Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts

Current Biology, Год журнала: 2018, Номер 28(16), С. 2570 - 2580.e6

Опубликована: Авг. 1, 2018

The advent of molecular data has transformed the science organizing and studying life on Earth. Genetics-based evidence provides fundamental insights into diversity, ecology, origins many biological systems, including mutualisms between metazoan hosts their micro-algal partners. A well-known example is dinoflagellate endosymbionts ("zooxanthellae") that power growth stony corals coral reef ecosystems. Once assumed to encompass a single panmictic species, genetic revealed divergent rich diversity within zooxanthella genus Symbiodinium. Despite decades reporting significance this formal systematics these eukaryotic microbes have not kept pace, major revision long overdue. With consideration molecular, morphological, physiological, ecological data, we propose evolutionarily Symbiodinium "clades" are equivalent genera in family Symbiodiniaceae, provide descriptions for seven them. Additionally, recalibrate clock group amend date earliest diversification middle Mesozoic Era (∼160 mya). This timing corresponds with adaptive radiation analogs modern shallow-water during Jurassic Period connects rise symbiotic dinoflagellates emergence evolutionary success reef-building corals. improved framework acknowledges Symbiodiniaceae's history while filling pronounced taxonomic gap. Its adoption will facilitate scientific dialog future research physiology, evolution important micro-algae.

Язык: Английский

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Contrasting futures for ocean and society from different anthropogenic CO ₂ emissions scenarios

Science, Год журнала: 2015, Номер 349(6243)

Опубликована: Июль 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

Язык: Английский

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

Trends in Microbiology, Год журнала: 2015, Номер 23(8), С. 490 - 497

Опубликована: Апрель 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

Язык: Английский

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

Frontiers in Microbiology, Год журнала: 2017, Номер 8

Опубликована: Март 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

Язык: Английский

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SymPortal: A novel analytical framework and platform for coral algal symbiont next‐generation sequencing ITS2 profiling

Molecular Ecology Resources, Год журнала: 2019, Номер 19(4), С. 1063 - 1080

Опубликована: Фев. 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.

Язык: Английский

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Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment

Scientific Reports, Год журнала: 2015, Номер 5(1)

Опубликована: Дек. 2, 2015

Abstract Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal subtidal naturally Kimberley region in northwest Australia. Here tides up to 10 m cause aerial exposure corals temperatures as high 37 °C that fluctuate daily by 7 °C. Control were maintained at ambient nearshore which varied diurnally 4-5 °C, while treatment exposed similar diurnal variations heat stress corresponding ~20 degree heating days. All hosted Symbiodinium clade C independent or origin. Detailed physiological measurements showed these nevertheless highly sensitive average exceeding their maximum monthly mean ~31 1 for only a few Generally, was much more susceptible than experienced 75% mortality, whereas all survived. Furthermore, corals, originated thermally stable environment compared bleaching. This demonstrates fluctuating enhance resilience stress, they do not immunity events.

Язык: Английский

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The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

Frontiers in Marine Science, Год журнала: 2018, Номер 5

Опубликована: Фев. 2, 2018

Global climate change and localised anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental providing insight into how organisms will potentially respond to future climates. However, such inevitably limited their ability reproduce the complex interactions that govern systems. Studies examining communities already persist under naturally-occurring extreme marginal physicochemical conditions therefore become increasingly popular advance ecosystem scale predictions of form function, although no single site provides a perfect analogue reefs. Here we review current state knowledge exists on distribution corals environments, geographic sites at latitudinal extremes growth, as well variety shallow systems reef-neighbouring environments (including upwelling CO2 vent sites). We also conduct synthesis abiotic data collected these systems, provide first collective assessment range which currently persist. use increase our understanding biological ecological mechanisms facilitate survival success sub-optimal conditions. This comprehensive can begin to: (i) highlight extent scenarios persist, (ii) explore whether there commonalities taxa able extremes, (iii) evidence for key required support and/or persistence environmental conditions, iv) evaluate potential act refugia changing Such approach is critical better understand environment. finally outline priority areas research discuss additional management options they may through refuge or by genetic stocks stress tolerant proactive strategies.

Язык: Английский

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Thermal refugia against coral bleaching throughout the northern Red Sea

Global Change Biology, Год журнала: 2017, Номер 24(2)

Опубликована: Окт. 17, 2017

Abstract Tropical reefs have been impacted by thermal anomalies caused global warming that induced coral bleaching and mortality events globally. However, there only very few recordings of within the Red Sea despite covering a latitudinal range 15° consequently it has considered region is less sensitive to anomalies. We therefore examined historical patterns sea surface temperature ( SST ) associated (1982–2012) compared trends with unique compilation corresponding records from throughout region. These data indicated northern not experienced mass intensive Degree Heating Weeks DHW >15°C‐weeks. Severe was restricted central southern where s more frequent, but far intense (DHWs <4°C‐weeks). A similar pattern observed during 2015–2016 El Niño event which time corals in did bleach high stress (i.e. DHWs >8°C‐weeks), lower < 8°C‐weeks). Heat assays carried out (Hurghada) (Thuwal) on four key reef‐building species confirmed different regional susceptibility, are as those north. Together, our demonstrate much higher heat tolerance than their prevailing regime would suggest. In contrast, close limits, closely match maximum annual water temperatures. The harbours live well below thresholds thus we propose represents refuge importance.

Язык: Английский

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Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Proceedings of the National Academy of Sciences, Год журнала: 2016, Номер 113(16), С. 4416 - 4421

Опубликована: Апрель 4, 2016

Significance Reef corals in the Persian/Arabian Gulf (PAG) withstand exceptionally high salinity and regular summer temperatures of ∼35 °C that kill conspecifics elsewhere. These thermotolerant communities established themselves within only ∼6,000 y under pressure rapid climate change can therefore inform how other coral reefs may respond to global warming. One key thermotolerance PAG is their symbiosis with Symbiodinium thermophilum . Phylogeographic evidence indicates this symbiont represents a stress-tolerant subpopulation an ancestral taxonomic group surprising genetic diversity exists at barely detectable levels outside PAG. Our results highlight critical importance present-day biodiversity for future adaptation ecosystems general.

Язык: Английский

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The Anthropocene as a Geological Time Unit

Cambridge University Press eBooks, Год журнала: 2019, Номер unknown

Опубликована: Фев. 26, 2019

The Anthropocene, a term launched into public debate by Nobel Prize winner Paul Crutzen, has been used informally to describe the time period during which human actions have had drastic effect on Earth and its ecosystems. This book presents evidence for defining Anthropocene as geological epoch, written high-profile international team analysing potential addition scale. ranges from chemical signals arising pollution, landscape changes associated with urbanisation, biological species invasion extinctions. Global environmental change is placed within context of planetary processes deep time, allowing reader appreciate scale human-driven compare global transition taking place today major transitions in history. an authoritative review graduate students academic researchers across scientific, social science humanities disciplines.

Язык: Английский

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