit{A. nodosum}
\cite{bib122,bib126,bib137}, and 21 in unidentified species of
\textit{Fucus}~\cite{bib140,bib141}. Among these 126 fungal strains,
most of them belong to Ascomycota (95\%) and only a few to Mucoromycota
(2.5\%) and Basidiomycota (2.5\%). The Ascomycota community, in turn,
is equally dominated by Dothideomycetes (35\%) and Sordariomycetes
(34.2\%), followed by Eurotiomycetes (22.5\%) and Leothiomycetes
(5.8\%). The use of CARD-FISH to study the tissue of \textit{F.
vesiculosus} also revealed a positive signal for fungi belonging to
the class Eurotiomycetes~\cite{bib118}. The majority of these studies
have concentrated on characterizing the endophytic algicolous fungi
associated with different species of \textit{Fucus spp.}\looseness=-1


\begin{sidewaystable*}[p!]
\vspthree
\caption{\label{tab3}Description of fungal diversity of Fucaceae from the literature}
\fontsize{7.1}{8.6}\selectfont
\tabcolsep=4pt
\begin{tabular}{cccccc}
\thead
Seaweed & 
\parbox[t]{11cm}{\centering Taxonomy (p\_phylum;c\_class;f\_family;g\_genus;s\_species)} &
Approach & Host localization & Zone & Ref \\
\endthead 
\morerows{2}{\parbox[t]{1.8cm}{\centering\textit{Pelvetia canaliculata}}}  &
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium};s\_\textit{cladosporioides}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Didymellaceae;g\_\textit{Didymella};s\_\textit{exigua}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Alternaria};s\_\textit{metachromatica}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Stemphylium};s\_\textit{vesicarium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreomycetidae;g\_\textit{Acremonium};s\_\textit{exuvarium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Chlamydocillium};s\_\textit{cyanophilum}} & 
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering Wenbry, Devon, UK} & 
\cite{bib142} 
\vspace*{6pt}\\
& \parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Mycosphaerellaceae;g\_\textit{Mycosphaerella};s\_\textit{ascophylli}} & 
Cultivable &  Endo &
\parbox[t]{2.1cm}{\centering College Rocks, Aberystwyth, UK} & 
\cite{bib126} 
\vspace*{6pt}\\
& \parbox[t]{11cm}{\raggedright   p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Paradendryphiella};s\_\textit{arenariae}} & 
Cultivable & Endo & 
\parbox[t]{2.1cm}{\centering Oban, Scotland, UK} &
\cite{bib122} 
\vspace*{6pt}\\
\parbox[t]{1.8cm}{\centering\textit{Ascophyllum nodosum}} &
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Agaricomycetes;f\_Polyporaceae;g\_\textit{Trametes};s\_\textit{versicolor}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium};s\_\textit{cucumerinum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Paradendryphiella};s\_\textit{arenariae}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Phaeosphaeriaceae;g\_\textit{Phaeosphaeria}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Thyridariaceae;g\_\textit{Roussoella}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_;g\_\textit{Exosporium};s\_\textit{stylobatum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{brevicompactum}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Sclerotiniaceae;g\_\textit{Botryotinia};s\_\textit{fuckeliana}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Plectosphaerellaceae;g\_\textit{Verticillium} ;s\_cf \textit{biguttatum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Xylariaceae;g\_\textit{Brunneiperidium};s\_\textit{gracilentum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Moheitospora}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Microsphaeropsidaceae;g\_\textit{Microsphaeropsis};s\_\textit{olivacea}} & 
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering Roscoff, France \& Oban, Scotland, UK} & 
\cite{bib122} 
\vspace*{6pt}\\ 
\parbox[t]{1.8cm}{\centering\textit{Fucus spiralis}} &
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Dictyosporiaceae;g\_\textit{Dendryphiella};s\_\textit{salina}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus} ;s\_\textit{fumigatus}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus}\break 
p\_Mucoromycota;c\_Mucoromycetes;f\_Lichtheimiaceae;g\_\textit{Lichtheimia};s\_\textit{corymbifera}} & 
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering West Burra, Shetland Islands, UK \&  Etete, New Brunswick, Canada} & 
\cite{bib137} 
\vspace*{6pt}\\
\tabthreesplittabular
\morerows{2}{\parbox[t]{1.8cm}{\centering\textit{Fucus serratus}}} &
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Mycosphaerellaceae;g\_\textit{Mycosphaerella};s\_\textit{ascophylli}} & 
Cultivable & Endo & 
\parbox[t]{2.1cm}{\centering College Rocks, Aberystwyth, UK} & 
\cite{bib126} 
\vspace*{6pt}\\
& \parbox[t]{11cm}{\raggedright   p\_Ascomycota;c\_Ascomycetes;f\_Myxotrichaceae;g\_\textit{Oidiodendron}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Acroconidiella}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Coniothyriaceae;g\_\textit{Coniothyrium}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Dictyosporiaceae;g\_\textit{Dendryphiella};s\_\textit{salina}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Didymellaceae;g\_\textit{Epicoccum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Mycospaerellaceae;g\_\textit{Mycosphaerella}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Periconiaceae;g\_\textit{Periconia}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Alternaria}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_;g\_\textit{Phoma}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Herpotrchiellaceae;g\_\textit{Phialophora}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Thermoascaceae;g\_\textit{Paecilomyces}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Sclerotiniaceae;g\_\textit{Botrytis};s\_\textit{cinerea}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Apiosporaceae;g\_\textit{Arthrinium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Chaetomiaceae;g\_\textit{Chaetomium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Chaetomiaceae;g\_\textit{Humicola};s\_\textit{fuscoatra}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Halosphaeriaceae;g\_\textit{Corollospora};s\_\textit{angusta}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreaceae;g\_\textit{Trichoderma}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Acremonium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Emericellopsis};s\_\textit{minima}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Nectriaceae;g\_\textit{Fusarium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Microascaceae;g\_\textit{Scopulariopsis}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Plectosphaerellaceae;g\_\textit{Verticillium};s\_\textit{cinnabarinum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Xylariaceae;g\_\textit{Nodulisporium}\break 
p\_Mucoromycota;c\_Mucoromycetes;f\_Mucoraceae;g\_\textit{Mucor}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Didymellaceae;g\_\textit{Epicoccum};s\_\textit{purpurascens}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Dematiaceae;g\_\textit{Asteromyces};s\_\textit{cruciatus}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Pseudeurotiaceae;g\_\textit{Geomyces}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_;g\_\textit{Tetracladium};s\_\textit{maxilliformis}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Chaetomiaceae;g\_\textit{Chaetomium};s\_\textit{funicola}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Diaporthaceae;g\_\textit{Phomopsis}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Halosphaeriaceae;g\_\textit{Corollospora};s\_\textit{intermedia}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Halosphaeriaceae;g\_\textit{Sigmoidea};s\_\textit{marina}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreaceae;g\_\textit{Gliocladium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Acremonium};s\_\textit{mumorum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Acremonium};s\_\textit{tubakii}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Acremonium};s\_\textit{fuci}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Lulworthiaceae;g\_\textit{Lindra};s\_\textit{obtusa}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Microascaceae;g\_\textit{Microascus}} &
Cultivable & Mixed & 
\parbox[t]{2.1cm}{\centering Heligoland Island, Germany} & 
\cite{bib138} 
\vspace*{6pt}\\
\tabthreesplittabular
& \parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Coniothyriaceae;g\_\textit{Coniothyrium}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus} ;s\_\textit{fumigatus}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium}} &
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering West Burra, Shetland Islands, UK} & 
\cite{bib137} 
\vspace*{6pt}\\
\morerows{5}{\parbox[t]{1.8cm}{\centering\textit{Fucus vesiculosus}}}  & 
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_;g\_\textit{Phoma}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{chrysogenum}} &
Cultivable &  Epi &
\parbox[t]{2.1cm}{\centering Kiel Fjord, Baltic Sea, Germany} & 
\cite{bib121} 
\vspace*{6pt}\\
& \parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Pyrenochaetopsidaceae;g\_\textit{Pyrenochaetopsis}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{atrovenetum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{biourgeianum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{canescens}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{glabrum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{sanguifluum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{spathulatum}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Ploettnerulaceae;g\_\textit{Cadophora};s\_\textit{malorum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Acremonium};s\_\textit{furcatum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Stilbella};s\_\textit{fimeteria}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreaceae;g\_\textit{Trichoderma};s\_\textit{gamsii}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreaceae;g\_\textit{Trichoderma};s\_\textit{paraviridescens}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Nectriaceae;g\_\textit{Fusarium};s\_\textit{graminearum}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Plectosphaerellaceae;g\_\textit{Gibellulopsis}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Plectosphaerellaceae;g\_\textit{Gibellulopsis};s\_\textit{nigrescens}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Emericellopsis}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_;g\_\textit{Emericellopsis};s\_\textit{terricola}\break 
p\_Ascomycota;c\_Wallemiomycetes;f\_Wallemiaceae;g\_\textit{Wallemia};s\_\textit{muriae}} &
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering Kiel Fjord, Baltic Sea, Germany} & 
\cite{bib121} 
\vspace*{6pt}\\
&\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{brevicompactum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{coralligerum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium}} &
Cultivable & Mixed &
\parbox[t]{2.1cm}{\centering Kiel Fjord, Baltic Sea, Germany} & 
\cite{bib121} 
\vspace*{6pt}\\
&\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus} ;s\_\textit{fumigatus}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium}\break 
p\_Ascomycota;c\_Leotiomyctes;f\_Pezizellaceae;g\_\textit{Chalara}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Alternaria}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Coniothyriaceae;g\_\textit{Coniothyrium}} &
Cultivable & Endo & 
\parbox[t]{2.1cm}{\centering West Burra, Shetland Islands, UK} & 
\cite{bib137} 
\vspace*{6pt}\\
& \parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Dendryphiella};s\_\textit{salina}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_;g\_\textit{Phoma}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Ophiocordycipitaceae;g\_\textit{Tolypcladium};s\_\textit{inflatum}} & 
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering Lulworth Coast, UK \&  Cuxhaven, Germany} & 
\cite{bib140} 
\vspace*{6pt}\\
&\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Didymellaceae;g\_\textit{Epicoccum}} &
Cultivable & Endo & 
\parbox[t]{2.1cm}{\centering T\"{o}nning, Germany} & 
\cite{bib139} 
\vspace*{6pt}\\
\tabthreesplittabular
\morerows{1}{\parbox[t]{1.8cm}{\centering\textit{Fucus} sp.}}  & 
\parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium};s\_\textit{europaeum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium};s\_\textit{ramotenellum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium};s\_\textit{sphaerospermum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Cladosporiaceae;g\_\textit{Cladosporium}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Didymellaceae;g\_\textit{Epicoccum};s\_\textit{nigrum}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Alternaria}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Aspergillus}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium};s\_\textit{brevicompactum}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Aspergillaceae;g\_\textit{Penicillium}\break 
p\_Ascomycota;c\_Eurotiomycetes;f\_Herpotrichiellaceae;g\_\textit{Exophiala}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Bionectriaceae;g\_\textit{Clonostachys};s\_\textit{rosea}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Cordycipitaceae;g\_\textit{Engyodontium}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Hypocreaceae;g\_\textit{Trichoderma};s\_\textit{paraviridescens}\break 
p\_Basidiomycota;c\_Cystobasidiomycetes;f\_Symmetrosporaceae;g\_\textit{Symmetrospora}\break 
p\_Basidiomycota;c\_Microbotryomycetes;f\_;g\_\textit{Leucosporidium}\break 
p\_Basidiomycota;c\_Tremellomycetes;f\_Cryptococcaceae;g\_\textit{Cryptococcus}\break 
p\_Mucoromycota;c\_Mucoromycetes;f\_Mucoraceae;g\_\textit{Rhizopus};s\_\textit{orysae}} & 
Cultivable & Mixed & 
\parbox[t]{2.1cm}{\centering Scheveningen, Netherlands} & 
\cite{bib141} 
\vspace*{6pt}\\
 & \parbox[t]{11cm}{\raggedright  p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Dendryphiella};s\_\textit{arenariae}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_Pleosporaceae;g\_\textit{Dendryphiella};s\_\textit{salina}\break 
p\_Ascomycota;c\_Dothideomycetes;f\_;g\_\textit{Phoma}\break 
p\_Ascomycota;c\_Sordariomycetes;f\_Apiosporaceae;g\_\textit{Arthrinium}} & 
Cultivable & Endo &
\parbox[t]{2.1cm}{\centering Lulworth Coast, UK \& T\"{o}nning, Travem\"{u}nde,  Cuxhaven, Germany} & 
\cite{bib140} 
\botline
\end{tabular}
\end{sidewaystable*}

To date, only two studies have explored the non-cultivable fungal
diversity of Fucaceae by DNA fingerprinting methods
\cite{bib134,bib138}. The fungal endophytes of \textit{P. canaliculata}
are mainly composed of Ascomycota, including one abundant unclassified
Amplicon Sequence Variant (ASV), and of Basiodiomycota. In other
studies of the \textit{P. canaliculata}- or \textit{A.
nodosum}-associated microbiota, the endophyte \textit{M. ascophylli}
remained unidentified either in culture or in fungal NGS
databases~\cite{bib134}. The identity of fungi colonizing \textit{F.
serratus} has been explored through Denaturing Gradient Gel
Electrophoresis (DGGE) analysis. These studies indicate that
understanding the ecological role and deciphering the core fungal
composition in seaweeds is challenged by a lack of knowledge of the
non-cultivable fungal diversity. Indeed, there is a limited amount of
available reference ITS rDNA sequences of fungal taxa from marine
environments. There is thus an urgent need for the development of
culture collections, the description of new species, and the sequencing
of specimens, particularly those that are not amenable to culture. The
development of new tools such as Mass Imaging Spectrometry (MIS)
associated with CARD-FISH are also useful to further investigate the
fungal diversity associated with its metabolic potential and to
decipher the molecular interactions involved in seaweed--fungal\break
symbiosis.


\subsection{Archaeal and viral community associated with Fucaceae: the
great unknown}

Unlike fungi and bacteria, to date no study on the archaeal or viral
partners of the Fucaceae holobiont is available in the literature, but
this does not indicate their absence or a lack of importance. While
archaea were initially discovered in extreme environments, we now know
that they are widely distributed in marine environments
\cite{bib143}. Among the four phylogenetic groups (i.e., the
Euryarchaeota phylum and the TACK, Asgardarchaeota, and DPANN
superphyla), archaea of the DPANN superphylum are commonly found living
in symbiosis, frequently with other archaea or bacteria
\cite{bib144}. However, most metabarcoding studies examining
alga-associated microbiota (see above) use bacteria-biased primers and
remove any sequences potentially resembling archaea during the usual
assembly pipeline although suitable generic primers now exist
\cite{bib145}. Even when looking beyond the Fucaceae to other brown
algae, archaeal diversity on brown algae has so far only been examined
in one study. Trias et~al.~\cite{bib146} used primers targeting the
\textit{amoA} gene combined with a cloning approach to assess the
diversity of ammonium-oxidizing bacteria and archaea in
\textit{Laminaria rodriguezii}, and revealed the presence of a
diverse archaeal community.


Similar observations can also be made for viruses. It is generally
accepted that viruses infect virtually all living organisms including
brown algae~\cite{bib147}. Much of the work on brown algal viruses
has focused on Phaeoviruses, large double-stranded DNA viruses that
infect wall-less gametes or spores~\cite{bib148}. The most prominent
representative of this group is arguably \textit{Ectocarpus
siliculosus} virus 1 (EsV-1), which was also found integrated into
its host's genome~\cite{bib149} but representatives of this group
have also been found in other Ectocarpales~\cite{bib150} and in kelp
\cite{bib151,bib152}. Other studied brown algal viromes are known from
the kelp \textit{Ecklonia radiata} and that of the
\textit{Scytosiphon lomentaria} (Ectocarpales). In the former,
numerous members of Siphoviridae, Myoviridae and other viruses were
detected, including a CRESS DNA virus-related sequence found
specifically in bleached individuals~\cite{bib153}. In the latter,
two Endornaviridae and two unclassified RNA viruses were sequenced, but
no information about their interactions with the host is available
\cite{bib154}. However, within the Fucaceae no virome studies have
been published so far, although one study reported that \textit{F.
serratus} expresses a range of RNA Interference-like responses to
viruses \cite{bib155}, suggesting that there is regular contact with
viruses in Nature.~Indeed, viromes may be highly dynamic, and shifts
may occur in response to stress, as shown in the brown alga
\textit{Ectocarpus}~\cite{bib155}. Furthermore, host-associated
viromes also include phages, which interact directly with the bacterial
components of the alga-associated microbiota and as such affect
interactions~\cite{bib156}.

This lack of knowledge on archaea and viruses may considerably limit
our capacity to understand the full spectrum of processes occurring
within Fucaceae holobionts. We thus undeniably require more data on
both to improve our understanding of the interactions within the
Fucaceae holobionts.



\section{Microbiota-derived compounds and their biological
activities}\label{sec4}

{\vspace*{2pt}}

Host-associated microbiota, whether they are endophytes or part of the
biofilm (i.e., epiphytes), are likely to interact with their hosts in
various ways and frequently these interactions are based on their
capacity to produce specific essential metabolites for algal holobiont
\cite{bib117,bib122,bib157,bib158}. In the following section, we will
provide an overview of the current knowledge of the chemical landscape
of algal partners, highlighting key specialized metabolites with
potential applications in different economic\break sectors.

{\vspace*{2pt}}

\subsection{Bacterial metabolites}

Most of the reported secondary metabolites from bacteria associated
with Fucaceae have been derived from strains isolated from the surface
of \textit{Fucus} and notably the genus \textit{Roseobacter}. This
particular genus of bacteria is renowned for its capability to
synthetize N-Acyl Homoserine Lactones (AHLs), which are well-known
bacterial Type 1 Autoinducer signal compounds used by Gram-negative
bacteria for Quorum Sensing (QS). QS is a cell density-dependent
mechanism regulating physiological traits such as antibiotic
production, virulence, motility, bioluminescence, or biofilm
formation~\cite{bib159,bib160}. The AHLs isolated from
\textit{Roseobacter} are commonly made up of a $\gamma$-lactone ring
and an acyl side chain which is usually even-numbered and unbranched,
ranging in chain length from C\tsub{4} to C\tsub{18}. A sampling
campaign of \textit{Roseobacter} from \textit{F. spiralis} harvested in
the German Wadden Sea and in the eastern North Sea led to the isolation
of several marine strains, including \textit{Roseovarius} sp.,
\textit{Loktanella} sp., \textit{Octadecabacter} sp., and
\textit{Dinoroseobacter} sp. In 2019, Ziesche et~al.~\cite{bib161}
isolated known AHLs (Figure~\ref{fig3}.\textbf{1}, \textbf{2},
\textbf{5}--\textbf{18}) and identified two original ones (\textbf{3},
\textbf{4}), and their structures were confirmed by
synthesis~\cite{bib161,bib162,bib163,bib164,bib165}. All of these
compounds displayed a high QS activity in biosensor models. High
variability in the composition of AHLs has been observed among strains
from different sample locations. For instance, surface-associated
strains produce AHLs more frequently compared to strains isolated from
sediments or from the water column~\cite{bib161}.\looseness=-1


\begin{figure*}
\includegraphics{fig03}
\caption{\label{fig3}\fontsize{9.93}{12}\selectfont Chemical structures of seaweed-associated bacterial compounds
(1--45). All these compounds have been classified according to their
putative metabolic pathway: Polyketide Synthase (PKS), Fatty acids and
structurally modify fatty acids, Alkaloids, Shikimates and
Phenylpropanoids, and miscellaneous.}
\end{figure*}


Chemical studies of the strains \textit{Loktanella} sp.\ and
\textit{Roseovarius} sp.\ isolated from \textit{F. spiralis} led
to the isolation of seventeen related \textit{N}-acylalanine methyl
esters (NAMEs) (\textbf{19}--\textbf{34}, \textbf{36}) \cite{bib166}.
Seven \textit{N}-acylglycine methyl esters (NAGMEs)
(\textbf{19}--\textbf{25}) were extracted from \textit{Loktanella}
sp., nine \textit{N}-acylalanine methyl esters (NAMEs)
(\textbf{26}--\textbf{34}) and one \textit{N}-acyl-2-aminobutyric
acid methyl ester (NABME) (\textbf{36}) from \textit{Roseovarius}
sp.\ Compounds \textbf{35} (NABME derivative) and \textbf{37}
(\textit{N}-acylvaline methyl ester derivative---NAVME)
were also isolated from bacterial strains found in an unidentified
species of \textit{Fucus}~\cite{bib166}. Despite their structural
analogy with AHLs, no QS activity was found, thus suggesting that they
play a different ecological role. Compound \textbf{36} displayed some
antibacterial activities and compound \textbf{35} had both
antibacterial and cytotoxic properties (Supplementary Table~S1).


Phaeochromycin E, C, and B (respectively \textbf{38}, \textbf{39},
\textbf{40}) along with the chroman derivative (\textbf{41}) were
isolated from the endophytic strain \textit{Streptomyces
sundarbansensis} associated with a species of \textit{Fucus}
collected from the coastline of Algeria \cite{bib167}. These
compounds showed anti-inflammatory and antibacterial activities
\cite{bib167,bib168}. Furthermore, the stilbene Kocumarin
(\textbf{42}) isolated from the actinobacterium \textit{Kocuria
marina} associated with \textit{P. canaliculata}~\cite{bib169}
displayed antibacterial effects\break \cite{bib169,bib170}.


In 2019, the first study based on the surface microbiota of \textit{F.
vesiculosus} combining Mass Spectrometry Imaging (MSI), metabolomics,
and dereplication allowed for the putative annotation of compounds
produced by \textit{Streptomyces spp.} such as Obelmycin F
(\textbf{43}), Azinomycin B (\textbf{44}), and Indolmycin (\textbf{45})
and their localization on the thallus and tips of the algal
tissues~\cite{bib83}. Compounds \textbf{43} and \textbf{45} show both
antibacterial activities and bacteriostatic effects, while compound
\textbf{44} is known for its antitumor
activity~\cite{bib171,bib172,bib173}. This MSI approach also
demonstrated the presence of AHLs on the surface of the seaweed,
although it cannot identify the organisms responsible for its
production. \looseness=-1

Altogether the capacity of these Fucaceae-associated strains to produce
antibacterial and cytotoxic compounds likely impacts both the host and
other members of the microbiota, but also harbors great potential for
numerous industrial applications as described in Section~\ref{sec2}. 

\subsection{Fungal metabolites}

Fungi have proven to be a highly diverse yet understudied reservoir of
biologically active compounds exhibiting a plethora of potential
functions and applications. Here we present a non-exhaustive list of
secondary metabolites isolated from fungal strains associated with the
Fucaceae.


Chemical investigation of the fungus \textit{Paradendryphiella salina},
isolated from the marine brown alga \textit{A. nodosum} and \textit{P.
canaliculata}, led to the identification of the dendryphiellones A and
D (Figure~\ref{fig4}.\textbf{46}--\textbf{47})~\cite{bib174}, which have
the ability to inhibit the AHL-mediated QS. In the same way, extracts
of fungal endophytes have been found to inhibit the auto inducer 2
(AI-2) pathway, another QS-signaling pathway known to be involved in
cross-kingdom signaling~\cite{bib117}. As QS is thought to be
responsible for a significant increase in the expression of
virulence-related genes in aquaculture farms~\cite{bib175}, compounds
\textbf{46} and \textbf{47} have been suggested as possible agents to
target specific bacterial pathogens~\cite{bib174} and could be
interesting as aquaculture feed additives.


\begin{figure*}
\includegraphics{fig04}
\vspace*{-1pc}
\caption{\label{fig4}Chemical structures of seaweed-associated fungal compounds
(\textbf{46}--\textbf{82}). All compounds have been classified
according to their putative metabolic pathway: Polyketide Synthase
(PKS), Non-Ribosomal Peptide synthetase (NRPS),
Terpenoids.}
\vspace*{-4pt}
\end{figure*}


The endophytic fungus \textit{Phaeosphaeria} sp.\ isolated from
\textit{A. nodosum} led to the discovery of several polyketides
including the new Pyrenocine S (\textbf{48}) along with known
Pyrenocines (\textbf{49}, \textbf{50}, \textbf{51}, \textbf{52}) and
Pyrenochaetic acid C (\textbf{53}) \cite{bib122}. Most of the
Pyrenocines described to date are effective in inhibiting infection by
protistan pathogens in the brown alga \textit{Ectocarpus siliculosus}.
Strikingly, these compounds also inhibited the infection of nori
(\textit{Pyropia yezoensis}) by its two most devastating oomycete
pathogens, \textit{Olpidiopsis pyropiae} and \textit{Pythium
porphyrae}~\cite{bib122}. Several polyketides were also identified in
other fungal strains. For instance, the fungus \textit{Epicoccum} sp.\ 
isolated from \textit{F. vesiculosus} produces Epicoccone A
(\textbf{54}), (3\textit{R},4\textit{S})-4-hydroxymellein
(\textbf{55}), (3\textit{R})-5-hydroxymellein (\textbf{56}), and acetyl
Sumiki's acid (\textbf{57})~\cite{bib139}. The ensuing biological
evaluation pointed out the antibacterial activity of the acetyl
Sumiki's acid (\textbf{57)}~\cite{bib176} while Epicoccone A
(\textbf{54)} displayed antioxidant, antibacterial, and cytotoxic
properties~\cite{bib177,bib178,bib179}, making these metabolites
potential candidates for cosmetics and pharmaceutical industries
(Supplementary Table~S1).


The derivatives of the ubiquitous mellein, (\textbf{55})
\cite{bib156,bib157,bib158,bib159,bib160,bib161} and (\textbf{56})
have numerous interesting properties such as cytotoxic, antibacterial,
\mbox{antitrypanosomal} activities as well as insecticidal properties
\cite{bib180,bib181,bib182,bib183,bib185,bib186,bib187,bib188,bib189}.
5-hydroxyramulosin
(\textbf{58}), a polyketide analog of \textbf{55} and \textbf{56}
was isolated from the endophytic fungus \textit{Phoma tropica}
associated with \textit{F. spiralis} and showed activities in a
range of biological assays~\cite{bib190}. It displayed a potent
cytotoxic activity along with some antifungal and antibacterial
effects\break \cite{bib191,bib192}.


3,5-dibromo-p-hydroxybenzyl alcohol (\textbf{59}) and Lanosol
(\textbf{60}) were isolated from a non-assigned marine
\textit{Ascomycetes} sp.\ from \textit{A. nodosum}~\cite{bib133}.
Lanosol (\textbf{60}) was also detected in the brown algae
\textit{F. vesiculosus} and \textit{A. nodosum}
\cite{bib133,bib193}. Thus, the possibility that marine Ascomycetes
living as epi- or endophytes in these brown algae were producing these
bromophenols cannot be neglected. Both compounds displayed
antibacterial effects~\cite{bib193} and their halogenated nature
suggests antifouling properties. Indeed, red algae cultivated in a
bromide-free environment exhibited increased bacterial colonization in
comparison with cultivation in a bromide-containing medium
\cite{bib194}.


Chemical exploration using a bioactivity-driven molecular networking
approach on the endophytic fungi \textit{Pyrenochaetopsis} sp.\ from
\textit{F. vesiculosus} led to the identification of six new hybrid
\mbox{polyketides,} thought to be synthesized by polyketide
synthases/non-ribosomal peptide synthetases (PKS--NRPS)
\cite{bib195,bib196,bib197}, Pyrenosetins A-F
(\textbf{61}--\textbf{66}). They have antineoplastic and cytotoxic
activities, except for Pyrenosetin E (\textbf{65}) which shows only
cytotoxic activity, and Pyrenosetin F (\textbf{66}) bearing no
biological activity on the assayed targets \cite{bib195,bib196,bib197}.


The study of the toxic metabolites produced by species of
\textit{Fusarium}, \textit{Alternaria}, \textit{Penicillium}, and
\textit{Aspergillus} associated with \textit{A. nodosum}, \textit{P.
canaliculata}, and \textit{F. vesiculosus} demonstrated the presence of
numerous mycotoxins on the surface of the thallus of these three
seaweeds~\cite{bib198}. Among them, polyketides such as Mycophenolic
acid (\textbf{67}), Zearalenone (\textbf{68}), Citrinin (\textbf{69}),
Aflatoxin B1 (\textbf{70}), Sterigmatocystin (\textbf{71}), and Emodin
(\textbf{72}) along with Alternariol (\textbf{73}) and Ochratoxin A
(\textbf{74}) were found. Moreover, other common mycotoxins were
detected, such as the Deoxynivalenol (\textbf{75}), PR toxin
(\textbf{76}), Diacetoxyscirpenol (\textbf{77}), T-2 toxin
(\textbf{78}), Roridin A (\textbf{79}) and $\alpha$-Cyclopiazonic acid
(\textbf{80}). Indeed, species of the family Fucaceae show a broad
profile of mycotoxins, while no mycotoxins were found on \textit{L.
digitata} and \textit{S. latissima} surfaces from the family
Laminariaceae~\cite{bib198}. Lastly, Pestalamide B (\textbf{81}) and
Dihydrosorbicillin (\textbf{82}) were detected by MSI in \textit{F.
vesiculosus} tissues~\cite{bib83}. Of these two compounds, only
Pestalamide B has antifungal activity against \textit{Aspergillus
fumigatus}~\cite{bib199}.


Together, these results suggest that fungal endophytes associated with
Fucaceae produce a wide range of bioactive metabolites which might
confer protection against pathogen infection or prevent dysbiosis in
the phycosphere, i.e., microscale area around phytoplankton cells
enriched in organic\unskip\break substrates~\cite{bib200}. However, few studies
have reported on the potential ecological roles of isolated
metabolites. Indeed, most of the studies looked for potential
biological activities of the fungal compounds and are thus largely
confined to classical in vitro laboratory assays. The in situ study of
chemical interactions within algae is a key element to help understand
the chemical ecology of the holobiont as a whole. Inoculations of
seaweeds with known microbiota are necessary to transpose studies on
isolated microorganisms to the holobiont community. Such multivariable
and integrative experiments are still in their infancy but new tools
such as MiSCoTo~\cite{bib201} allow predicting the metabolic networks
of a host and members of the microbiota, and these models have some
predictive power for metabolite profiles of the ``reconstituted''
holobiont observed in vitro~\cite{bib202}.



\section{Conclusions and perspectives}

We have shown here the huge diversity of the bacterial and fungal
communities associated with members of the Fucaceae, as well as the
chemical diversity of metabolites produced by these microorganisms.
Although our knowledge of the microbiota of Fucaceae is still
rudimentary, in particular regarding Archaea and viruses, we are
starting to notice that some fungal and bacterial species appear
repeatedly and in high abundance in the studies conducted so far. One
of the challenges in the near future will be to properly define a core
microbiota for each algal host, to monitor the factors (i.e.,
geographical areas and seasons) that may lead to some variations in the
holobiont composition, to link these variations to the host fitness,
and lastly to decipher the chemical traits which might impact the
bioactivities and thus the applications.

As the field of marine chemical ecology continues to grow, we are
gaining a more comprehensive understanding of the numerous ecological
functions of marine natural products. Recent research has made
significant contributions to our understanding of the diverse roles of
host-associated bacteria and fungi in marine algal communities.
Furthermore, advances in molecular methods have shown that some
microorganisms are responsible for the production of specialized
metabolites that chemically defend and/or structure the microbiota of
the host organism. Chemical communication and sensory ecology are among
the main topics in marine ecology that have grown significantly in
recent years. Only by bringing together biology, chemistry,
bioinformatics, systems biology, as well as bioactivity screening can
we start exploring algal holobiont as a whole. Such interdisciplinary
approaches and new technologies will play a key role in furthering our
understanding of marine chemical ecology. Furthermore, deciphering the
chemical role of each partner within the algal holobiont will lead to a
better understanding of the origins and functions of the metabolites
produced by the holobiont, including some of the compounds of economic
interest cited before as well as novel bioactive compounds, the
exploration of which is still in its infancy. In the long run, we
anticipate this knowledge will then feed back into the harvesting
(e.g., choice of ideal harvesting period), production (e.g., use of
probiotics to manipulate holobiont metabolomes or direct use of
microbes to enrich in the target metabolites) and valorization of the
Fucaceae.

\section*{Declaration of interests}
The authors do not work for, advise, own shares in, or receive funds
from any organization that could benefit from this article, and have
declared no affiliations other than their research organizations.

\section*{Funding}
This work was funded in part by the SEABIOZ ANR project (AAPG2020,
ANR-20-CE43-0013), the ANRT and the Centre Mondial de l'Innovation of
the Groupe Roullier (Cifre grant number 2022/0938 to GD), the UMR 8227
of the Roscoff Biological Station (CNRS, Sorbonne University), the UMR
7245 of the National Museum of Natural History. 

\CDRGrant[SEABIOZ ANR]{AAPG2020}
\CDRGrant[SEABIOZ ANR]{ANR-20-CE43-0013}
\CDRGrant[Cifre]{2022/0938}

\section*{Acknowledgments} 
We would like to greatly thank Christelle Parchemin (Centre de
Recherches Insulaires et Observatoire de l'Environnement---CRIOBE,
Perpignan France) for providing help and support for this work.

\back{}

\section*{Supplementary data}

Supporting information for this article is available on the journal's
website under \printDOI\ or from the author.  

\CDRsupplementaryTwotypes{supplementary-material}{\cdrattach{Table-S1.xlsx}}

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