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Host-Microbe Interactions in Octocoral Holobionts - Recent Advances and Perspectives Jeroen A

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Host-Microbe Interactions in Octocoral Holobionts - Recent Advances and Perspectives Jeroen A van de Water et al. Microbiome (2018) 6:64 https://doi.org/10.1186/s40168-018-0431-6 REVIEW Open Access Host-microbe interactions in octocoral holobionts - recent advances and perspectives Jeroen A. J. M. van de Water* , Denis Allemand and Christine Ferrier-Pagès Abstract Octocorals are one of the most ubiquitous benthic organisms in marine ecosystems from the shallow tropics to the Antarctic deep sea, providing habitat for numerous organisms as well as ecosystem services for humans. In contrast to the holobionts of reef-building scleractinian corals, the holobionts of octocorals have received relatively little attention, despite the devastating effects of disease outbreaks on many populations. Recent advances have shown that octocorals possess remarkably stable bacterial communities on geographical and temporal scales as well as under environmental stress. This may be the result of their high capacity to regulate their microbiome through the production of antimicrobial and quorum-sensing interfering compounds. Despite decades of research relating to octocoral-microbe interactions, a synthesis of this expanding field has not been conducted to date. We therefore provide an urgently needed review on our current knowledge about octocoral holobionts. Specifically, we briefly introduce the ecological role of octocorals and the concept of holobiont before providing detailed overviews of (I) the symbiosis between octocorals and the algal symbiont Symbiodinium; (II) the main fungal, viral, and bacterial taxa associated with octocorals; (III) the dominance of the microbial assemblages by a few microbial species, the stability of these associations, and their evolutionary history with the host organism; (IV) octocoral diseases; (V) how octocorals use their immune system to fight pathogens; (VI) microbiome regulation by the octocoral and its associated microbes; and (VII) the discovery of natural products with microbiome regulatory activities. Finally, we present our perspectives on how the field of octocoral research should move forward, and the recognition that theseorganismsmaybesuitablemodelorganismstostudycoral-microbesymbioses. Keywords: Microbiome, Holobiont, Symbiodinium, Immunity, Bacteria, Fungi, Gorgonians, Octocoral, Soft coral Background the precious red coral Corallium rubrum (Fig. 1)has The Octocorallia (Haeckel, 1866) is a subclass within the been extensively used for jewelry and other art crafts [3]. Anthozoans (Ehrenberg, 1834, phylum Cnidaria (Verrill, Octocorals are ubiquitous organisms of the sea, having 1865)) and is comprised of soft corals, including sea fans been recorded at all depths, from littoral waters down to and sea whips (order Alcyonacea (Lamouroux, 1812)), the deep-sea abyss, from the tropics to the arctic re- sea pens (order Pennatulacea (Verrill, 1865)), and blue gions, and in all the world’s oceans, although the highest corals (order Helioporacea (Bock, 1938)). The main diversity of octocorals is observed in the Indo-Pacific characteristic of Octocorallia that distinguishes them (reviewed in [4]). While octocoral distribution is signifi- from the Hexacorallia (Haeckel, 1896), such as the reef- cantly influenced by various environmental factors [5], building Scleractinia (Bourne, 1900), is the eightfold the presence of octocorals in nearly all benthic marine symmetry of their polyps (Fig. 1), compared to the six- habitats indicates the adaptive nature of this taxonomic fold symmetry in their relatives. To date, over 3500 spe- group compared to other cnidarian taxa. In some geo- cies belonging to approximately 378 octocoral genera graphical areas, reef ecosystems have even undergone a from 55 families [1, 2] have been described worldwide. phase shift from a hard coral-dominated state towards a Some of those have been famous since the Classical higher abundance of soft corals (Table 1). Antiquity: for example, the beautifully red skeleton of Octocorals are important foundational members of the benthic community. Through the formation of three- * Correspondence: [email protected] dimensional structures, they provide structural complexity Centre Scientifique de Monaco, 8 Quai Antoine 1er, 98000 Monaco, Monaco © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. van de Water et al. Microbiome (2018) 6:64 Page 2 of 28 Fig. 1 Octocorals as habitat providers. a–c Gorgonians form three-dimensional structures in a range of environments, such as a Leptogorgia sarmentosa on sandy bottoms, b Corallium rubrum on the walls and ceilings of caves and overhangs, and c Paramuricea clavata forming “marine animal forests” on rocky substrates. Close-up of the gorgonian colonies of d Paramuricea clavata with open (front) and retracted (back) polyps and e C. rubrum, showing their eightfold body symmetry. f Colonies can consist of thousands of polyps forming large three-dimensional structures. Together colonies can form vast “forests” providing refuge and habitat for numerous marine organisms (photos a and f by Eric Béraud and photos b–e by Sergio Rossi) to ecosystems and thereby refuge and habitats to a rich between plankton and benthos as they capture large quan- fauna (Fig. 1). While all octocorals are suspension feeders, tities of plankton and thereby regulate the primary and sec- relying upon currents to have access to food (reviewed in ondary productions of the coastal food chains [6]. [6]), some octocorals also live in a mutualistic association As all multicellular organisms, corals (encompassing both with phototrophic zooxanthellae (dinoflagellates from the the Octocorallia and Hexacorallia) are holobiont entities, genus Symbiodinium). Although these zooxanthellate octo- forming intricate and complex interactions with a range of corals are restricted to the euphotic zone, they significantly microbes, including dinoflagellates, fungi, bacteria, archaea, contribute to the primary productivity of the shallow coastal and viruses [10]. These microbial symbionts play active ecosystems [7]. Azooxanthellate octocorals, however, rely roles in the health (e.g., nutrient supply, protection against solely on heterotrophic feeding and generally populate dark pathogens) and adaptive response (e.g., toxin degradation) and deep environments, where they can develop very dense of the host to environmental changes [11, 12]. In zooxan- populations providing biomass and structural complexity thellate corals, endosymbiotic photosynthetic dinoflagellates [8, 9]. Because of their abundance, octocorals play a major (Symbiodinium) are the main food providers to their coral role in the benthic-pelagic coupling and the energy transfer host, via the transfer of carbon rich compounds acquired van de Water et al. Microbiome (2018) 6:64 Page 3 of 28 Table 1 Reported coral community shifts from reef-building scleractinian corals to soft corals and their causes Location Cause Shift in octocoral cover References From (%) Up to (%) Red Sea North and Center Crown of thorns starfish 5–10 30–50 [245–247] Anthropogenic pollution South Storms, bleaching 430[248, 249] Anthropogenic pollution Caribbean Florida Keys Bleaching 6 14 [159] US Virgin Islands Diseases [250] Indian Ocean Madagascar/Seychelles Bleaching 1.3 2 [251] Seychelles Bleaching and anthropogenic pollution [245] Pacific Ocean Malaysia Bleaching 130[252] Dynamite fishing Crown of thorns starfish Indonesia Anthropogenic pollution 713[253, 254] Dynamite fishing Australia Bleaching 10 16 [255] Crown of thorns starfish Fiji Anthropogenic pollution N/A N/A [256] through photosynthesis, as well as the recycling of nitrogen the relevance of these findings for our general understanding and phosphorus through the host catabolic wastes [13]. In on the structure, function, and evolution of coral-microbe corals, bacterial symbionts have been implicated in several symbioses, a comprehensive assessment is warranted. other services, such as nitrogen fixation [14], sulfur cycling In this review, we outline the recent discoveries and [15], or antibiotic production to exclude pathogens [16]. current knowledge regarding (I) the octocoral-Symbiodinium Maintaining a multi-functional microbial community is mutualism, (II) the diversity and function of microbes therefore essential to holobiont fitness. Recent studies have (including fungi, viruses and bacteria) associated with shown that corals have a “core microbiome” [17], com- tropical, temperate, and cold-water octocorals, and (III) posed of microbes that are consistently associated with a the structure and stability of the microbial assemblages host species, as well as transient microbes whose presence and remarkable dominance of a few bacterial species that depends on local conditions [18–20]. In case of environ- suggest a close evolutionary history. We will also address mental stress, such as rising sea water temperatures, (IV) the potential for microbiome regulation by the host changes in the resident microbial community composition and (V) the octocoral immune system in case of (VI) the and
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