Diversity, structure and convergent evolution of the global sponge microbiome

Nature Communications, Journal Year: 2016, Volume and Issue: 7(1)

Published: June 16, 2016

Abstract Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host–microbe interactions. We show that sponges reservoir exceptional diversity major contributors total world’s oceans. Little commonality in species composition or structure is evident across phylum, although symbiont communities characterized by specialists generalists rather than opportunists. Core sponge microbiomes stable generalist symbionts exhibiting amensal and/or commensal Symbionts phylogenetically unique do not disproportionally contribute core microbiome, host phylogeny impacts complexity community. Our findings support model independent assembly evolution entire with convergent forces resulting analogous community organization

Language: Английский

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Diet of Worms Emended: An Update of Polychaete Feeding Guilds

Annual Review of Marine Science, Journal Year: 2014, Volume and Issue: 7(1), P. 497 - 520

Published: Sept. 24, 2014

Polychaetes are common in most marine habitats and dominate many infaunal communities. Functional guild classification based on taxonomic identity morphology has linked community structure to ecological function. The functional guilds now include osmotrophic siboglinids as well sipunculans, echiurans, myzostomes, which molecular genetic analyses have placed within Annelida. Advances understanding of encounter mechanisms explicitly relate motility feeding mode. New burrowing mechanics explain the prevalence bilateral symmetry blur boundary between surface subsurface feeding. dichotomy microphagous deposit suspension feeders macrophagous carnivores, herbivores, omnivores is further supported by divergent digestive strategies. Deposit appears be limited largely worms longer than 1 cm, with juveniles small general restricted ingesting highly digestible organic material larger, rich food items, blurring macrophage-microphage that applies larger worms.

Language: Английский

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Nitrogen cycling in corals: the key to understanding holobiont functioning?

Trends in Microbiology, Journal Year: 2015, Volume and Issue: 23(8), P. 490 - 497

Published: April 11, 2015

•Nitrogen cycling in reef-building corals is a function of all holobiont members.•Control nitrogen may stabilize functioning under oligotrophic and eutrophic conditions.•Anthropogenic change sway the control cycling, promoting coral decline.•Elevated fixation rates foster bleaching disease. Corals are animals that form close mutualistic associations with endosymbiotic photosynthetic algae genus Symbiodinium. Together they provide calcium carbonate framework reef ecosystems. The importance microbiome (i.e., bacteria, archaea, fungi, viruses) to has only recently been recognized. Given growth density Symbiodinium within host highly dependent on availability, nitrogen-cycling microbes be fundamental stability coral–algae symbiosis functioning, particular nutrient-enriched -depleted scenarios. We summarize what known about conclude disturbance microbial tightly linked Tropical commonly flourish nutrient-poor environments. contradiction high productivity one hand limited nutrient availability other coined 'Darwin Paradox' reference its first observer [1Darwin C. Structure Distribution Coral Reefs. Smith, Elder Co, 1842Google Scholar, 2Sammarco P.W. et al.Cross-continental shelf trends δ15N Great Barrier Reef: further consideration paradox.Mar. Ecol. Prog. Ser. 1999; 180: 131-138Crossref Scopus (76) Google Scholar]. efficient uptake recycling nutrients by organisms can help explain this paradox [3De Goeij J.M. al.Surviving marine desert: sponge loop retains resources reefs.Science. 2013; 342: 108-111Crossref PubMed (489) 4Wild al.Coral mucus functions as an energy carrier particle trap ecosystem.Nature. 2004; 428: 66-70Crossref (442) Particularly for corals, association between animal dinoflagellate enables effective use retention photosynthates, is, photosynthetically fixed carbon [5Muscatine L. Porter J.W. Reef corals: symbioses adapted environments.Bioscience. 1977; 27: 454-460Crossref their algal symbionts, associated variety microorganisms, including protozoans, bacteria [6Ainsworth T.D. al.The future reefs: perspective.Trends Evol. 2010; 25: 233-240Abstract Full Text PDF (175) 7Rohwer F. al.Diversity distribution coral-associated bacteria.Mar. 2002; 243: 1-10Crossref (857) Scholar], assemblage termed (see Glossary). resulting meta-organism represents complex interactive system potential extend physiological capabilities [8Rosenberg E. role microorganisms health, disease evolution.Nat. Rev. Microbiol. 2007; 5: 355-362Crossref (913) Hence, knowledge underlying mechanisms interactions essential comprehend response environmental change, such ocean acidification, warming, eutrophication. Distinct assemblages surface layer, tissue, gastro-vascular cavity, skeleton This habitats results diverse where potentially perform multitude services fixation, metabolism, sulfur antimicrobial defense among many others 9Wegley al.Metagenomic analysis community Porites astreoides.Environ. 9: 2707-2719Crossref (400) 10Kimes N.E. al.Microbial functional structure Montastraea faveolata, important Caribbean coral, differs healthy yellow-band diseased colonies.Environ. 12: 541-556Crossref (133) 11Krediet C.J. al.Coral-associated micro-organisms roles health thwarting diseases.Proc. Biol. Sci. 280: 20122328Crossref (194) Owing different groups holobiont, have evolved enable intergenerational transfer specific ensure offspring fitness [12Ceh J. al.Intergenerational possible implications fitness.Microb. 65: 227-231Crossref (40) 13Hirose M. al.Timing process entry zooxanthellae into oocytes hermatypic corals.Coral 2001; 20: 273-280Crossref (43) vertical presumably facilitated evolution host-specific persistent communities [14Bayer T. red sea stylophora pistillata dominated tissue-associated endozoicomonas bacteria.Appl. Environ. 79: 4759-4762Crossref (188) 15Roder al.Bacterial profiling white plague comparative species framework.ISME 2014; 8: 31-39Crossref (99) 16Lema K.A. al.Corals characteristic symbiotic nitrogen-fixing 2012; 78: 3136-3144Crossref (177) 17Lema al.Amplicon pyrosequencing reveals spatial temporal consistency diazotroph Acropora millepora microbiome.Environ. 16: 3345-3349Crossref (69) 18Lema K.a. al.Onset establishment diazotrophs bacterial associates early life history stages millepora.Mol. 23: 4682-4695Crossref (71) In context, Reshef al. [19Reshef probiotic hypothesis.Environ. 2006; 2068-2073Crossref (418) Scholar] proposed hypothesis – stating that, despite presence consistent communities, alterations rapidly adjust conditions (Box 1).Box 1The hypothesisCorals harbor archaea bacteria. Changing alter composition abundance rapidly. colleagues 'coral hypothesis' dynamic relationship selects most advantageous varying conditions. Therefore, shifts facilitate adjustment changing considerably faster than mutation selection alone. implies combined rather individual members unit natural selection, led development 'hologenome theory evolution' Scholar].Some studies suggest changes acting select partners which beneficial [94Silverstein R.N. al.Change symbiont after bleaching, not prior heat exposure, increases tolerance corals.Glob. Change 2015; 21: 236-249Crossref 95Hume B.C.C. al.Symbiodinium thermophilum sp. nov., thermotolerant alga prevalent world's hottest sea, Persian/Arabian Gulf.Sci. Rep. 8562Crossref (171) particular, resistance lack adaptive immune system, highlights [96Nissimov al.Antimicrobial properties resident Oculina patagonica.FEMS Lett. 2009; 292: 210-215Crossref Scholar].It shown affect [46Rädecker N. al.Ocean acidification reduces dinitrogen Seriatopora hystrix.Mar. 511: 297-302Crossref (28) soft supplement reduced Red Sea [97Bednarz V.N. al.Seasonal variation oxygen fluxes two dominant zooxanthellate from northern Sea.Mar. 519: 141-152Crossref (36) It likely these capacity microbiome. accordance hypothesis, serve means adapt availability. Some appear ubiquitous 20Olson N.D. Lesser M.P. Diazotrophic diversity cavernosa.Arch. 195: 853-859Crossref (26) 21Fiore C.L. al.Nitrogen transformations symbioses.Trends 18: 455-463Abstract (149) production [22Falkowski P.G. al.Population corals.Bioscience. 1993; 43: 606-611Crossref (311) 23Béraud scleractinian Turbinaria reniformis thermal stress depends status holobiont.J. Exp. 216: 2665-2674Crossref (64) factors crucial acquisition sustain primary photosynthesis). review we current symbiosis. Furthermore, discuss effects pathways focus putative occurrence deleterious assimilation nitrogen. Heterotrophic feeding meet large part requirements if sufficient food available [24Houlbrèque Ferrier-Pagès Heterotrophy tropical corals.Biol. Camb. Philos. Soc. 84: 1-17Crossref (430) addition, acquire forms foundation holobionts shallow-water reefs. association, phototrophic dinoflagellates photosynthates host. However, translocated referred 'junk food' because show C:N ratio therefore require additional supplementation [25Falkowski P. al.Light bioenergetics coral.Bioscience. 1984; 34: 705-709Crossref benefit inorganic released metabolic waste products 26Rahav O. al.Ammonium metabolism Stylophora pistillata.Proc. 1989; 236: 325-337Crossref Their utilization dissolved (DIN) facilitates surrounding seawater. Although both enzymatic machinery incorporate ammonium, account environment, mainly ammonium (NH4+) nitrate (NO3−) [27Pernice al.A single-cell view coral-dinoflagellate symbiosis.ISME 6: 1314-1324Crossref (172) nitrogen, together host-derived compounds, either stored or used partially organic example, amino acids [28Wang J.T. Douglas a.E. Essential acid synthesis alga-invertebrate symbiosis.Mar. 135: 219-222Crossref (108) 29Kopp al.Highly cellular-level sudden increase nitrogen.mBio. 4: 1-9Crossref (1) 30Reynaud S. al.Effect light isotopic coral: recycling.Mar. 392: 103-110Crossref thus compounds sources reefs, however, underlies strong seasonal diel variations, affected anthropogenic activities [31D'Angelo Wiedenmann Impacts enrichment new perspectives coastal management survival.Curr. Opin. Sustain. 7: 82-93Crossref (267) Consequently, internal regulation need place fluctuations. At least three identified exert over symbionts: (i) so-called release (HRFs), trigger freshly isolated [32Gates R.D. al.Free exhibit anthozoan 'host factor' activity: induce photosynthate vitro.Proc. Natl. Acad. U.S.A. 1995; 92: 7430-7434Crossref (117) 33Wang A.E. Nutrients, signals, algae.Plant Physiol. 1997; 114: 631-636Crossref (102) 34Cook C.B. Davy S.K. Are free responsible extracts tissue?.Hydrobiologia. 461: 71-78Crossref (29) These HRFs nutrition (via unknown mechanisms). (ii) Control numbers degradation/digestion [35Titlyanov E.A. al.Degradation corals.Mar. 1996; 139: 167-178Crossref (121) Via contained symbionts. (iii) limiting Nitrogen limitation regulate cell division faster-proliferating match those [36Yellowlees D. al.Metabolic symbionts invertebrate hosts.Plant Cell 2008; 31: 679-694Crossref (357) 37Muscatine effect external population dynamics coral.Proc. R. Lond. B: 311-324Crossref (250) translocation maintain favorable proceeds intense environments [38Dubinsky Z. Jokiel P.L. Ratio regulates corals.Pac. 1994; 48: 313-324Google [39Wiedenmann al.Nutrient susceptibility bleaching.Nat. Clim. Change. 2: 1-5Crossref showed shift away excess provision ultimately result phosphate starvation, stress-mediated loss (coral bleaching). low specifically seems production, while simultaneously controlling growth. ability assimilate suggested allow more seawater maintaining diffusion gradient enabling 36Yellowlees 40Wooldridge S.A. Breakdown coral-algae symbiosis: towards formalising linkage warm-water thresholds rate intracellular zooxanthellae.Biogeosciences. 10: 1647-1658Crossref (83) same time, symbiosome pH ions [41Barott K.L. cells acidify microenvironment promote photosynthesis.Proc. 112: 607-612Crossref (100) mechanism contributing stabilization, conversely destabilization, reefs net [42Webb al.Enewetak (Eniwetok) Atoll: aspects cycle reef.Limnol. Oceanogr. 1975; 198-210Crossref (97) words conversion elemental (N2) substrates (e.g., sand, rock, rubble) benthic macroalgae, sponges) [21Fiore 43Cardini U. al.Benthic N2 human-induced change.Ecol. 1706-1727Crossref (63) input ecosystem helps compensate export instance currents [44Wiebe W.J. community.Science. 188: 257-259Crossref (124) reported several [45Shashar (acetylene reduction) stony evidence coral-bacteria interactions.Mar. 111: 259-264Crossref (142) 46Rädecker 47Grover corals.J. 217: 3962-3963Crossref (25) 48Lesser cyanobacteria provides source cavernosa.Mar. 346: 143-152Crossref (197) suggesting relevance holobiont. magnitude lower found sediments bare rock [43Cardini minor contributors overall budget For long were believed main drivers [49Lesser al.Discovery corals.Science. 305: 997-1000Crossref (351) 50Williams W.M. living variabilis.Mar. 1987; 94: 531-535Crossref 51Crossland Barnes D.J. Acetylene reduction skeletons.Limnol. 1976; 153-156Crossref (27) but recent revealed archaea) consisting mostly heterotrophic [16Lema 52Olson al.Diazotrophic Hawaiian Montipora correlation dinoflagellates.J. Mar. 371: 140-146Crossref (112) species-specific space time Moreover, Lema [18Lema parental colonies larvae, Alphaproteobacteria group Rhizobiales. suggests functioning. compartments Symbiodinium) quantified yet, contribute supply [48Lesser cyan

Language: Английский

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The sponge holobiont in a changing ocean: from microbes to ecosystems

Microbiome, Journal Year: 2018, Volume and Issue: 6(1)

Published: March 9, 2018

The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, microbiota, interactions among them. Accordingly, ecological concepts can be applied to understand host-derived processes govern dynamics interactive networks within holobiont. In marine systems, holobionts further integrated into larger more ecosystems, concept referred as "nested ecosystems." this review, we discuss dynamic interact at multiple scales respond environmental change. We focus on symbiosis sponges their communities—a resulted one most diverse environment. recent years, sponge microbiology remarkably advanced terms curated databases, standardized protocols, information functions microbiota. Like Russian doll, these translated holobiont impact surrounding ecosystem. For example, sponge-associated metabolisms, fueled by high filtering capacity substantially affect biogeochemical cycling key nutrients like carbon, nitrogen, phosphorous. Since increasingly threatened anthropogenic stressors jeopardize stability ecosystem, link between perturbations, dysbiosis, diseases. Experimental studies suggest community composition is tightly linked health, but whether dysbiosis cause or consequence collapse remains unresolved. Moreover, potential role microbiome mediating for acclimate adapt change unknown. Future should aim identify mechanisms underlying scales, from develop management strategies preserve provided our present future oceans.

Language: Английский

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Coral reef ecosystem services in the Anthropocene

Functional Ecology, Journal Year: 2019, Volume and Issue: 33(6), P. 1023 - 1034

Published: March 19, 2019

Abstract Coral reefs underpin a range of ecosystem goods and services that contribute to the well‐being millions people. However, tropical coral in Anthropocene are likely be functionally different from past. In this perspective piece, we ask, what does mean for provision reefs? First, provide examples provisioning, regulating, cultural supporting underpinned by reef ecosystems. We conclude service research has lagged behind multidisciplinary advances broader science, such as an explicit recognition interactions between social ecological systems services. Second, drawing on tools functional ecology, outline how these social–ecological relationships can incorporated into mechanistic understanding might used anticipate future changes Finally, explore emergence novel services, example tropicalized coastlines, or through changing technological connections reefs. Indeed, when conceived coming system dynamics, novelty emerge elements people ecosystem. This synthesis literature suggests field is poorly prepared understand anticipated Anthropocene. A new agenda needed better connects ecology provision. should embrace more holistic approaches research, recognizing them co‐produced ecosystems society. Importantly, likelihood configurations requires further conceptualization empirical assessment. As with current loss gain will not affect all equally must understood context which they occur. With uncertainty surrounding Anthropocene, exploring benefits change great importance. plain language summary available article.

Language: Английский

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An extensive reef system at the Amazon River mouth

Science Advances, Journal Year: 2016, Volume and Issue: 2(4)

Published: April 1, 2016

A novel Amazonian reef biome was discovered, encompassing large rhodolith and sponge beds under low light, oxygen, high POC.

Language: Английский

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The Sponge Hologenome

mBio, Journal Year: 2016, Volume and Issue: 7(2)

Published: April 22, 2016

A paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many aspects a host's phenotype and evolution. In process, an era "holobiont" research emerged investigate intricate network interactions between host its symbiotic microbial consortia. Marine sponges early-diverging metazoa known for hosting dense, specific, often highly diverse communities. Here we synthesize current thoughts about environmental evolutionary forces that influence diversity, specificity, distribution symbionts within sponge holobiont, explore physiological pathways contribute holobiont function, describe mechanisms underpin establishment maintenance these partnerships. The collective genomes form hologenome, highlight define sponge's in fact act on genomic interplay different components holobiont.

Language: Английский

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Global microbialization of coral reefs

Nature Microbiology, Journal Year: 2016, Volume and Issue: 1(6)

Published: April 25, 2016

Language: Английский

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Microbes in the coral holobiont: partners through evolution, development, and ecological interactions

Frontiers in Cellular and Infection Microbiology, Journal Year: 2015, Volume and Issue: 4

Published: Jan. 7, 2015

In the last two decades, genetic and genomic studies have revealed astonishing diversity ubiquity of microorganisms. Emergence expansion human microbiome project has reshaped our thinking about how microbes control host health – not only as pathogens, but also symbionts. coral reef environments, scientists begun to examine role that microorganisms play in life history. Herein we review current literature on coral-microbe interactions within context their evolution, development, ecology. We ask following questions, first posed by McFall-Ngai et al., 2013 animal with specific attention coral-microbial may be affected under future environmental conditions: 1) How do corals affect each other's genomes? 2) does development depend microbial partners? 3) is homeostasis maintained between symbionts? 4) can ecological approaches deepen understanding multiple levels interactions? Elucidating structure function holobiont essential for maintain acclimate changing conditions.

Language: Английский

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The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs

Biological reviews/Biological reviews of the Cambridge Philosophical Society, Journal Year: 2018, Volume and Issue: 93(4), P. 1846 - 1873

Published: May 7, 2018

Teleost fishes are the most diverse group of vertebrates on Earth. On tropical coral reefs, their species richness exceeds 6000 species; one tenth total vertebrate biodiversity. A large proportion this diversity is composed cryptobenthic reef (CRFs): bottom-dwelling, morphologically or behaviourally cryptic typically less than 50 mm in length. Yet, despite and abundance, these both poorly defined understood. Herein we provide a new quantitative definition synthesise current knowledge diversity, distribution life history CRFs. First, use size distributions within families to define 17 core CRF as characterised by high prevalence (>10%) small-bodied (<50 mm). This stands strong contrast 42 fishes, which virtually no have evolved. We posit that small body has allowed CRFs diversify at extremely rates, primarily allowing for fine partitioning microhabitats facilitation allopatric reproductive isolation; yet, far from understanding documenting biodiversity Using rates description since 1758, predict approximately 30 will be described per year until 2050 (approximately twice annual rate compared fishes). Furthermore, 2031, more half fish consist These 'hidden half' reefs. Notably, global geographic coverage spatial resolution data communities uniformly poor, further emphasises remarkable reservoir yet discovered. Although may enabled extensive diversification families, also comes with suite ecological challenges affect fishes' capacities feed, survive reproduce; identify range life-history adaptations overcome limitations. In turn, bestow unique socio-ecological role CRFs, includes key trophodynamics cycling trophic energy provided microscopic prey larger consumers. size, ecology evolutionary make them critical component coral-reef food webs; our review shows highly susceptible variety anthropogenic disturbances. Understanding consequences changes ecosystems require us shed light frequently overlooked but abundant guild fishes.

Language: Английский

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