Metagenomic analysis of the microbial community associated with the coral Porites astreoides

Environmental Microbiology, Journal Year: 2007, Volume and Issue: 9(11), P. 2707 - 2719

Published: July 21, 2007

Summary The coral holobiont is a dynamic assemblage of the animal, zooxanthellae, endolithic algae and fungi, Bacteria , Archaea viruses. Zooxanthellae some form relatively stable species‐specific associations with corals. Other are less specific; coral‐associated differ from those in water column, but same archaeal species may be found on different species. It has been hypothesized that animal can adapt to differing ecological niches by ‘switching’ its microbial associates. In case corals this termed adaptive bleaching it important implications for carbon cycling within ultimately survival reefs. However, roles other components essentially unknown. To better understand these associates, fractionation procedure was used separate microbes, mitochondria viruses cells zooxanthellae. resulting metagenomic DNA sequenced using pyrosequencing. Fungi, phage were most commonly identified organisms metagenome. Three four fungal phyla represented, including wide diversity genes involved nitrogen metabolism, suggesting community more than previously appreciated. particular, data suggested fungi could converting nitrate nitrite ammonia, which would enable fixed cycle holobiont. prominent bacterial groups Proteobacteria (68%), Firmicutes (10%), Cyanobacteria (7%) Actinobacteria (6%). Functionally, primarily heterotrophic included number pathways degradation aromatic compounds, abundant being homogentisate pathway. family ssDNA Microphage eukaryotic closely related known infect aquatic organisms. This study provides metabolic taxonomic snapshot microbes associated reef‐building Porites astreoides presents basis understanding how coral–microbial interactions structure

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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Changes in coral-associated microbial communities during a bleaching event

The ISME Journal, Journal Year: 2007, Volume and Issue: 2(4), P. 350 - 363

Published: Dec. 6, 2007

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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Beneficial Microorganisms for Corals (BMC): Proposed Mechanisms for Coral Health and Resilience

Frontiers in Microbiology, Journal Year: 2017, Volume and Issue: 8

Published: March 7, 2017

The symbiotic association between the coral animal and its endosymbiotic dinoflagellate partner Symbiodinium is central to success of corals. However, an array other microorganisms associated with (i.e., Bacteria, Archaea, Fungi viruses) have a complex intricate role in maintaining homeostasis corals Symbiodinium. Corals are sensitive shifts surrounding environmental conditions. One most widely reported responses stressful conditions bleaching. During this event, expel cells from their gastrodermal tissues upon experiencing extended seawater temperatures above thermal threshold. An stressors can also destabilize microbiome, resulting compromised health host, which may include disease mortality worst scenario. exact mechanisms by microbiome supports increases resilience poorly understood. Earlier studies microbiology proposed probiotic hypothesis, wherein dynamic relationship exists microorganisms, selecting for holobiont that best suited prevailing Here, we discuss microbial-host relationships within holobiont, along potential roles health. We propose term BMC (Beneficial Microorganisms Corals) define (specific) symbionts promote This concept analogous Plant Growth Promoting Rhizosphere (PGPR), has been explored manipulated agricultural industry inhabit rhizosphere directly or indirectly plant growth development through production regulatory signals, antibiotics nutrients. Additionally, effects on corals, suggesting strategies use knowledge manipulate reversing dysbiosis restore protect reefs. developing using consortia as "probiotics" improve resistance after bleaching events and/or such human-assisted acclimation/adaption shifting

Language: Английский

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The Hologenome Concept: Helpful or Hollow?

PLoS Biology, Journal Year: 2015, Volume and Issue: 13(12), P. e1002311 - e1002311

Published: Dec. 4, 2015

With the increasing appreciation for crucial roles that microbial symbionts play in development and fitness of plant animal hosts, there has been a recent push to interpret evolution through lens "hologenome"—the collective genomic content host its microbiome. But how evolve and, particularly, whether they undergo natural selection benefit hosts are complex issues associated with several misconceptions about evolutionary processes host-associated communities. Microorganisms can have intimate, ancient, and/or mutualistic associations without having undergone hosts. Likewise, observing host-specific community composition or greater similarity among more closely related does not imply coevolved let alone evolved host. Although at level symbiotic community, hologenome, occurs some cases, it should be accepted as null hypothesis explaining features host–symbiont associations.

Language: Английский

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The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis

Nature Chemistry, Journal Year: 2011, Volume and Issue: 3(4), P. 331 - 335

Published: Feb. 27, 2011

Language: Английский

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Microbes Drive Evolution of Animals and Plants: the Hologenome Concept

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

Published: April 1, 2016

The hologenome concept of evolution postulates that the holobiont (host plus symbionts) with its genome microbiome) is a level selection in evolution. Multicellular organisms can no longer be considered individuals by classical definitions term. Every natural animal and plant consisting host diverse symbiotic microbes viruses. Microbial symbionts transmitted from parent to offspring variety methods, including via cytoplasmic inheritance, coprophagy, direct contact during after birth, environment. A large number studies have demonstrated these contribute anatomy, physiology, development, innate adaptive immunity, behavior finally also genetic variation origin species. Acquisition microbial genes powerful mechanism for driving complexity. Evolution proceeds both cooperation competition, working parallel.

Language: Английский

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Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur

Applied and Environmental Microbiology, Journal Year: 2009, Volume and Issue: 75(11), P. 3492 - 3501

Published: April 4, 2009

Marine bacteria play a central role in the degradation of dimethylsulfoniopropionate (DMSP) to dimethyl sulfide (DMS) and acrylic acid, DMS being critical cloud formation thereby cooling effects on climate. High concentrations DMSP have been reported scleractinian coral tissues although, date, there no investigations into influence these organic sulfur compounds coral-associated bacteria. Two species, Montipora aequituberculata Acropora millepora, were sampled their bacterial communities characterized by both culture-dependent molecular techniques. Four genera, Roseobacter, Spongiobacter, Vibrio, Alteromonas, which isolated media with either or as sole carbon source, comprised majority clones retrieved from mucus tissue 16S rRNA gene clone libraries. Clones affiliated Roseobacter sp. constituted 28% M. libraries, while 59% A. millepora libraries sequences related Spongiobacter genus. Vibrio spp. commonly acid enrichments also present mucus, suggesting that under "normal" environmental conditions, they are natural component communities. Genes homologous dddD, dddL, previously implicated degradation, strains, confirming associated corals potential metabolize this compound when tissues. Our results demonstrate DMSP, DMS, potentially act nutrient sources for likely structuring corals, important consequences health reef ecosystems.

Language: Английский

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The hologenome concept of evolution after 10 years

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

Published: April 25, 2018

The holobiont (host with its endocellular and extracellular microbiome) can function as a distinct biological entity, an additional organismal level to the ones previously considered, on which natural selection operates. whole: anatomically, metabolically, immunologically, developmentally, during evolution. Consideration of hologenome independent in evolution has led better understanding underappreciated modes genetic variation is comprised two complimentary parts: host microbiome genomes. Changes either genome result variations that be selected for or against. highly conserved, changes within it occur slowly, whereas dynamic change rapidly response environment by increasing reducing particular microbes, acquisition novel horizontal gene transfer, mutation. Recent experiments showing microbiota play initial role speciation have been suggested mode enhancing Some transferred offspring variety mechanisms. Strain-specific DNA analysis shown at least some maintained across hundreds thousands generations, implying existence microbial core. We argue rapid could allow holobionts adapt survive under changing environmental conditions thus providing time necessary evolve. As Darwin wrote, "It not strongest species survives but most adaptable".

Language: Английский

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