View source for Marine microbiome

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[[File:Marine animal host-microbiome relationships.jpg|thumb|upright=1.8| {{center|'''Marine animal host-microbiome relationship'''}} Relationships are generally thought to exist in a symbiotic state, and are normally exposed to environmental and animal-specific factors that may cause natural variations. Some events may change the relationship into a functioning but altered symbiotic state, whereas extreme stress events may cause [[dysbiosis]] or a breakdown of the relationship and interactions.<ref name=Apprill2017>Apprill, A. (2017) "Marine animal microbiomes: toward understanding host–microbiome interactions in a changing ocean". ''Frontiers in Marine Science'', '''4''': 222. {{doi|10.3389/fmars.2017.00222}}. [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref>]]

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of [[marine microorganisms]] associating with diverse [[Marine life#Origin of animals|marine animal]] hosts is moving the field into studies that address interactions between the animal host and a more multi-member [[microbiome]]. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.<ref name=Apprill2017 />

In the oceans, it is challenging to find [[eukaryotic organism]]s that do not live in close relationship with a microbial partner. Host-associated microbiomes also influence [[Marine biogeochemical cycles|biogeochemical cycling]] within ecosystems with [[Ecological cascade|cascading]] effects on biodiversity and ecosystem processes. The microbiomes of diverse marine animals are currently under study, from simplistic organisms including [[sponge]]s and [[ctenophore]]s to more complex organisms such as [[sea squirt]]s and [[shark]]s.

==Background==
{{microbiomes|marine}}
{{see also|Marine microbial symbiosis}}
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Within the vast [[biological diversity]] that inhabits the world's oceans, it would be challenging to find a [[Eukaryote|eukaryotic organism]] that does not live in close relationship with a [[Microorganism|microbial partner]].<ref name=Wilkins2019 /> Such [[symbioses]], i.e., persistent interactions between host and microbe in which none of the partners gets harmed and at least one of them benefits, are ubiquitous from shallow reefs to [[deep-sea hydrothermal vent]]s. Studies on [[coral]]s,<ref name=Krediet2013>{{cite journal |doi = 10.1098/rspb.2012.2328|title = Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases|year = 2013|last1 = Krediet|first1 = Cory J.|last2 = Ritchie|first2 = Kim B.|last3 = Paul|first3 = Valerie J.|last4 = Teplitski|first4 = Max|journal = Proceedings of the Royal Society B: Biological Sciences|volume = 280|issue = 1755|pmid = 23363627|pmc = 3574386}}</ref> [[sponge]]s,<ref name=Webster2016>{{cite journal |doi = 10.1128/mBio.00135-16|title = The Sponge Hologenome|year = 2016|last1 = Webster|first1 = Nicole S.|last2 = Thomas|first2 = Torsten|journal = mBio|volume = 7|issue = 2|pages = e00135-16|pmid = 27103626|pmc = 4850255}}</ref> and [[mollusk]]s{{hsp}}<ref>{{cite journal |doi = 10.1128/AEM.57.8.2376-2382.1991|title = Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by using 16S rRNA sequence analysis and oligodeoxynucleotide probe hybridization|year = 1991|last1 = Distel|first1 = D. L.|last2 = Delong|first2 = E. F.|last3 = Waterbury|first3 = J. B.|journal = Applied and Environmental Microbiology|volume = 57|issue = 8|pages = 2376–2382|pmid = 1722662|pmc = 183578| bibcode=1991ApEnM..57.2376D }}</ref><ref>{{cite journal |doi = 10.1111/j.1462-2920.2008.01728.x|title = Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments|year = 2008|last1 = Ruehland|first1 = Caroline|last2 = Blazejak|first2 = Anna|last3 = Lott|first3 = Christian|last4 = Loy|first4 = Alexander|last5 = Erséus|first5 = Christer|last6 = Dubilier|first6 = Nicole|journal = Environmental Microbiology|volume = 10|issue = 12|pages = 3404–3416|pmid = 18764872| bibcode=2008EnvMi..10.3404R }}</ref><ref name=Nyholm2004>{{cite journal |doi = 10.1038/nrmicro957|title = The winnowing: Establishing the squid–vibrio symbiosis|year = 2004|last1 = Nyholm|first1 = Spencer V.|last2 = McFall-Ngai|first2 = Margaret|journal = Nature Reviews Microbiology|volume = 2|issue = 8|pages = 632–642|pmid = 15263898|s2cid = 21583331}}</ref> have revealed some of the profoundly important symbiotic roles microbes play in the lives of their hosts. These studies, however, have tended to focus on a small number of specific microbial taxa. In contrast, most hosts retain groups of many hundreds of different microbes (i.e., a [[microbiome]],<ref>{{cite journal |doi = 10.1093/femsle/fnz117|title = Not all animals need a microbiome|year = 2019|last1 = Hammer|first1 = Tobin J.|last2 = Sanders|first2 = Jon G.|last3 = Fierer|first3 = Noah|journal = FEMS Microbiology Letters|volume = 366|issue = 10|pmid = 31132110}}</ref><ref>{{cite journal |doi = 10.3389/fmicb.2019.00292|title = A Developing Symbiosis: Enabling Cross-Talk Between Ecologists and Microbiome Scientists|year = 2019|last1 = Tipton|first1 = Laura|last2 = Darcy|first2 = John L.|last3 = Hynson|first3 = Nicole A.|journal = Frontiers in Microbiology|volume = 10|page = 292|pmid = 30842763|pmc = 6391321| doi-access=free }}</ref> which themselves can vary throughout the ontogeny of the host and as a result of environmental perturbations.<ref>{{cite journal |doi = 10.3389/fmars.2017.00222|title = Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean|year = 2017|last1 = Apprill|first1 = Amy|journal = Frontiers in Marine Science|volume = 4|s2cid = 9729436|doi-access = free}}</ref><ref name=McFall-Ngai2013>{{cite journal |doi = 10.1073/pnas.1218525110|title = Animals in a bacterial world, a new imperative for the life sciences|year = 2013|last1 = McFall-Ngai|first1 = Margaret|last2 = Hadfield|first2 = Michael G.|last3 = Bosch|first3 = Thomas C. G.|last4 = Carey|first4 = Hannah V.|last5 = Domazet-Lošo|first5 = Tomislav|last6 = Douglas|first6 = Angela E.|last7 = Dubilier|first7 = Nicole|last8 = Eberl|first8 = Gerard|last9 = Fukami|first9 = Tadashi|last10 = Gilbert|first10 = Scott F.|last11 = Hentschel|first11 = Ute|last12 = King|first12 = Nicole|last13 = Kjelleberg|first13 = Staffan|last14 = Knoll|first14 = Andrew H.|last15 = Kremer|first15 = Natacha|last16 = Mazmanian|first16 = Sarkis K.|last17 = Metcalf|first17 = Jessica L.|last18 = Nealson|first18 = Kenneth|last19 = Pierce|first19 = Naomi E.|last20 = Rawls|first20 = John F.|last21 = Reid|first21 = Ann|last22 = Ruby|first22 = Edward G.|last23 = Rumpho|first23 = Mary|last24 = Sanders|first24 = Jon G.|last25 = Tautz|first25 = Diethard|last26 = Wernegreen|first26 = Jennifer J.|journal = Proceedings of the National Academy of Sciences|volume = 110|issue = 9|pages = 3229–3236|pmid = 23391737|pmc = 3587249|bibcode = 2013PNAS..110.3229M| doi-access=free }}</ref><ref>{{cite journal |doi = 10.1111/j.1462-2920.2011.02460.x|title = Marine sponges and their microbial symbionts: Love and other relationships|year = 2012|last1 = Webster|first1 = Nicole S.|last2 = Taylor|first2 = Michael W.|journal = Environmental Microbiology|volume = 14|issue = 2|pages = 335–346|pmid = 21443739|doi-access = free| bibcode=2012EnvMi..14..335W }}</ref> Rather than host-associated microbes functioning independently, complex multi-assemblage microbiomes have major impact on the fitness and function of their hosts. Studying these complex interactions and biological outcomes is difficult, but to understand the origin and evolution of organisms and populations and the structure and function of communities and ecosystems, the understanding of symbioses in host–microbiome systems needs advancing.<ref>{{cite journal |doi = 10.1126/science.1093892|title = OCEANOGRAPHY: Microbes, Molecules, and Marine Ecosystems|year = 2004|last1 = Azam|first1 = F.|last2 = Worden|first2 = A. Z.|journal = Science|volume = 303|issue = 5664|pages = 1622–1624|pmid = 15016987|s2cid = 10101482}}</ref><ref>{{cite journal |doi = 10.1038/s41579-019-0222-5|title = Scientists' warning to humanity: Microorganisms and climate change|year = 2019|last1 = Cavicchioli|first1 = Ricardo|last2 = Ripple|first2 = William J.|last3 = Timmis|first3 = Kenneth N.|last4 = Azam|first4 = Farooq|last5 = Bakken|first5 = Lars R.|last6 = Baylis|first6 = Matthew|last7 = Behrenfeld|first7 = Michael J.|last8 = Boetius|first8 = Antje|last9 = Boyd|first9 = Philip W.|last10 = Classen|first10 = Aimée T.|last11 = Crowther|first11 = Thomas W.|last12 = Danovaro|first12 = Roberto|last13 = Foreman|first13 = Christine M.|last14 = Huisman|first14 = Jef|last15 = Hutchins|first15 = David A.|last16 = Jansson|first16 = Janet K.|last17 = Karl|first17 = David M.|last18 = Koskella|first18 = Britt|last19 = Mark Welch|first19 = David B.|last20 = Martiny|first20 = Jennifer B. H.|last21 = Moran|first21 = Mary Ann|last22 = Orphan|first22 = Victoria J.|last23 = Reay|first23 = David S.|last24 = Remais|first24 = Justin V.|last25 = Rich|first25 = Virginia I.|last26 = Singh|first26 = Brajesh K.|last27 = Stein|first27 = Lisa Y.|last28 = Stewart|first28 = Frank J.|last29 = Sullivan|first29 = Matthew B.|last30 = Van Oppen|first30 = Madeleine J. H.|journal = Nature Reviews Microbiology|volume = 17|issue = 9|pages = 569–586|pmid = 31213707|pmc = 7136171}}</ref><ref name=Wilkins2019>{{cite journal |doi = 10.1371/journal.pbio.3000533|title = Host-associated microbiomes drive structure and function of marine ecosystems|year = 2019|last1 = Wilkins|first1 = Laetitia G. E.|last2 = Leray|first2 = Matthieu|last3 = o'Dea|first3 = Aaron|last4 = Yuen|first4 = Benedict|last5 = Peixoto|first5 = Raquel S.|last6 = Pereira|first6 = Tiago J.|last7 = Bik|first7 = Holly M.|last8 = Coil|first8 = David A.|last9 = Duffy|first9 = J. Emmett|last10 = Herre|first10 = Edward Allen|last11 = Lessios|first11 = Harilaos A.|last12 = Lucey|first12 = Noelle M.|last13 = Mejia|first13 = Luis C.|last14 = Rasher|first14 = Douglas B.|last15 = Sharp|first15 = Koty H.|last16 = Sogin|first16 = Emilia M.|last17 = Thacker|first17 = Robert W.|last18 = Vega Thurber|first18 = Rebecca|last19 = Wcislo|first19 = William T.|last20 = Wilbanks|first20 = Elizabeth G.|last21 = Eisen|first21 = Jonathan A.|journal = PLOS Biology|volume = 17|issue = 11|pages = e3000533|pmid = 31710600|pmc = 6874084 | doi-access=free }} [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref>

There are many outstanding questions in ecology and evolution that could be addressed by expanding the phylogenetic and ecological breadth of host-associated microbiome studies, including all possible interactions throughout the microbiome. There is strong empirical evidence and new consensus that biodiversity (i.e., the richness of species and their interactions) pervasively influences the functioning of Earth's ecosystems, including ecosystem productivity.<ref>{{cite journal |doi = 10.1038/nature23886|title = Biodiversity effects in the wild are common and as strong as key drivers of productivity|year = 2017|last1 = Duffy|first1 = J. Emmett|last2 = Godwin|first2 = Casey M.|last3 = Cardinale|first3 = Bradley J.|journal = Nature|volume = 549|issue = 7671|pages = 261–264|pmid = 28869964|bibcode = 2017Natur.549..261D|s2cid = 4459856}}</ref><ref>{{cite journal |doi = 10.1038/nature11148|title = Biodiversity loss and its impact on humanity|year = 2012|last1 = Cardinale|first1 = Bradley J.|last2 = Duffy|first2 = J. Emmett|last3 = Gonzalez|first3 = Andrew|last4 = Hooper|first4 = David U.|last5 = Perrings|first5 = Charles|last6 = Venail|first6 = Patrick|last7 = Narwani|first7 = Anita|last8 = Mace|first8 = Georgina M.|last9 = Tilman|first9 = David|last10 = Wardle|first10 = David A.|last11 = Kinzig|first11 = Ann P.|last12 = Daily|first12 = Gretchen C.|last13 = Loreau|first13 = Michel|last14 = Grace|first14 = James B.|last15 = Larigauderie|first15 = Anne|last16 = Srivastava|first16 = Diane S.|last17 = Naeem|first17 = Shahid|journal = Nature|volume = 486|issue = 7401|pages = 59–67|pmid = 22678280|bibcode = 2012Natur.486...59C|s2cid = 4333166|url = https://pub.epsilon.slu.se/10240/7/wardle_d_etal_130415.pdf}}</ref> However, this research has focused almost exclusively on macroorganisms. Because microbial symbionts are integral parts of most living organisms,<ref name=McFall-Ngai2013 /><ref>{{cite journal |doi = 10.1073/pnas.1809349115|title = Microbiome interactions shape host fitness|year = 2018|last1 = Gould|first1 = Alison L.|last2 = Zhang|first2 = Vivian|last3 = Lamberti|first3 = Lisa|last4 = Jones|first4 = Eric W.|last5 = Obadia|first5 = Benjamin|last6 = Korasidis|first6 = Nikolaos|last7 = Gavryushkin|first7 = Alex|last8 = Carlson|first8 = Jean M.|last9 = Beerenwinkel|first9 = Niko|last10 = Ludington|first10 = William B.|journal = Proceedings of the National Academy of Sciences|volume = 115|issue = 51|pages = E11951–E11960|pmid = 30510004|pmc = 6304949| doi-access=free | bibcode=2018PNAS..11511951G }}</ref> the understanding of how microbial symbionts contribute to host performance and adaptability needs broadening.<ref name=Wilkins2019 />

==Foundations of productive ecosystems==
[[File:Dynamics in symbiosis with aquatic ciliates as host.jpg|thumb|upright=1.8| {{center|'''Possible dynamics in symbiosis with aquatic ciliates as host'''<br /><small>Black circle: macronucleus, white big circle: food vacuoles, green circles: phototrophs, brown circles: chemoautotrophs, yellow ovals: heterotrophic prokaryotes</small>}}]]

[[Ecosystem engineer]]s, such as many types of corals, deep-sea [[mussel]]s, and hydrothermal vent [[tubeworm]]s, contribute to [[primary productivity]] and create the structural habitats and nutrient resources that are the foundation of their respective ecosystems.<ref>{{cite journal |doi = 10.7717/peerj.4455|title = The importance of sponges and mangroves in supporting fish communities on degraded coral reefs in Caribbean Panama|year = 2018|last1 = Seemann|first1 = Janina|last2 = Yingst|first2 = Alexandra|last3 = Stuart-Smith|first3 = Rick D.|last4 = Edgar|first4 = Graham J.|last5 = Altieri|first5 = Andrew H.|journal = PeerJ|volume = 6|pages = e4455|pmid = 29610704|pmc = 5878927 | doi-access=free }}</ref> All of these taxa engage in [[Mutualism (biology)|mutualistic]] nutritional symbioses with microbes. There are many examples of marine nutritional mutualisms in which microbes enable hosts to utilize resources or substrates otherwise unavailable to the host alone. Such symbioses have been described in detail in reduced and anoxic sediments (e.g., [[Lucinid|lucinid clams]], [[Stilbonematid|stilbonematid nematodes]], and gutless [[oligochaetes]]) and hydrothermal vents (e.g., the [[giant tube worm]] or [[Bathymodiolus|deep-sea mussels]]).<ref>{{cite journal |doi = 10.1128/mBio.02241-18|title = Host-Microbe Coevolution: Applying Evidence from Model Systems to Complex Marine Invertebrate Holobionts|year = 2019|last1 = o'Brien|first1 = Paul A.|last2 = Webster|first2 = Nicole S.|last3 = Miller|first3 = David J.|last4 = Bourne|first4 = David G.|journal = mBio|volume = 10|issue = 1|pmid = 30723123|pmc = 6428750}}</ref> Moreover, many [[foundational species]] of marine [[macroalgae]] are vitamin [[auxotroph]]s (for example, half of more than 300 surveyed species were unable to synthesize [[cobalamin]]), and their productivity depends on provisioning from their [[epiphytic]] bacteria.<ref>{{cite journal |doi = 10.1038/nature04056|title = Algae acquire vitamin B12 through a symbiotic relationship with bacteria|year = 2005|last1 = Croft|first1 = Martin T.|last2 = Lawrence|first2 = Andrew D.|last3 = Raux-Deery|first3 = Evelyne|last4 = Warren|first4 = Martin J.|last5 = Smith|first5 = Alison G.|journal = Nature|volume = 438|issue = 7064|pages = 90–93|pmid = 16267554|bibcode = 2005Natur.438...90C|s2cid = 4328049}}</ref> Reefs often consist of [[stony corals]], one of the most well-known examples of a mutualistic symbiosis, in which the [[dinoflagellate]] alga Symbiodiniaceae supplies the coral with [[glucose]], [[glycerol]], and [[amino acid]]s, while the coral provides the algae with a protected environment and limiting compounds (e.g., nitrogen species) needed for photosynthesis. However, this is a classic example of a mutualistic symbiosis that is sensitive to environmental disturbances, which can disrupt the fragile interactions between host and microbe. When reefs become warm and eutrophic, mutualistic Symbiodiniaceae may induce cellular damage to the host and/or sequester more resources for their own growth, thereby injuring and parasitizing their hosts.<ref>{{cite journal |doi = 10.3354/meps12652|title = Leveraging new knowledge of Symbiodinium community regulation in corals for conservation and reef restoration|year = 2018|last1 = Quigley|first1 = KM|last2 = Bay|first2 = LK|last3 = Willis|first3 = BL|journal = Marine Ecology Progress Series|volume = 600|pages = 245–253|bibcode = 2018MEPS..600..245Q| s2cid=90469901 }}</ref><ref>{{cite journal |doi = 10.1038/s41396-018-0046-8|title = Climate change promotes parasitism in a coral symbiosis|year = 2018|last1 = Baker|first1 = David M.|last2 = Freeman|first2 = Christopher J.|last3 = Wong|first3 = Jane C.Y.|last4 = Fogel|first4 = Marilyn L.|last5 = Knowlton|first5 = Nancy|journal = The ISME Journal|volume = 12|issue = 3|pages = 921–930|pmid = 29379177|pmc = 5864192| bibcode=2018ISMEJ..12..921B }}</ref> [[Reef fishes]], which seek homes on [[coral reef]]s, are important in fostering coral recovery in the wake of disturbance. Epulopiscium bacteria in the guts of surgeonfishes produce enzymes that allow their hosts to digest complex [[polysaccharide]]s, enabling the host fish to feed on tough, leathery red and brown macroalgae.<ref>{{cite journal |doi = 10.1073/pnas.1703070114|title = Genomic diversification of giant enteric symbionts reflects host dietary lifestyles|year = 2017|last1 = Ngugi|first1 = David Kamanda|last2 = Miyake|first2 = Sou|last3 = Cahill|first3 = Matt|last4 = Vinu|first4 = Manikandan|last5 = Hackmann|first5 = Timothy J.|last6 = Blom|first6 = Jochen|last7 = Tietbohl|first7 = Matthew D.|last8 = Berumen|first8 = Michael L.|last9 = Stingl|first9 = Ulrich|journal = Proceedings of the National Academy of Sciences|volume = 114|issue = 36|pages = E7592–E7601|pmid = 28835538|pmc = 5594648| doi-access=free | bibcode=2017PNAS..114E7592N }}</ref> This trophic innovation has facilitated [[niche diversification]] among coral reef [[herbivore]]s. [[Surgeonfish]]es are critical to the functioning of Indo-Pacific coral reefs, as they are among the only fishes capable of consuming large macroalgae that bloom in the wake of [[ecosystem disturbance]] and suppress coral recovery.<ref>{{cite journal |doi = 10.1007/s10021-009-9291-z|title = Limited Functional Redundancy in a High Diversity System: Single Species Dominates Key Ecological Process on Coral Reefs|year = 2009|last1 = Hoey|first1 = Andrew S.|last2 = Bellwood|first2 = David R.|journal = Ecosystems|volume = 12|issue = 8|pages = 1316–1328| bibcode=2009Ecosy..12.1316H |s2cid = 42138428}}</ref><ref name=Wilkins2019 />

[[File:Olavius algarvensis from Elba, Italy.jpg|thumb|left| The gutless worm ''[[Olavius algarvensis]]'' depends on symbiotic bacteria living under its cuticle as its source of food. The bacteria are responsible for the bright white appearance of the worms.]]

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Along with more standard examples of nutritional symbioses in animals, recent advances in [[genome sequencing]] technology have led to the discovery of many endosymbiotic associations in [[marine protists]] (a protist is a general term to refer to a non-[[monophyletic]] collection of [[unicellular]] [[eukaryote]]s that are not [[fungi]] or in the [[Plantae]] group) These illustrate the incorporation of various new biochemical functions, such as photosynthesis, nitrogen fixation and recycling, and methanogenesis, into protist hosts by endosymbionts.<ref>{{cite journal |doi = 10.1098/rstb.2009.0188|title = Endosymbiotic associations within protists|year = 2010|last1 = Nowack|first1 = Eva C. M.|last2 = Melkonian|first2 = Michael|journal = Philosophical Transactions of the Royal Society B: Biological Sciences|volume = 365|issue = 1541|pages = 699–712|pmid = 20124339|pmc = 2817226}}</ref> Endosymbiosis in protists is widespread and represents an important source of innovation. Previously unrecognized metabolic innovations of marine microbial symbioses that are ecologically important are discovered regularly.<ref>{{cite journal |doi = 10.1016/j.cub.2016.10.034|title = Caribbean Spiny Lobster Fishery is Underpinned by Trophic Subsidies from Chemosynthetic Primary Production|year = 2016|last1 = Higgs|first1 = Nicholas D.|last2 = Newton|first2 = Jason|last3 = Attrill|first3 = Martin J.|journal = Current Biology|volume = 26|issue = 24|pages = 3393–3398|pmid = 27939312|s2cid = 14401680|doi-access = free| bibcode=2016CBio...26.3393H |hdl = 10026.1/9129|hdl-access = free}}</ref> For example, ''[[Candidatus]]'' Kentron (a clade of [[Gammaproteobacteria]] found in association with [[ciliate]]s) nourish their ciliate hosts in the genus ''[[Kentrophoros]]'' and recycle [[acetate]] and [[propionate]], which are low-value cellular waste products from their hosts, into [[Biomass (ecology)|biomass]].<ref>{{cite journal |doi = 10.1128/mBio.01112-19|title = Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO2Fixation|year = 2019|last1 = Seah|first1 = Brandon K. B.|last2 = Antony|first2 = Chakkiath Paul|last3 = Huettel|first3 = Bruno|last4 = Zarzycki|first4 = Jan|last5 = Schada von Borzyskowski|first5 = Lennart|last6 = Erb|first6 = Tobias J.|last7 = Kouris|first7 = Angela|last8 = Kleiner|first8 = Manuel|last9 = Liebeke|first9 = Manuel|last10 = Dubilier|first10 = Nicole|last11 = Gruber-Vodicka|first11 = Harald R.|journal = mBio|volume = 10|issue = 3|pmid = 31239380|pmc = 6593406}}</ref> Another example is the anaerobic marine [[ciliate]] ''[[Strombidium|Strombidium purpureum]]''.<ref>{{cite journal |doi = 10.1016/j.tim.2009.09.001|title = Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes|year = 2009|last1 = Gast|first1 = Rebecca J.|last2 = Sanders|first2 = Robert W.|last3 = Caron|first3 = David A.|journal = Trends in Microbiology|volume = 17|issue = 12|pages = 563–569|pmid = 19828317}}</ref> The ciliate lives under anaerobic conditions and harbors endosymbiotic [[purple nonsulfur bacteria]] that contain both [[bacteriochlorophyll a]] and spirilloxanthin. The endosymbionts are photosynthetically active; hence, this symbiosis represents an evolutionary transition of an aerobic organism to an anaerobic one while incorporating [[organelle]]s.<ref name=Wilkins2019 />

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==Reproduction and host development==
{{marine life sidebar}}

Extending beyond nutritional symbioses, microbial symbionts can alter the reproduction, development, and growth of their hosts. Specific bacterial strains in marine biofilms often directly control the recruitment of planktonic larvae and propagules, either by inhibiting settlement or by serving as a settlement cue.<ref>{{cite journal |doi = 10.1038/srep00228|pmc=3260340|title = Recruitment in the sea: Bacterial genes required for inducing larval settlement in a polychaete worm|year = 2012|last1 = Huang|first1 = Ying|last2 = Callahan|first2 = Sean|last3 = Hadfield|first3 = Michael G.|journal = Scientific Reports|volume = 2|page = 228|pmid=22355742 |bibcode = 2012NatSR...2E.228H|s2cid = 14731587|doi-access = free}}</ref><ref>{{cite journal |doi = 10.3389/fmicb.2016.00001|title = Revisiting the STEC Testing Approach: Using espK and espV to Make Enterohemorrhagic Escherichia coli (EHEC) Detection More Reliable in Beef|year = 2016|last1 = Delannoy|first1 = Sabine|last2 = Chaves|first2 = Byron D.|last3 = Ison|first3 = Sarah A.|last4 = Webb|first4 = Hattie E.|last5 = Beutin|first5 = Lothar|last6 = Delaval|first6 = José|last7 = Billet|first7 = Isabelle|last8 = Fach|first8 = Patrick|journal = Frontiers in Microbiology|volume = 7|page = 1|pmid = 26834723|pmc = 4722105| doi-access=free }}</ref> For example, the settlement of zoospores from the green alga Ulva intestinalis onto the biofilms of specific bacteria is mediated by their attraction to the quorum-sensing molecule, acyl-homoserine lactone, secreted by the bacteria.<ref>{{cite journal |doi = 10.1111/j.1365-3040.2005.01440.x|title = Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism|year = 2006|last1 = Wheeler|first1 = Glen L.|last2 = Tait|first2 = Karen|last3 = Taylor|first3 = Alison|last4 = Brownlee|first4 = Colin|last5 = Joint|first5 = IAN|journal = Plant, Cell and Environment|volume = 29|issue = 4|pages = 608–618|pmid = 17080611|doi-access = free}}</ref> Classic examples of marine host–microbe developmental dependence include the observation that algal cultures grown in isolation exhibited abnormal morphologies{{hsp}}<ref>{{cite journal |doi = 10.1111/j.1529-8817.1980.tb03019.x|title = Bacteria Induced Polymorphism in an Axenic Laboratory Strain of Ulva Lactuca (Chlorophyceae)1|year = 1980|last1 = Provasoli|first1 = Luigi|last2 = Pintner|first2 = Irma J.|journal = Journal of Phycology|volume = 16|issue = 2|pages = 196–201| bibcode=1980JPcgy..16..196P |s2cid = 85817449}}</ref> and the subsequent discovery of morphogenesis-inducing compounds, such as thallusin, secreted by epiphytic bacterial symbionts.<ref>{{cite journal |doi = 10.1126/science.1105486|title = Isolation of an Algal Morphogenesis Inducer from a Marine Bacterium|year = 2005|last1 = Matsuo|first1 = Y.|last2 = Imagawa|first2 = H.|last3 = Nishizawa|first3 = M.|last4 = Shizuri|first4 = Y.|journal = Science|volume = 307|issue = 5715|page = 1598|pmid = 15761147|s2cid = 28850526}}</ref> Bacteria are also known to influence the growth of marine plants, macroalgae, and phytoplankton by secreting phytohormones such as indole acetic acid and cytokinin-type hormones.<ref name=Goecke2010>{{cite journal |doi = 10.3354/meps08607|title = Chemical interactions between marine macroalgae and bacteria|year = 2010|last1 = Goecke|first1 = F.|last2 = Labes|first2 = A.|last3 = Wiese|first3 = J.|last4 = Imhoff|first4 = JF|journal = Marine Ecology Progress Series|volume = 409|pages = 267–299|bibcode = 2010MEPS..409..267G|doi-access =free }}</ref><ref>{{cite journal |doi = 10.1038/nature14488|title = Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria|year = 2015|last1 = Amin|first1 = S. A.|last2 = Hmelo|first2 = L. R.|last3 = Van Tol|first3 = H. M.|last4 = Durham|first4 = B. P.|last5 = Carlson|first5 = L. T.|last6 = Heal|first6 = K. R.|last7 = Morales|first7 = R. L.|last8 = Berthiaume|first8 = C. T.|last9 = Parker|first9 = M. S.|last10 = Djunaedi|first10 = B.|last11 = Ingalls|first11 = A. E.|last12 = Parsek|first12 = M. R.|last13 = Moran|first13 = M. A.|last14 = Armbrust|first14 = E. V.|journal = Nature|volume = 522|issue = 7554|pages = 98–101|pmid = 26017307|bibcode = 2015Natur.522...98A|s2cid = 4462055}}</ref><ref>{{cite journal |doi = 10.3354/meps09672|title = Effects of epibiotic bacteria on leaf growth and epiphytes of the seagrass Posidonia oceanica|year = 2012|last1 = Celdrán|first1 = D.|last2 = Espinosa|first2 = E.|last3 = Sánchez-Amat|first3 = A.|last4 = Marín|first4 = A.|journal = Marine Ecology Progress Series|volume = 456|pages = 21–27|bibcode = 2012MEPS..456...21C|doi-access = free}}</ref> In the marine choanoflagellate Salpingoeca rosetta, both multicellularity and reproduction are triggered by specific bacterial cues, offering a view into the origins of bacterial control over animal development (reviewed by Woznica and King.<ref>{{cite journal |doi = 10.1016/j.mib.2017.12.013|title = Lessons from simple marine models on the bacterial regulation of eukaryotic development|year = 2018|last1 = Woznica|first1 = Arielle|last2 = King|first2 = Nicole|journal = Current Opinion in Microbiology|volume = 43|pages = 108–116|pmid = 29331767|pmc = 6051772}}</ref> The benefit to the bacteria, in return, is that they receive physical space to colonize at particular points in the water column typically accessible only to planktonic microbes. Perhaps the best-studied example of intimate host–microbe interactions controlling animal development is the Hawaiian bobtail squid Euprymna scolopes.<ref>{{cite journal |doi = 10.1146/annurev-micro-091313-103654|title = The Importance of Microbes in Animal Development: Lessons from the Squid-Vibrio Symbiosis|year = 2014|last1 = McFall-Ngai|first1 = Margaret J.|journal = Annual Review of Microbiology|volume = 68|pages = 177–194|pmid = 24995875|pmc = 6281398}}</ref> It lives in a mutualistic symbiosis with the bioluminescent bacteria Aliivibrio fischeri. The bacteria are fed a solution of sugars and amino acids by the host and, in return, provide bioluminescence for countershading and predator avoidance.<ref name=Nyholm2004 /> This mutualism with microbes provides a selective advantage for the squid in predator–prey interactions. Another invertebrate example can be found in tubeworms, in which Hydroides elegans metamorphosis is mediated by a bacterial inducer and mitogen-activated protein kinase (MAPK) signaling in biofilms.<ref>{{cite journal |doi = 10.1073/pnas.1603142113|title = Stepwise metamorphosis of the tubeworm ''Hydroides'' elegansis mediated by a bacterial inducer and MAPK signaling|year = 2016|last1 = Shikuma|first1 = Nicholas J.|last2 = Antoshechkin|first2 = Igor|last3 = Medeiros|first3 = João M.|last4 = Pilhofer|first4 = Martin|last5 = Newman|first5 = Dianne K.|journal = Proceedings of the National Academy of Sciences|volume = 113|issue = 36|pages = 10097–10102| pmid=27551098 | pmc=5018781 |s2cid = 23501584|doi-access = free| bibcode=2016PNAS..11310097S }}</ref><ref name=Wilkins2019 />

{{clear}}

==Biofouling and microbial community assembly==
[[File:Marine animals and their associated microbiomes.jpg|thumb|upright=2| {{center|'''Some marine animals and associated microbiomes'''}} (A) [[Hawaiian bobtail squid]] and (B) a [[transmission electron micrograph|TEM]] of ''[[Vibrio fischeri]]'' cells associating with dense [[microvilli]] (MV) and in proximity to the [[epithelial]] nucleus (N) within the light organ.<br /> (C) the reef-building coral ''[[Stylophora pistillata]]'' and (D) a microscopy image of ''[[Endozoicomonas]]'' cells (probed yellow using in situ hybridization) within the tentacles of a ''S. pistillata'' host.<br /> (E) the [[Atlantic killifish]] and (F) a [[scanning electron microscopy|SEM]] image of the surface and scales of the fish, with arrows pointing to bacterial-sized cells and larger cells (which are not noted) are presumably phytoplankton.<br /> (G) a [[humpback whale]] breaching and (H) a SEM image of a humpback's skin surface associated bacteria, with arrows indicating two different cell morphologies.<ref name=Apprill2017 />]]

Some host-associated microbes produce compounds that prevent [[biofouling]] and regulate microbiome assembly and maintenance in many marine organisms, including sponges, macroalgae, and corals.<ref>{{cite journal |doi = 10.1111/1574-6941.12064|title = Characterization of thegacA-dependent surface and coral mucus colonization by an opportunistic coral pathogen ''Serratia'' marcescensPDL100|year = 2013|last1 = Krediet|first1 = Cory J.|last2 = Carpinone|first2 = Emily M.|last3 = Ritchie|first3 = Kim B.|last4 = Teplitski|first4 = Max|journal = FEMS Microbiology Ecology|volume = 84|issue = 2|pages = 290–301|pmid = 23278392|doi-access = free| bibcode=2013FEMME..84..290K }}</ref><ref name=Pita2018>{{cite journal | vauthors = Pita L, Rix L, Slaby BM, Franke A, Hentschel U | title = The sponge holobiont in a changing ocean: from microbes to ecosystems | journal = Microbiome | volume = 6 | issue = 1 | pages = 46 | date = March 2018 | pmid = 29523192 | doi = 10.1186/s40168-018-0428-1 | pmc = 5845141 | doi-access = free }} [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref> For example, tropical corals harbor diverse bacteria in their surface mucus layer that produce quorum-sensing inhibitors and other antibacterial compounds as a defense against colonization and infection by potential microbial pathogens.<ref name=Krediet2013 /> [[Epiphytic bacteria]] of marine macroalgae excrete a diverse chemical arsenal capable of selectively shaping further bacterial colonization and deterring the settlement of biofouling marine invertebrates such as bryozoans.<ref name=Goecke2010 /><ref>{{cite journal |doi = 10.1046/j.1529-8817.2002.02042.x|title = Chemical Mediation of Colonization of Seaweed Surfaces1|year = 2002|last1 = Steinberg|first1 = Peter D.|last2 = De Nys|first2 = Rocky|journal = Journal of Phycology|volume = 38|issue = 4|pages = 621–629| bibcode=2002JPcgy..38..621S |s2cid = 83963124}}</ref> As in corals, these diverse, microbially secreted compounds include not only bactericidal and bacteriostatic antibiotics but also compounds like halogenated furanones, cyclic dipeptides, and acyl-homoserine lactone mimics that disrupt bacterial quorum sensing and inhibit biofilm formation.<ref>{{cite journal |doi = 10.1080/08927014.2013.776042|title = Mini-review: Inhibition of biofouling by marine microorganisms|year = 2013|last1 = Dobretsov|first1 = Sergey|last2 = Abed|first2 = Raeid M.M.|last3 = Teplitski|first3 = Max|journal = Biofouling|volume = 29|issue = 4|pages = 423–441|pmid = 23574279|s2cid = 34459128|doi-access = free| bibcode=2013Biofo..29..423D }}</ref> The bacteria likely are able to utilize the carbon-rich exudates from their hosts.<ref name=Reed1996>{{cite journal |doi = 10.1002/lno.10154|title = Patterns and controls of reef-scale production of dissolved organic carbon by giant kelp M acrocystis pyrifera|year = 2015|last1 = Reed|first1 = Daniel C.|last2 = Carlson|first2 = Craig A.|last3 = Halewood|first3 = Elisa R.|last4 = Nelson|first4 = J. Clinton|last5 = Harrer|first5 = Shannon L.|last6 = Rassweiler|first6 = Andrew|last7 = Miller|first7 = Robert J.|journal = Limnology and Oceanography|volume = 60|issue = 6|pages = 1996–2008|bibcode = 2015LimOc..60.1996R| s2cid=85962482 |doi-access = free}}</ref><ref name=Vollmers2017>{{cite journal |doi = 10.1371/journal.pone.0169662|title = Comparing and Evaluating Metagenome Assembly Tools from a Microbiologist's Perspective - Not Only Size Matters!|year = 2017|last1 = Vollmers|first1 = John|last2 = Wiegand|first2 = Sandra|last3 = Kaster|first3 = Anne-Kristin|journal = PLOS ONE|volume = 12|issue = 1|pages = e0169662|pmid = 28099457|pmc = 5242441|bibcode = 2017PLoSO..1269662V| doi-access=free }}</ref> For example, in the case of giant kelp, the alga emits approximately 20% of primary production as dissolved organic carbon.<ref name=Vollmers2017 /> Whereas these prior examples illustrate how the microbiomes can protect hosts from surface colonization, a similar phenomenon has also been observed internally in the shipworm Bankia setacea, in which symbionts produce a boronated [[tartrolon]] antibiotic thought to keep the wood-digesting cecum clear of bacterial foulants.<ref>{{cite journal |doi = 10.1073/pnas.1213892110|title = Boronated tartrolon antibiotic produced by symbiotic cellulose-degrading bacteria in shipworm gills|year = 2013|last1 = Elshahawi|first1 = Sherif I.|last2 = Trindade-Silva|first2 = Amaro E.|last3 = Hanora|first3 = Amro|last4 = Han|first4 = Andrew W.|last5 = Flores|first5 = Malem S.|last6 = Vizzoni|first6 = Vinicius|last7 = Schrago|first7 = Carlos G.|last8 = Soares|first8 = Carlos A.|last9 = Concepcion|first9 = Gisela P.|last10 = Distel|first10 = Dan L.|last11 = Schmidt|first11 = Eric W.|last12 = Haygood|first12 = Margo G.|journal = Proceedings of the National Academy of Sciences|volume = 110|issue = 4|pages = E295–E304|pmid = 23288898|pmc = 3557025| doi-access=free }}</ref> By producing antimicrobial compounds, these microbes are able to defend their niche space to prevent other organisms from crowding them out.<ref name=Wilkins2019 />

==Biogeochemical cycling==
{{see also|Marine biogeochemical cycle}}

Host-associated microbiomes also influence biogeochemical cycling within ecosystems with cascading effects on biodiversity and ecosystem processes. For example, microbial symbionts comprise up to 40% of the biomass of their sponge hosts.<ref>{{cite journal |doi = 10.1126/science.1241981|title = Surviving in a Marine Desert: The Sponge Loop Retains Resources within Coral Reefs|year = 2013|last1 = De Goeij|first1 = Jasper M.|last2 = Van Oevelen|first2 = Dick|last3 = Vermeij|first3 = Mark J. A.|last4 = Osinga|first4 = Ronald|last5 = Middelburg|first5 = Jack J.|last6 = De Goeij|first6 = Anton F. P. M.|last7 = Admiraal|first7 = Wim|journal = Science|volume = 342|issue = 6154|pages = 108–110|pmid = 24092742|bibcode = 2013Sci...342..108D|s2cid = 6720678}}</ref> Through a process termed the "sponge-loop," they convert dissolved organic carbon released by reef organisms into [[particulate organic carbon]] that can be consumed by [[heterotrophic]] organisms.<ref name=Webster2016 /> Along with the coral–Symbiodiniaceae mutualism, this sponge-bacterial symbiosis helps explain Darwin's paradox, i.e., how highly productive coral reef ecosystems exist within otherwise oligotrophic tropical seas. Some sponge symbionts play a significant role in the marine phosphorus cycle by sequestering nutrients in the form of polyphosphate granules in the tissue of their host{{hsp}}<ref>{{cite journal |doi = 10.1073/pnas.1502763112|title = Sponge symbionts and the marine P cycle|year = 2015|last1 = Colman|first1 = Albert S.|journal = Proceedings of the National Academy of Sciences|volume = 112|issue = 14|pages = 4191–4192|pmid = 25825737|pmc = 4394276|bibcode = 2015PNAS..112.4191C| doi-access=free }}</ref> and nitrogen cycling, e.g., through nitrification, denitrification, and ammonia oxidation.<ref name=Webster2016 /><ref name=Pita2018 />]. Many macroalgal-associated bacteria are specifically adapted to degrade complex algal polysaccharides (e.g., fucoidan, porphyran, and laminarin{{hsp}}<ref>{{cite journal |doi = 10.1128/JB.00020-18|title = Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates|year = 2018|last1 = Corzett|first1 = Christopher H.|last2 = Elsherbini|first2 = Joseph|last3 = Chien|first3 = Diana M.|last4 = Hehemann|first4 = Jan-Hendrik|last5 = Henschel|first5 = Andreas|last6 = Preheim|first6 = Sarah P.|last7 = Yu|first7 = Xiaoqian|last8 = Alm|first8 = Eric J.|last9 = Polz|first9 = Martin F.|journal = Journal of Bacteriology|volume = 200|issue = 15|pmid = 29632094| pmc=6040190 |doi-access = free}}</ref><ref>{{cite journal |doi = 10.3354/ame01477|title = Utilization of kelp-derived carbon sources by kelp surface-associated bacteria|year = 2011|last1 = Bengtsson|first1 = MM|last2 = Sjøtun|first2 = K.|last3 = Storesund|first3 = JE|last4 = Øvreås|first4 = J.|journal = Aquatic Microbial Ecology|volume = 62|issue = 2|pages = 191–199|doi-access = free|hdl = 1956/4610|hdl-access = free}}</ref>) and modify both the quality and quantity of organic carbon supplied to the ecosystem.<ref name=Reed1996 /><ref>{{cite journal |doi = 10.1002/ecy.2798|title = Kelp beds and their local effects on seawater chemistry, productivity, and microbial communities|year = 2019|last1 = Pfister|first1 = Catherine A.|last2 = Altabet|first2 = Mark A.|last3 = Weigel|first3 = Brooke L.|journal = Ecology|volume = 100|issue = 10|pages = e02798|pmid = 31233610| bibcode=2019Ecol..100E2798P | s2cid=195355739 }}</ref> The sulfur-oxidizing gill endosymbionts of lucinid clams contribute to primary productivity through chemosynthesis and facilitate the growth of seagrasses (important foundation species) by lowering sulfide concentrations in tropical sediments.<ref>{{cite journal |doi = 10.1126/science.1219973 |title = A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems |year = 2012 |last1 = Van Der Heide |first1 = T. |last2 = Govers |first2 = L. L. |last3 = De Fouw |first3 = J. |last4 = Olff |first4 = H. |last5 = Van Der Geest |first5 = M. |last6 = Van Katwijk |first6 = M. M. |last7 = Piersma |first7 = T. |last8 = Van De Koppel |first8 = J. |last9 = Silliman |first9 = B. R. |last10 = Smolders |first10 = A. J. P. |last11 = Van Gils |first11 = J. A. |journal = Science |volume = 336 |issue = 6087 |pages = 1432–1434 |pmid = 22700927 |bibcode = 2012Sci...336.1432V |s2cid = 27806510 |url = https://research.rug.nl/en/publications/a-threestage-symbiosis-forms-the-foundation-of-seagrass-ecosystems(23625acb-7ec0-4480-98d7-fad737d7d4fe).html |hdl = 11370/23625acb-7ec0-4480-98d7-fad737d7d4fe |hdl-access = free }}</ref> Gammaproteobacterial symbionts of lucinid clams and stilbonematid nematodes were also recently shown to be capable of nitrogen fixation (bacterial symbiont genomes encode and express nitrogenase genes,<ref>{{cite journal |doi = 10.1038/nmicrobiol.2016.195 |title = Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation |year = 2017 |last1 = Petersen |first1 = Jillian M. |last2 = Kemper |first2 = Anna |last3 = Gruber-Vodicka |first3 = Harald |last4 = Cardini |first4 = Ulisse |last5 = Van Der Geest |first5 = Matthijs |last6 = Kleiner |first6 = Manuel |last7 = Bulgheresi |first7 = Silvia |last8 = Mußmann |first8 = Marc |last9 = Herbold |first9 = Craig |last10 = Seah |first10 = Brandon K.B. |last11 = Antony |first11 = Chakkiath Paul |last12 = Liu |first12 = Dan |last13 = Belitz |first13 = Alexandra |last14 = Weber |first14 = Miriam |journal = Nature Microbiology |volume = 2 |issue = 1 |page = 16195 |pmid = 27775707 |pmc = 6872982 }}</ref> highlighting the role of symbiotic microbes in nutrient cycling in shallow marine systems.<ref name=Wilkins2019 />

These examples demonstrate the importance of microbial symbioses for the functioning of ocean ecosystems. Understanding symbioses with this same level of detail in the context of complex communities (i.e., whole microbiomes) remains ripe for exploration and, indeed, requires a more integrated framework from the fields of microbiology, evolutionary biology, community ecology, and oceanography. Individual taxa within the microbiome may help hosts withstand a wide range of environmental conditions, including those predicted under scenarios of climate change. Next, we explore two different avenues of how interdisciplinary collaborations could advance this line of research.<ref name=Wilkins2019 />

==Examples==
[[File:Relationships between corals and their microbial symbionts.jpg|thumb|upright=2.4|  {{center|Relationships between corals and their microbial [[symbiont]]s <ref>Peixoto, R.S., Rosado, P.M., Leite, D.C.D.A., Rosado, A.S. and Bourne, D.G. (2017) "Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience". ''Frontiers in Microbiology'', '''8''': 341. {{doi|10.3389/fmicb.2017.00341}}.</ref>}}]]

The microbiomes of diverse marine animals are currently under study, from simplistic organisms including sponges<ref>Webster, N.S., Negri, A.P., Botté, E.S., Laffy, P.W., Flores, F., Noonan, S., Schmidt, C. and Uthicke, S. (2016) "Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification". ''Scientific reports'', '''6''': 19324. {{doi|10.1038/srep19324}}.</ref> and ctenophores <ref>Daniels, C. and Breitbart, M. (2012) "Bacterial communities associated with the ctenophores ''Mnemiopsis leidyi'' and ''Beroe ovata''". ''FEMS Microbiology Ecology'', '''82'''(1): 90–101. {{doi|10.1111/j.1574-6941.2012.01409.x}}.</ref> to more complex organisms such as sea squirts<ref>Blasiak, L.C., Zinder, S.H., Buckley, D.H. and Hill, R.T. (2014) "Bacterial diversity associated with the tunic of the model chordate ''Ciona intestinalis''". ''The ISME Journal'', '''8'''(2): 309–320. {{doi|10.1038/ismej.2013.156}}.</ref> and sharks.<ref>Givens, C.E., Ransom, B., Bano, N. and Hollibaugh, J.T. (2015) "Comparison of the gut microbiomes of 12 bony fish and 3 shark species". ''Marine Ecology Progress Series'', '''518''': 209–223. {{doi|10.3354/meps11034}}.</ref><ref name=Apprill2017 />

The relationship between the [[Hawaiian bobtail squid]] and the bioluminescent bacterium ''[[Aliivibrio fischeri]]'' is one of the best studied symbiotic relationships in the sea and is a choice system for general symbiosis research. This relationship has provided insight into fundamental processes in animal-microbial symbioses, and especially biochemical interactions and signaling between the host and bacterium.<ref>McFall-Ngai, M.J. (2000) "Negotiations between animals and bacteria: the 'diplomacy'of the squid-vibrio symbiosis". ''Comparative Biochemistry and Physiology'', ''Part A: Molecular & Integrative Physiology'', '''126'''(4): 471–480. {{doi|10.1016/S1095-6433(00)00233-6}}.</ref><ref>McFall-Ngai, M. (2014) "Divining the essence of symbiosis: insights from the squid-vibrio model". ''PLoS Biology'', '''12'''(2): e1001783. {{doi|10.1371/journal.pbio.1001783}}.</ref><ref name=Apprill2017 />

The gutless marine [[oligochaete]] worm ''[[Olavius algarvensis]]'' is another relatively well-studied marine host to microbes. These three centimetre long worms reside within shallow marine sediments of the Mediterranean Sea. The worms do not contain a mouth or a digestive or excretory system, but are instead nourished with the help of a suite of extracellular bacterial endosymbionts that reside upon coordinated use of sulfur present in the environment.<ref>Dubilier, N., Mülders, C., Ferdelman, T., de Beer, D., Pernthaler, A., Klein, M., Wagner, M., Erséus, C., Thiermann, F., Krieger, J. and Giere, O. (2001) "Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm". ''Nature'', '''411'''(6835): 298–302. {{doi|10.1038/35077067}}.</ref> This system has benefited from some of the most sophisticated 'omics and visualization tools.<ref name=Woyke2006>Woyke, T., Teeling, H., Ivanova, N.N., Huntemann, M., Richter, M., Gloeckner, F.O., Boffelli, D., Anderson, I.J., Barry, K.W., Shapiro, H.J. and Szeto, E. (2006) "Symbiosis insights through metagenomic analysis of a microbial consortium". ''Nature'', '''443'''(7114): 950–955. {{doi|10.1038/nature05192}}.</ref> For example, multi-labeled probing has improved visualization of the microbiome<ref>Schimak, M.P., Kleiner, M., Wetzel, S., Liebeke, M., Dubilier, N. and Fuchs, B.M. (2016) "MiL-FISH: Multilabeled oligonucleotides for fluorescence in situ hybridization improve visualization of bacterial cells". ''Applied and Environmental Microbiology'', '''82'''(1): 62–70. {{doi|10.1128/AEM.02776-15}}.</ref> and transcriptomics and proteomics have been applied to examine host–microbiome interactions, including energy transfer between the host and microbes<ref>Kleiner, M., Wentrup, C., Lott, C., Teeling, H., Wetzel, S., Young, J., Chang, Y.J., Shah, M., VerBerkmoes, N.C., Zarzycki, J. and Fuchs, G. (2012) "Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use". ''Proceedings of the National Academy of Sciences'', '''109'''(19): E1173–E1182. {{doi|10.1073/pnas.1121198109}}.</ref> and recognition of the consortia by the worm's innate immune system.<ref>Wippler, J., Kleiner, M., Lott, C., Gruhl, A., Abraham, P.E., Giannone, R.J., Young, J.C., Hettich, R.L. and Dubilier, N. (2016) "Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm ''Olavius algarvensis''". ''BMC Genomics'', '''17'''(1): 942. {{doi|10.1186/s12864-016-3293-y}}.</ref> The major strength of this system is that it does offer the ability to study host–microbiome interactions with a low diversity microbial consortium, and it also offers a number of host and microbial genomic resources<ref name=Woyke2006 /><ref>Ruehland, C., Blazejak, A., Lott, C., Loy, A., Erséus, C. and Dubilier, N. (2008) "Multiple bacterial symbionts in two species of co‐occurring gutless oligochaete worms from Mediterranean sea grass sediments". ''Environmental microbiology'', '''10'''(12): 3404–3416. {{doi|10.1111/j.1462-2920.2008.01728.x}}.</ref><ref name=Apprill2017 />

===Corals===
[[File:Bacterial OTUs from clone libraries and next-generation sequencing.png|thumb|upright=1.7| Phylogenetic tree representing bacterial OTUs from [[clone libraries]] and [[next-generation sequencing]]. OTUs from next-generation sequencing are displayed if the OTU contained more than two sequences in the unrarefied OTU table (3626 OTUs).<ref>{{cite journal |doi = 10.1186/s40168-017-0329-8|title = Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata|year = 2017|last1 = Sharp|first1 = Koty H.|last2 = Pratte|first2 = Zoe A.|last3 = Kerwin|first3 = Allison H.|last4 = Rotjan|first4 = Randi D.|last5 = Stewart|first5 = Frank J.|journal = Microbiome|volume = 5|issue = 1|page = 120|pmid = 28915923|pmc = 5603060 | doi-access=free }}</ref>]]

[[Coral]]s  are one of the more common examples of an animal host whose symbiosis with microalgae can turn to dysbiosis, and is visibly detected as bleaching. Coral microbiomes have been examined in a variety of studies, which demonstrate how variations in the ocean environment, most notably temperature, light, and inorganic nutrients, affect the abundance and performance of the microalgal symbionts, as well as [[calcification]] and physiology of the host.<ref>Dubinsky, Z. and Jokiel, P.L. (1994) "Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals". ''Pacific Science'', '''48'''(3): 313–324.</ref><ref>Anthony, K.R., Kline, D.I., Diaz-Pulido, G., Dove, S. and Hoegh-Guldberg, O.(2008) "Ocean acidification causes bleaching and productivity loss in coral reef builders". ''Proceedings of the National Academy of Sciences'', '''105'''(45): 17442–17446. {{doi|10.1073/pnas.0804478105}}.</ref><ref name=Apprill2017 />

Studies have also suggested that resident bacteria, archaea, and fungi additionally contribute to nutrient and organic matter cycling within the coral, with viruses also possibly playing a role in structuring the composition of these members, thus providing one of the first glimpses at a multi-domain marine animal symbiosis.<ref>Bourne, D.G., Morrow, K.M. and Webster, N.S. (2016) "Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems". ''Annual Review of Microbiology'', '''70''': 317–340. {{doi|10.1146/annurev-micro-102215-095440}}.</ref> The [[gammaproteobacterium]] ''[[Endozoicomonas]]'' is emerging as a central member of the coral's microbiome, with flexibility in its lifestyle.<ref name=Neave2016>Neave, M.J., Apprill, A., Ferrier-Pagès, C. and Voolstra, C.R. (2016) "Diversity and function of prevalent symbiotic marine bacteria in the genus ''Endozoicomonas''". ''Applied Microbiology and Biotechnology'', '''100'''(19): 8315–8324. {{doi|10.1007/s00253-016-7777-0}}.</ref><ref>Neave, M.J., Michell, C.T., Apprill, A. and Voolstra, C.R. (2017) "Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts". ''Scientific Reports'', '''7''': 40579. {{doi|10.1038/srep40579}}.</ref> Given the recent mass bleaching occurring on reefs,<ref>Hughes, T.P., Kerry, J.T., Álvarez-Noriega, M., Álvarez-Romero, J.G., Anderson, K.D., Baird, A.H., Babcock, R.C., Beger, M., Bellwood, D.R., Berkelmans, R. and Bridge, T.C. (2017) "Global warming and recurrent mass bleaching of corals". ''Nature'', '''543'''(7645): 373–377. {{doi|10.1038/nature21707}}.</ref> corals will likely continue to be a useful and popular system for symbiosis and dysbiosis research.<ref name=Apprill2017 />

''[[Astrangia poculata]]'', the northern star coral, is a temperate [[stony coral]], widely documented along the eastern coast of the United States. The coral can live with and without [[zooxanthellae]] (algal symbionts), making it an ideal [[model organism]] to study microbial community interactions associated with symbiotic state. However, the ability to develop [[Primer (molecular biology)|primers]] and [[Molecular probe|probes]] to more specifically target key microbial groups has been hindered by the lack of full length [[16S rRNA]] sequences, since sequences produced by the Illumina platform are of insufficient length (approximately 250 base pairs) for the design of primers and probes.<ref>[https://www.usgs.gov/center-news/usgs-scientists-publish-long-read-microbiome-sequences-temperate-coral-providing?qt-news_science_products=3#qt-news_science_products USGS scientists publish long-read microbiome sequences from temperate coral, providing community resource for probe and primer design], ''United States Geological Survey'', 6 March 2019. [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref> In 2019, Goldsmith et al demonstrated [[Sanger sequencing]] was capable of reproducing the biologically-relevant diversity detected by deeper [[next-generation sequencing]], while also producing longer sequences useful to the research community for probe and primer design (see diagram on right).<ref name=Goldsmith2019>{{cite journal |doi = 10.3934/microbiol.2019.1.62|title = Stability of temperate coral ''Astrangia poculata'' microbiome is reflected across different sequencing methodologies|year = 2019|last1 = b. Goldsmith|first1 = Dawn|last2 = a. Pratte|first2 = Zoe|last3 = a. Kellogg|first3 = Christina|last4 = e. Snader|first4 = Sara|last5 = h. Sharp|first5 = Koty|journal = AIMS Microbiology|volume = 5|issue = 1|pages = 62–76|pmid = 31384703|pmc = 6646935}} [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref>

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===Sponges===
{{main|Sponge microbiomes}}
[[Sponge]]s are common members of the ocean's diverse benthic habitats and their abundance and ability to filter large volumes of seawater have led to the awareness that these organisms play critical roles in influencing benthic and pelagic processes in the ocean.<ref>Bell, J.J. (2008) "The functional roles of marine sponges". ''Estuarine, Coastal and Shelf Science'', '''79'''(3): 341–353. {{doi|10.1016/j.ecss.2008.05.002}}.</ref> They are one of the oldest lineages of animals, and have a relatively simple body plan that commonly associates with bacteria, archaea, algal protists, fungi, and viruses.<ref name=Webster2016 /> Sponge microbiomes are composed of specialists and generalists, and complexity of their microbiome appears to be shaped by host phylogeny.<ref>Thomas, T., Moitinho-Silva, L., Lurgi, M., Björk, J.R., Easson, C., Astudillo-García, C., Olson, J.B., Erwin, P.M., López-Legentil, S., Luter, H. and Chaves-Fonnegra, A. (2016) "Diversity, structure and convergent evolution of the global sponge microbiome". ''Nature Communications'', '''7'''(1): 1-12. {{doi|10.1038/ncomms11870}}.</ref> Studies have shown that the sponge microbiome contributes to nitrogen cycling in the oceans, especially through the oxidation of ammonia by archaea and bacteria.<ref>Bayer, K., Schmitt, S. and Hentschel, U. (2008) "Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge ''Aplysina aerophoba''". ''Environmental Microbiology'', '''10'''(11): 2942–2955. {{doi|10.1111/j.1462-2920.2008.01582.x}}.</ref><ref>Radax, R., Hoffmann, F., Rapp, H.T., Leininger, S. and Schleper, C. (2012) "Ammonia‐oxidizing archaea as main drivers of nitrification in cold‐water sponges". ''Environmental Microbiology'', '''14'''(4): 909_923. {{doi|10.1111/j.1462-2920.2011.02661.x}}.
</ref> Most recently, microbial symbionts of tropical sponges were shown to produce and store polyphosphate granules,<ref>Zhang, F., Blasiak, L.C., Karolin, J.O., Powell, R.J., Geddes, C.D. and Hill, R.T. (2015) "Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges". ''Proceedings of the National Academy of Sciences'', '''112'''(14): 4381–4386. {{doi|10.1073/pnas.1423768112}}.</ref> perhaps enabling the host to survive periods of phosphate depletion in oligotrophic marine environments.<ref>Colman, A.S. (2015) "Sponge symbionts and the marine P cycle". ''Proceedings of the National Academy of Sciences'', '''112'''(14): 4191–4192. {{doi|10.1073/pnas.1502763112}}.</ref> The microbiomes of some sponge species do appear to change in community structure in response to changing environmental conditions, including temperature<ref>Simister, R., Taylor, M.W., Tsai, P., Fan, L., Bruxner, T.J., Crowe, M.L. and Webster, N. (2012) "Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, ''Rhopaloeides odorabile''. ''Environmental Microbiology'', '''14'''(12): 3232–3246. {{doi|10.1111/1462-2920.12010}}.</ref> and ocean acidification,<ref>Morrow, K.M., Bourne, D.G., Humphrey, C., Botté, E.S., Laffy, P., Zaneveld, J., Uthicke, S., Fabricius, K.E. and Webster, N.S. (2015) "Natural volcanic CO 2 seeps reveal future trajectories for host–microbial associations in corals and sponges". ''The ISME Journal'', '''9'''(4): 894–908. {{doi|10.1038/ismej.2014.188}}.</ref><ref>Ribes, M., Calvo, E., Movilla, J., Logares, R., Coma, R. and Pelejero, C. (2016) "Restructuring of the sponge microbiome favors tolerance to ocean acidification''. ''Environmental Microbiology Reports'', '''8'''(4): 536–544. {{doi|10.1111/1758-2229.12430}}.</ref> as well as synergistic impacts.<ref>Lesser, M.P., Fiore, C., Slattery, M. and Zaneveld, J. (2016) "Climate change stressors destabilize the microbiome of the Caribbean barrel sponge, ''Xestospongia muta''". ''Journal of Experimental Marine Biology and Ecology'', '''475''': 11–18. {{doi|10.1016/j.jembe.2015.11.004}}.</ref>

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[[File:Whale_blow_sampling_with_drone.png|thumb|upright=1| Collecting a sample of blow from a [[blue whale]] using a helicopter drone{{hsp}}<ref name = "Acevedo-Whitehouse_2010">{{cite journal | vauthors = Acevedo-Whitehouse K, Rocha-Gosselin A, Gendron D | title = A novel non-invasive tool for disease surveillance of free-ranging whales and its relevance to conservation programs. | journal = Animal Conservation | date = April 2010 | volume = 13 | issue = 2 | pages = 217–225 | doi = 10.1111/j.1469-1795.2009.00326.x | s2cid = 86518859 }}</ref>]]

===Cetaceans===
{{main|Cetacean microbiome}}

[[File:Cetacean_blow's_bacteria.png|thumb|upright=1| Relative abundance of bacterial classes identified in sampled whale blow, air and seawater.<ref name="Pirotta_2017" />]]

The access of microbial samples from the gut out of marine mammals is limited because most species are rare, endangered, and deep divers. There are different techniques for sampling the cetacean's gut microbiome. The most common is collecting fecal samples from the environment and taking a probe from the center that is non-contaminated.<ref name="Suzuki_2019">{{cite journal | vauthors = Suzuki A, Ueda K, Segawa T, Suzuki M | title = Fecal microbiota of captive Antillean manatee Trichechus manatus manatus | journal = FEMS Microbiology Letters | volume = 366 | issue = 11 | pages = | date = June 2019 | pmid = 31210263 | doi = 10.1093/femsle/fnz134 | url = }}</ref> Besides there are studies from rectal swabs and rare studies from stranded dead or living animals direct from the intestine.<ref name="Sehnal_2021">{{cite journal | vauthors = Sehnal L, Brammer-Robbins E, Wormington AM, Blaha L, Bisesi J, Larkin I, Martyniuk CJ, Simonin M, Adamovsky O | title = Microbiome Composition and Function in Aquatic Vertebrates: Small Organisms Making Big Impacts on Aquatic Animal Health | journal = Frontiers in Microbiology | volume = 12 | issue = | pages = 567408 | date = 2021 | pmid = 33776947 | pmc = 7995652 | doi = 10.3389/fmicb.2021.567408 | doi-access = free }}</ref><ref name="Bik_2016">{{cite journal | vauthors = Bik EM, Costello EK, Switzer AD, Callahan BJ, Holmes SP, Wells RS, Carlin KP, Jensen ED, Venn-Watson S, Relman DA | title = Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea | journal = Nature Communications | volume = 7 | issue = | pages = 10516 | date = February 2016 | pmid = 26839246 | pmc = 4742810 | doi = 10.1038/ncomms10516 | bibcode = 2016NatCo...710516B }}</ref><ref name="Bai_2021">{{cite journal | vauthors = Bai S, Zhang P, Lin M, Lin W, Yang Z, Li S | title = Microbial diversity and structure in the gastrointestinal tracts of two stranded short-finned pilot whales (Globicephala macrorhynchus) and a pygmy sperm whale (Kogia breviceps) | journal = Integrative Zoology | volume = 16 | issue = 3 | pages = 324–335 | date = May 2021 | pmid = 33174288 | doi = 10.1111/1749-4877.12502 | s2cid = 226302293 | pmc = 9292824 }}</ref>

The outermost epidermal layer, i.e. the skin, is the first barrier that protects the individual from the outside world and the epidermal microbiome on it is considered an indicator not only of the health of the animal but is also considered an ecological indicator that shows the state of the surrounding environment. Knowing the microbiome of the skin of marine mammals under <nowiki>''normal''</nowiki> conditions has allowed us to understand how these communities are different from the free microbial communities found in the sea and how they can change according to abiotic and biotic variations, and also <nowiki>''</nowiki>''communities vary between healthy and sick individuals<nowiki>''</nowiki>''.<ref>{{cite journal | vauthors = Apprill A, Mooney TA, Lyman E, Stimpert AK, Rappé MS | title = Humpback whales harbour a combination of specific and variable skin bacteria | journal = Environmental Microbiology Reports | volume = 3 | issue = 2 | pages = 223–232 | date = April 2011 | pmid = 23761254 | doi = 10.1111/j.1758-2229.2010.00213.x | bibcode = 2011EnvMR...3..223A }}</ref>

[[Cetacea]]ns are in danger because they are affected by multiple stress factors which make them more vulnerable to various diseases. These animals have been noted to show high susceptibility to airway infections, but very little is known about their respiratory microbiome. Therefore, the sampling of the exhaled breath or "blow" of the cetaceans can provide an assessment of the state of health. Blow is composed of a mixture of [[microorganism]]s and [[Organic matter|organic material]], including [[lipid]]s, [[protein]]s , and cellular debris derived from the linings of the airways which, when released into the relatively cooler outdoor air, condense to form a visible mass of vapor, which can be collected. There are various methods for collecting exhaled breath samples, one of the most recent is through the use of aerial drones. This method provides a safer, quieter, and less invasive alternative and often a cost-effective option for monitoring fauna and flora. Once obtained, the blow samples are taken to the laboratory and we proceed with the amplification and sequencing of the respiratory tract microbiota. The use of aerial drones has been more successful with large cetaceans due to slow swim speeds and larger blow sizes.<ref name="Pirotta_2017">{{cite journal | vauthors = Pirotta V, Smith A, Ostrowski M, Russell D, Jonsen ID, Grech A, Harcourt R | title = An economical custom-built drone for assessing whale health. | journal = Frontiers in Marine Science | date = December 2017 | volume = 4 | pages = 425 | doi =  10.3389/fmars.2017.00425 | doi-access = free }}</ref><ref name="Apprill_2017">{{cite journal | vauthors = Apprill A, Miller CA, Moore MJ, Durban JW, Fearnbach H, Barrett-Lennard LG | title = Extensive Core Microbiome in Drone-Captured Whale Blow Supports a Framework for Health Monitoring | journal = mSystems | volume = 2 | issue = 5 | pages = | date = 2017 | pmid = 29034331 | pmc = 5634792 | doi = 10.1128/mSystems.00119-17 }}</ref><ref name="Vendl_2019">{{cite journal | vauthors = Vendl C, Ferrari BC, Thomas T, Slavich E, Zhang E, Nelson T, Rogers T | title = Interannual comparison of core taxa and community composition of the blow microbiota from East Australian humpback whales | journal = FEMS Microbiology Ecology | volume = 95 | issue = 8 | pages = | date = August 2019 | pmid = 31260051 | doi = 10.1093/femsec/fiz102 | doi-access = free }}</ref><ref name="Johnson_2009">{{cite journal | vauthors = Johnson WR, Torralba M, Fair PA, Bossart GD, Nelson KE, Morris PJ | title = Novel diversity of bacterial communities associated with bottlenose dolphin upper respiratory tracts | journal = Environmental Microbiology Reports | volume = 1 | issue = 6 | pages = 555–62 | date = December 2009 | pmid = 23765934 | doi = 10.1111/j.1758-2229.2009.00080.x | bibcode = 2009EnvMR...1..555J }}</ref><ref name="Centelleghe_2020">{{cite journal | vauthors = Centelleghe C, Carraro L, Gonzalvo J, Rosso M, Esposti E, Gili C, Bonato M, Pedrotti D, Cardazzo B, Povinelli M, Mazzariol S | title = The use of Unmanned Aerial Vehicles (UAVs) to sample the blow microbiome of small cetaceans | journal = PLOS ONE | volume = 15 | issue = 7 | pages = e0235537 | date = 2020 | pmid = 32614926 | pmc = 7332044 | doi = 10.1371/journal.pone.0235537 | bibcode = 2020PLoSO..1535537C | doi-access = free }}</ref><ref name="Acevedo-Whitehouse_2010" /><ref name="Raverty_2017">{{cite journal | vauthors = Raverty SA, Rhodes LD, Zabek E, Eshghi A, Cameron CE, Hanson MB, Schroeder JP | title = Respiratory Microbiome of Endangered Southern Resident Killer Whales and Microbiota of Surrounding Sea Surface Microlayer in the Eastern North Pacific | journal = Scientific Reports | volume = 7 | issue = 1 | pages = 394 | date = March 2017 | pmid = 28341851 | pmc = 5428453 | doi = 10.1038/s41598-017-00457-5 | bibcode = 2017NatSR...7..394R }}</ref><ref name="Lima_2012">{{cite journal | vauthors = Lima N, Rogers T, Acevedo-Whitehouse K, Brown MV | title = Temporal stability and species specificity in bacteria associated with the bottlenose dolphins respiratory system | journal = Environmental Microbiology Reports | volume = 4 | issue = 1 | pages = 89–96 | date = February 2012 | pmid = 23757234 | doi = 10.1111/j.1758-2229.2011.00306.x | bibcode = 2012EnvMR...4...89L }}</ref><ref name="Geoghegan_2018">{{cite journal | vauthors = Geoghegan JL, Pirotta V, Harvey E, Smith A, Buchmann JP, Ostrowski M, Eden JS, Harcourt R, Holmes EC | title = Virological Sampling of Inaccessible Wildlife with Drones | journal = Viruses | volume = 10 | issue = 6 | date = June 2018 | page = 300 | pmid = 29865228 | pmc = 6024715 | doi = 10.3390/v10060300 | doi-access = free }}</ref>
 
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==Marine holobionts==
{{main|Marine holobiont}}

Reef-building corals are holobionts that include the coral itself (a eukaryotic [[invertebrate]] within class [[Anthozoa]]), [[Photosynthesis|photosynthetic]] [[dinoflagellate]]s called [[zooxanthellae]] (''[[Symbiodinium]]''), and associated bacteria and viruses.<ref name=Knowlton2003>{{cite journal | vauthors = Knowlton N, Rohwer F | title = Multispecies microbial mutualisms on coral reefs: the host as a habitat | journal = The American Naturalist | volume = 162 | issue = 4 Suppl | pages = S51–62 | date = October 2003 | pmid = 14583857 | doi = 10.1086/378684 | s2cid = 24127308 }}</ref> Co-evolutionary patterns exist for coral microbial communities and coral phylogeny.<ref>{{cite journal | vauthors = Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL, Medina M, Thurber RV, Zaneveld JR | title = Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny | journal = Nature Communications | volume = 9 | issue = 1 | pages = 4921 | date = November 2018 | pmid = 30467310 | pmc = 6250698 | doi = 10.1038/s41467-018-07275-x | doi-access = free | bibcode = 2018NatCo...9.4921P }}</ref>

<gallery mode=packed style=float:left; heights=160px>
File:Trophic connections of the coral holobiont in the planktonic food web.jpg| [[Coral holobiont]]<ref name="pmid25621279">{{cite journal | vauthors = Thompson JR, Rivera HE, Closek CJ, Medina M | title = Microbes in the coral holobiont: partners through evolution, development, and ecological interactions | journal = Frontiers in Cellular and Infection Microbiology | volume = 4 | issue = | pages = 176 | date = 2014 | pmid = 25621279 | doi = 10.3389/fcimb.2014.00176 | pmc = 4286716 | doi-access = free }}</ref>
File:Processes within the seagrass holobiont.webp| [[Seagrass holobiont]]<ref name="Ugarelli2017">{{cite journal | vauthors = Ugarelli K, Chakrabarti S, Laas P, Stingl U | title = The Seagrass Holobiont and Its Microbiome | journal = Microorganisms | volume = 5 | issue = 4 | date = December 2017 | page = 81 | pmid = 29244764 | doi = 10.3390/microorganisms5040081 | pmc = 5748590 | doi-access = free }} [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License</ref>
File:The sponge holobiont.webp| [[Sponge holobiont]]<ref name=Pita2018 />
File:Climate change stressors and rhodolith holobiont fitness.webp| {{center|[[Rhodolith#Climate change and the rhodolith holobiont|Climate change and the rhodolith holobiont]]<ref name=Cavalcanti2018>{{cite journal | vauthors = Cavalcanti GS, Shukla P, Morris M, Ribeiro B, Foley M, Doane MP, Thompson CC, Edwards MS, Dinsdale EA, Thompson FL | title = Rhodoliths holobionts in a changing ocean: host-microbes interactions mediate coralline algae resilience under ocean acidification | journal = BMC Genomics | volume = 19 | issue = 1 | pages = 701 | date = September 2018 | pmid = 30249182 | doi = 10.1186/s12864-018-5064-4 | pmc = 6154897 | url =  | doi-access = free }} [[File:CC-BY icon.svg|50px]] Modified text was copied from this source, which is available under a [https://creativecommons.org/licenses/by/4.0/ Creative Commons Attribution 4.0 International License].</ref>}}
</gallery>

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==References==
{{reflist}}

==Further references==
* Stal, L. J. and Cretoiu, M. S. (Eds.) (2016) [https://books.google.com/books?id=MJ1PDAAAQBAJ&q=%22The+marine+microbiome%3A+an+untapped+source+of+biodiversity+and+biotechnological+potential%22 ''The marine microbiome: an untapped source of biodiversity and biotechnological potential''] Springer. {{ISBN|9783319330006}}.
* {{cite book | title=Marine Microbiome and Biogeochemical Cycles in Marine Productive Areas | publisher=Frontiers Media S.A | date=2020 | isbn=978-2-88963-276-3 | oclc=1291256407 | ref={{sfnref | Frontiers Media S.A}}}}

[[Category:Microbiomes]]