Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities DOI Creative Commons
Eslam O. Osman, David J. Suggett, Christian R. Voolstra

et al.

Microbiome, Journal Year: 2020, Volume and Issue: 8(1)

Published: Feb. 3, 2020

The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) potential mechanism that may assist thrive warm waters. northern Red Sea experiences extreme temperatures anomalies, yet this area rarely bleach suggesting possible refugia However, the composition, how it relates waters region, entirely unknown.We investigated microbiomes six species (Porites nodifera, Favia favus, Pocillopora damicornis, Seriatopora hystrix, Xenia umbellata, Sarcophyton trocheliophorum) from five sites spanning 4° latitude summer mean temperature ranges 26.6 °C 29.3 °C. A total 19 distinct dinoflagellate were identified as belonging three genera family Symbiodiniaceae (Symbiodinium, Cladocopium, Durusdinium). Of these, 86% belonged genus with notably novel types (19%). endosymbiont community showed high degree host-specificity despite latitudinal gradient. In contrast, diversity bacterial communities surface mucus layer (SML)-a compartment particularly sensitive environmental change-varied significantly between sites, however any given was species-specific.The conserved endosymbiotic suggests physiological plasticity support holobiont productivity across different regimes. Further, presence algal selection certain genotypes genetic adaptation) within semi-isolated Sea. dynamic bacteria associated SML contribute function broaden ecological niche. doing so, aid local acclimatization by readily responding changes host environment. Our study provides insight about selective endemic nature along refugia.

Language: Английский

Coral reefs in the Anthropocene DOI
Terry P. Hughes, Michele L. Barnes, David R. Bellwood

et al.

Nature, Journal Year: 2017, Volume and Issue: 546(7656), P. 82 - 90

Published: May 30, 2017

Language: Английский

Citations

1775

Contrasting futures for ocean and society from different anthropogenic CO 2 emissions scenarios DOI
Jean‐Pierre Gattuso, Alexandre Magnan,

Raphaël Billé

et al.

Science, Journal Year: 2015, Volume and Issue: 349(6243)

Published: July 3, 2015

Carbon emissions and their ocean impacts Anthropogenic CO 2 directly affect atmospheric chemistry but also have a strong influence on the oceans. Gattuso et al. review how physics, chemistry, ecology of oceans might be affected based two emission trajectories: one business as usual with aggressive reductions. Ocean warming, acidification, sea-level rise, expansion oxygen minimum zones will continue to distinct marine communities ecosystems. The path that humanity takes regarding largely determine severity these phenomena. Science , this issue 10.1126/science.aac4722

Language: Английский

Citations

1276

Nitrogen cycling in corals: the key to understanding holobiont functioning? DOI Creative Commons
Nils Rädecker, Claudia Pogoreutz,

Christian R. Voolstra

et al.

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

Citations

519

Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf DOI Creative Commons
Benjamin C. C. Hume, Cecilia D’Angelo, Edward G. Smith

et al.

Scientific Reports, Journal Year: 2015, Volume and Issue: 5(1)

Published: Feb. 27, 2015

Coral reefs are in rapid decline on a global scale due to human activities and changing climate. Shallow water depend the obligatory symbiosis between habitat forming coral host its algal symbiont from genus Symbiodinium (zooxanthellae). This association is highly sensitive thermal perturbations temperatures as little 1°C above average summer maxima can cause breakdown of this symbiosis, termed bleaching. Predicting capacity corals survive expected increase seawater depends strongly our understanding tolerance symbiotic algae. Here we use molecular phylogenetic analysis four genetic markers describe thermophilum, sp. nov. Persian/Arabian Gulf, thermally tolerant symbiont. Phylogenetic inference using non-coding region chloroplast psbA gene resolves S. thermophilum monophyletic lineage with large distances any other ITS2 C3 type found outside Gulf. Through characterisation associations 6 species (5 genera) Gulf corals, demonstrate that prevalent all year round world's hottest sea, southern

Language: Английский

Citations

282

SymPortal: A novel analytical framework and platform for coral algal symbiont next‐generation sequencing ITS2 profiling DOI Creative Commons
Benjamin C. C. Hume, Edward G. Smith, Maren Ziegler

et al.

Molecular Ecology Resources, Journal Year: 2019, Volume and Issue: 19(4), P. 1063 - 1080

Published: Feb. 11, 2019

Abstract We present SymPortal (SymPortal.org), a novel analytical framework and platform for genetically resolving the algal symbionts of reef corals using next‐generation sequencing (NGS) data ITS2 rDNA. Although marker is widely used to characterize taxa within family Symbiodiniaceae (formerly genus Symbiodinium) , multicopy nature complicates its use. Commonly, intragenomic diversity resultant from this collapsed by approaches, thereby focusing on only most abundant sequences. In contrast, employs logic identify within‐sample informative sequences, which we have termed ‘defining variants' (DIVs), ‐type profiles representative putative taxa. By making use diversity, able resolve genetic delineations at level that was previously possible additional markers. demonstrate comparing approach commonly alternative NGS data, 97% similarity clustering operational taxonomic units (OTUs). The accepts raw as input provide an easy‐to‐use, standardization‐enforced, community‐driven integrates with database gain power increased consider SymPortal, in conjunction ongoing large‐scale sampling efforts, should play instrumental role future efforts more comparable maximizing their efficacy working towards classification global diversity.

Language: Английский

Citations

260

Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales DOI Creative Commons
Matthew J. Neave, Rita Rachmawati,

Liping Xun

et al.

The ISME Journal, Journal Year: 2016, Volume and Issue: 11(1), P. 186 - 200

Published: July 8, 2016

Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also prokaryotic symbionts, the specificity of which remains elusive. To identify central microbial symbionts corals, across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes Bacteria Archaea from common Stylophora pistillata Pocillopora verrucosa 28 reefs within seven major geographical regions. We demonstrate that both harbor Endozoicomonas bacteria as prevalent symbiont. Importantly, catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) Endozoicomonas-specific probes confirmed residence large aggregations deep coral tissues. Using fine-scale genotyping techniques single-cell genomics, P. harbors same Endozoicomonas, whereas S. associates geographically distinct genotypes. This may be shaped by different reproductive strategies hosts, potentially uncovering a pattern symbiont selection is linked to life history. Spawning such acquire prokaryotes environment. In contrast, brooding release symbiont-packed planula larvae, explain strong regional signature microbiome. Our work contributes factors underlying microbiome adds detail holobiont functioning.

Language: Английский

Citations

241

Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? DOI Creative Commons
Corinna Bang, Tal Dagan, Peter Deines

et al.

Zoology, Journal Year: 2018, Volume and Issue: 127, P. 1 - 19

Published: Feb. 15, 2018

From protists to humans, all animals and plants are inhabited by microbial organisms. There is an increasing appreciation that these resident microbes influence the fitness of their plant animal hosts, ultimately forming a metaorganism consisting uni- or multicellular host community associated microorganisms. Research on host–microbe interactions has become emerging cross-disciplinary field. In both vertebrates invertebrates complex microbiome confers immunological, metabolic behavioural benefits; conversely, its disturbance can contribute development disease states. However, molecular cellular mechanisms controlling within poorly understood many key between organisms remain unknown. this perspective article, we outline some issues in interspecies particular address question how metaorganisms react adapt inputs from extreme environments such as deserts, intertidal zone, oligothrophic seas, hydrothermal vents.

Language: Английский

Citations

234

Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals DOI Creative Commons
Nadine Boulotte, Steven J. Dalton, Andrew Carroll

et al.

The ISME Journal, Journal Year: 2016, Volume and Issue: 10(11), P. 2693 - 2701

Published: April 19, 2016

Abstract Reef-building corals possess a range of acclimatisation and adaptation mechanisms to respond seawater temperature increases. In some corals, thermal tolerance increases through community composition changes their dinoflagellate endosymbionts (Symbiodinium spp.), but this mechanism is believed be limited the Symbiodinium types already present in coral tissue acquired during early life stages. Compelling evidence for symbiont switching, that is, acquisition novel from environment, by adult colonies, currently lacking. Using deep sequencing analysis rDNA internal transcribed spacer 2 (ITS2) PCR amplicons two pocilloporid species, we show consistent with de novo environment following consecutive bleaching events. Most these newly detected symbionts remained rare biosphere (background occurring below 1% relative abundance), one type reached abundance ~33%. Two belong thermally resistant clade D, suggesting switching may have been driven Our results are particularly important given maternal mode transmission study which generally high specificity. These findings will cause paradigm shift our understanding coral-Symbiodinium symbiosis flexibility environmental corals.

Language: Английский

Citations

222

Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella DOI Open Access
D. Tye Pettay, Drew C. Wham,

Robin T. Smith

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2015, Volume and Issue: 112(24), P. 7513 - 7518

Published: June 1, 2015

Human-induced environmental changes have ushered in the rapid decline of coral reef ecosystems, particularly by disrupting symbioses between reef-building corals and their photosymbionts. However, escalating stressful conditions enable some symbionts to thrive as opportunists. We present evidence that a stress-tolerant "zooxanthella" from Indo-Pacific Ocean, Symbiodinium trenchii, has rapidly spread communities across Greater Caribbean. In marked contrast populations Indo-Pacific, Atlantic S. trenchii contained exceptionally low genetic diversity, including several widespread genetically similar clones. Colonies with this symbiont tolerate temperatures 1-2 °C higher than other host-symbiont combinations; however, calcification hosts harboring is reduced nearly half, compared those natives, suggests these new are maladapted. Unforeseen opportunism geographical expansion invasive mutualistic microbes could profoundly influence response major perturbations but may ultimately compromise ecosystem stability function.

Language: Английский

Citations

216

Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change DOI Open Access
Ross Cunning,

Rachel N. Silverstein,

Andrew C. Baker

et al.

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2015, Volume and Issue: 282(1809), P. 20141725 - 20141725

Published: June 3, 2015

Dynamic symbioses may critically mediate impacts of climate change on diverse organisms, with repercussions for ecosystem persistence in some cases. On coral reefs, increases heat-tolerant symbionts after thermal bleaching can reduce susceptibility to future stress. However, the relevance this adaptive response is equivocal owing conflicting reports symbiont stability and change. We help reconcile conflict by showing that community composition (symbiont shuffling) Orbicella faveolata depends disturbance severity recovery environment. The proportion dramatically increased following severe experimental bleaching, especially a warmer environment, but tended decrease if was less severe. These patterns be explained variation performance changing microenvironments created differentially bleached host tissues. Furthermore, higher proportions linearly resistance reduced photochemical efficiency, suggesting any structure oppositely stress tolerance. Therefore, even minor shuffling adaptively benefit corals, although fitness effects resulting trade-offs are difficult predict. This work helps elucidate causes consequences dynamism symbiosis, which critical predicting responses multi-partner such as O. environmental

Language: Английский

Citations

205