Stress and stability: applying the Anna Karenina principle to animal microbiomes

Nature Microbiology, Journal Year: 2017, Volume and Issue: 2(9)

Published: Aug. 23, 2017

Language: Английский

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Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems

Annual Review of Microbiology, Journal Year: 2016, Volume and Issue: 70(1), P. 317 - 340

Published: Aug. 2, 2016

Corals are fundamental ecosystem engineers, creating large, intricate reefs that support diverse and abundant marine life. At the core of a healthy coral animal is dynamic relationship with microorganisms, including mutually beneficial symbiosis photosynthetic dinoflagellates (Symbiodinium spp.) enduring partnerships an array bacterial, archaeal, fungal, protistan, viral associates, collectively termed holobiont. The combined genomes this holobiont form hologenome, genomic interactions within hologenome ultimately define phenotype. Here we integrate contemporary scientific knowledge regarding ecological, host-specific, environmental forces shaping diversity, specificity, distribution microbial symbionts holobiont, explore physiological pathways contribute to fitness, describe potential mechanisms for homeostasis. Understanding role microbiome in resilience, acclimation, adaptation new frontier reef science will require large-scale collaborative research efforts.

Language: Английский

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Marine reserves can mitigate and promote adaptation to climate change

Proceedings of the National Academy of Sciences, Journal Year: 2017, Volume and Issue: 114(24), P. 6167 - 6175

Published: June 5, 2017

Strong decreases in greenhouse gas emissions are required to meet the reduction trajectory resolved within 2015 Paris Agreement. However, even these will not avert serious stress and damage life on Earth, additional steps needed boost resilience of ecosystems, safeguard their wildlife, protect capacity supply vital goods services. We discuss how well-managed marine reserves may help ecosystems people adapt five prominent impacts climate change: acidification, sea-level rise, intensification storms, shifts species distribution, decreased productivity oxygen availability, as well cumulative effects. explore role managed mitigating change by promoting carbon sequestration storage buffering against uncertainty management, environmental fluctuations, directional change, extreme events. highlight both strengths limitations conclude that a viable low-tech, cost-effective adaptation strategy would yield multiple cobenefits from local global scales, improving outlook for environment into future.

Language: Английский

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Climate Change, Human Impacts, and Coastal Ecosystems in the Anthropocene

Current Biology, Journal Year: 2019, Volume and Issue: 29(19), P. R1021 - R1035

Published: Oct. 1, 2019

Language: Английский

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The Globalization of Cultural Eutrophication in the Coastal Ocean: Causes and Consequences

Frontiers in Marine Science, Journal Year: 2020, Volume and Issue: 7

Published: Aug. 17, 2020

Coastal eutrophication caused by anthropogenic nutrient inputs is one of the greatest threats to health coastal estuarine and marine ecosystems worldwide. To better understand manage this threat, we compared six contrasting that are subjected a range riverine freshwater (buoyancy) nutrients address (i) impacts on ecosystem services; (ii) how traits minimize or amplify these impacts; (iii) synergies among pressures (nutrient enrichment, over fishing, development, climate-driven in particular); (iv) management ecosystems. Globally, ~ 24% N released watersheds estimated reach Our comparative assessment revealed terms spatial extent habitat degradation, Chesapeake Bay ranks number followed rank order northern Gulf Mexico, Baltic Sea, Great Barrier Reef, East China Sea Adriatic Sea; increases loading are, will continue be, exacerbated with other including development sea surface temperature, acidification rainfall; when defined quantitative ranges primary production, trophic status not useful for relating impacts. While managed reductions point source from sewage treatment plants increasingly successful, controlling diffuse sources remains challenging problem. Thus, it likely severity increase absence effectively enforced, ecosystem-based both nitrogen phosphorus. This requires sustained, integrated research monitoring, as well repeated assessments These must be informed guided ongoing collaborations scientists, politicians, managers public.

Language: Английский

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Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

Nature Communications, Journal Year: 2018, Volume and Issue: 9(1)

Published: Nov. 16, 2018

Scleractinian corals' microbial symbionts influence host health, yet how coral microbiomes assembled over evolution is not well understood. We survey bacterial and archaeal communities in phylogenetically diverse Australian corals representing more than 425 million years of diversification. show that are anatomically compartmentalized both modern ecology evolutionary assembly. Coral mucus, tissue, skeleton differ community composition, richness, response to vs. environmental drivers. also find evidence coral-microbe phylosymbiosis, which microbiome composition richness reflect phylogeny. Surprisingly, the represents most biodiverse microbiome, shows strongest phylosymbiosis. Interactions between phylogeny significantly abundance four groups bacteria-including Endozoicomonas-like bacteria, divide into host-generalist host-specific subclades. Together these results trace symbiosis across anatomy during a basal animal lineage.

Language: Английский

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Nutrient Availability and Metabolism Affect the Stability of Coral–Symbiodiniaceae Symbioses

Trends in Microbiology, Journal Year: 2019, Volume and Issue: 27(8), P. 678 - 689

Published: April 12, 2019

Mass coral bleaching is occurring at an unprecedented rate due to anthropogenic ocean warming, and it represents the greatest threat reef ecosystems globally.Coral predominantly attributed photo-oxidative stress under elevated temperature light, but recent experiments have unveiled nutritional mechanisms that can regulate bleaching.Bleaching may result when coral–Symbiodiniaceae symbiosis shifts from a mutualistic parasitic relationship thermal stress.Nutrient availability, specifically forms ratios of nutrients such as nitrogen phosphorus, mediates algal symbiont parasitism.Stable metabolic compatibility between host ameliorate increase resilience environmental stress. Coral reefs rely upon highly optimized symbiosis, making them sensitive change susceptible stress, yet nutrient availability metabolism underpin stability symbioses. Recent studies link proliferation enrichment bleaching; however, interactions symbiotic are nuanced. Here, we demonstrate how regulated by available their impacts on autotrophic carbon metabolism, rather than growth. By extension, historical conditions mediate host–symbiont tolerance over proximate evolutionary timescales. Renewed investigations into will be required truly elucidate cellular leading bleaching. hotspots biodiversity productivity which provide vital extensive ecosystem services [1.Fisher R. et al.Species richness pursuit convergent global estimates.Curr. Biol. 2015; 25: 500-505Abstract Full Text PDF PubMed Scopus (59) Google Scholar, 2.Crossland C.J. al.Role in production.Coral Reefs. 1991; 10: 55-64Crossref (0) 3.Moberg F. Folke C. Ecological goods ecosystems.Ecol. Econ. 1999; 29: 215-233Crossref (717) Scholar]. However, these values mass events triggered warming [4.Hughes T.P. al.Spatial temporal patterns corals Anthropocene.Science. 2018; 359: 80-83Crossref (25) (see Glossary) response heat light levels, where lose symbionts (Symbiodiniaceae) [5.Hoegh-Guldberg O. Climate change, future world's reefs.Mar. Freshw. Res. 50: 839-866Crossref 6.LaJeunesse T.C. al.Systematic revision Symbiodiniaceae highlights antiquity diversity endosymbionts.Curr. 28: 2570-2580.e6Abstract Corals acquire most energy through photosynthates translocated [7.Muscatine L. Porter J.W. Reef corals: Mutualistic symbioses adapted nutrient-poor environments.BioScience. 1977; 27: 454-460Crossref Scholar], loss this source for long periods starvation mortality Bleaching lead reductions cover, species genetic diversity, away coral-dominated state impedes [8.Graham N.A. al.Predicting climate-driven regime versus rebound potential reefs.Nature. 518: 94-97Crossref (232) 9.Hughes al.Global transforms assemblages.Nature. 556: 492-496Crossref (19) Although some remain resilient, there exists adapt oceans natural means [10.Matz M.V. al.Potential limits rapid adaptation Great Barrier coral.PLoS Genet. 14e1007220Crossref (1) Scholar] human interventions [11.Anthony K. al.New needed save reefs.Nat. Ecol. Evol. 2017; 1: 1420-1422Crossref (6) strong emissions ultimately ensure persistence reefs. also impacted local stressors, reduce water quality interact with susceptibility [12.D'Angelo Wiedenmann J. Impacts reefs: new perspectives implications coastal management survival.Curr. Opin. Environ. Sustain. 2014; 7: 82-93Crossref Changes land use adjacent primary further altered biological physical processes Scholar]; organisms across range trophic levels secondarily modify environment 13.Rädecker N. al.Nitrogen cycling The key understanding holobiont functioning?.Trends Microbiol. 23: 490-497Abstract localized fishing results removal significant subsidies [14.Allgeier J.E. al.Animal pee sea: consumer-mediated dynamics changing oceans.Glob. Chang. 2166-2178Crossref influences marine biogeochemistry scale, increased storm activity intensifies riverine flux column mixing 15.Knutson T.R. al.Tropical cyclones climate change.Nat. Geosci. 2010; 3: 157-163Crossref 16.Sinha E. al.Eutrophication during 21st century precipitation changes.Science. 357: 405-408Crossref (68) In contrast, increases stratification reduces 17.Behrenfeld M.J. al.Climate-driven trends contemporary productivity.Nature. 2006; 444: 752-755Crossref (1116) Synergistically, drivers subsequent not only impact nutrients, limitation possible suggest limitation, per se, lowers occurs [18.Wiedenmann al.Nutrient bleaching.Nat. Clim. 2013; 160-164Crossref (124) 19.Courtial al.Effects ultraviolet radiation level physiological organic matter release scleractinian Pocillopora damicornis following stress.PLoS One. 13e0205261Crossref 20.Ezzat impairs plasticity reef-building warming.Funct. 2019; (Published online January 12, 2019. https://doi.org/10.1111/1365-2435.13285)Crossref This review therefore discusses synthesizes direct external health tropical demonstrates this, together internal underpins holobiont. permits existence oligotrophic waters Tight recycling within provides respiratory CO2 nitrogenous waste products, exchange receives photosynthetically fixed [21.Davy S.K. al.Cell biology cnidarian-dinoflagellate symbiosis.Microbiol. Mol. Rev. 2012; 76: 229-261Crossref (256) Additionally, efficiently assimilate dissolved inorganic phosphorus [13.Rädecker 22.Ferrier-Pagès al.Phosphorus symbionts.Ecol. Monogr. 2016; 86: 262-277Crossref (13) heterotrophic feeding [23.Houlbrèque Ferrier-Pagès Heterotrophy corals.Biol. 2009; 84: 1-17Crossref microbiome translocation digestion [24.Bourne D.G. al.Insights microbiome: Underpinning ecosystems.Annu. 70: 317-340Crossref (8) relative modes acquisition depend individual capabilities each member, example fixation diazotrophs compensate limited or uptake [25.Pogoreutz aligns nifH abundance expression two functional groups.Front. 8: 1187Crossref 26.Bednarz V.N. al.The assimilation diazotroph-derived depends status.mBio. 8e02058-16Crossref (17) heterotrophy reduced Metabolic hosts communities likely performance [27.Rädecker al.Using Aiptasia model study cnidarian-Symbiodinium symbioses.Front. Physiol. 9: 214Crossref (4) 28.Suggett D.J. al.Symbiotic dinoflagellate survival ecological crisis.Trends 32: 735-745Abstract But bleach, they depleted major chances recovery partly determined ability restore autotrophy [29.Grottoli A.G. al.Heterotrophic bleached corals.Nature. 440: 1186-1189Crossref (357) 30.Tremblay P. al.Heterotrophy promotes re-establishment photosynthate after stress.Sci. Rep. 6: 38112Crossref 31.Levas S. al.Long-term Caribbean bleaching.J. Exp. Mar. 506: 124-134Crossref changes bleach [26.Bednarz 32.Cardini U. al.Microbial dinitrogen holobionts exposed bleaching.Environ. 18: 2620-2633Crossref (12) 33.Pootakham W. al.Dynamics coral-associated microbiomes event.MicrobiologyOpen. 7e00604Crossref 34.Littman al.Metagenomic analysis event Reef.Environ. 2011; 651-660Crossref (38) 35.Pogoreutz al.Sugar evidence role bleaching.Glob. 3838-3848Crossref While heterotrophically acquired help maintain recover populations [30.Tremblay 36.Lyndby N.H. al.Effect photosynthesis, respiration budget damicornis.bioRxiv. 2018Google contribution sources well understood. At level, widely accepted one light-induced photodamage symbionts, oxidative both partners [37.Weis V.M. Cellular cnidarian bleaching: Stress causes collapse symbiosis.J. 2008; 211: 3059-3066Crossref (329) shown absence heat, and/or 38.Rosset al.Phosphate deficiency reflected ultrastructure dinoflagellates.Mar. Pollut. Bull. 118: 180-187Crossref (7) 39.Tolleter D. al.Coral independent photosynthetic activity.Curr. 1782-1786Abstract 40.Nielsen D.A. single cell perspective.ISME 12: 1558-1567Crossref (3) 41.Rosset al.Ultrastructural biomarkers algae reflect particulate food holobiont.Front. Sci. 2: 103Crossref highlighting alternative pathways (Box 1). Importantly, now mounting initiation 25.Pogoreutz 42.Ezzat al.Limited Achilles heel ocean.Sci. 31768Crossref (14) 43.Baker D.M. al.Climate parasitism symbiosis.ISME 921-930Crossref (15) 44.Baker al.Nitrate competition varies among Symbiodinium clades.ISME 1248-1251Crossref (43) 45.Krueger T. al.Common Northern Red Sea resistant acidification.R. Soc. Open 4: 170038Crossref (22) 46.Gibbin E.M. al.Short-term acclimation modifies condition 5: 10Crossref 47.Krueger al.Temperature induce tissue allocation – NanoSIMS study.Sci. 12710Crossref Therefore, should considered, addition predicting stress.Box 1Coral Absence Photo-oxidative StressCoral contemporarily understood damage More specifically, temperatures render incoming resulting production reactive oxygen (ROS) cause tissues occur without characteristic [35.Pogoreutz Scholar].Tolleter al. [39.Tolleter observed dark, ROS. was similar nature control (kept light), demonstrating high directly photosystems Nielsen [40.Nielsen later found ROS light. were produced symbiont, released no attributable effects detected either corroborating field observations superoxide unrelated status [145.Diaz J.M. al.Species-specific event.Nat. Commun. 13801Crossref Furthermore, expel healthy [146.Ralph P.J. al.Zooxanthellae expelled 33°C competent.Mar. Prog. Ser. 2001; 220: 163-168Crossref 147.Bhagooli Hidaka M. Release zooxanthellae intact Galaxea fascicularis stress.Mar. 2004; 145: 329-337Crossref 148.Ralph al.Temporal effective quantum yield 2005; 316: 17-28Crossref (31) 149.Hill Ralph Post-bleaching viability damicornis.Mar. 2007; 352: 137-144Crossref does require could instead need eject dividing [150.Baghdasarian G. Muscatine Preferential expulsion cells mechanism regulating algal–cnidarian symbiosis.Biol. 2000; 199: 278-286Crossref (75) Scholar].Coral solely disruption kept phosphate sustain minimal communities, corresponding biomass increasing severity N:P (nitrate enrichment) moderate pathway originate internally, skewed microbial Scholar].It important note examples mutually exclusive extensively characterized Rather, point exacerbate 49.Wooldridge S.A. A conceptual warm-water breakdown coral–algae endosymbiosis.Mar. 60: 483-496Crossref Tolleter cont

Language: Английский

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Responses of Coral-Associated Bacterial Communities to Local and Global Stressors

Frontiers in Marine Science, Journal Year: 2017, Volume and Issue: 4

Published: Aug. 15, 2017

The microbial contribution to ecological resilience is still largely overlooked in coral reef ecology. Coral-associated bacteria serve a wide variety of functional roles with reference the host, and thus, composition overall microbiome community can strongly influence health survival. Here, we synthesize findings recent studies (n=45) that evaluated impacts top three stressors facing reefs, climate change, water pollution overfishing, on structure diversity. Contrary species losses are typical many communities under stress, here show richness tends be higher rather than lower for stressed corals (i.e. ~60% cases), regardless stressor. Microbial responses stress were taxonomically consistent across stressors, specific taxa typically increasing abundance (e.g. Vibrionales, Flavobacteriales, Rhodobacterales, Altermonadales, Rhizobiales, Rhodospirillales Desulfovibrionales) others declining Oceanosprillales). Emerging evidence also suggests may increase beta diversity amongst colonies, potentially reflecting reduced ability host regulate its microbiome. Moving forward, will need discern implications stress-induced shifts hosts able use identify resilient corals. present supports hypothesis play important resilience, encourage focus contributions future research.

Language: Английский

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Climate change promotes parasitism in a coral symbiosis

The ISME Journal, Journal Year: 2018, Volume and Issue: 12(3), P. 921 - 930

Published: Jan. 23, 2018

Abstract Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen carbon, respectively. Among most sensitive taxa to these changes scleractinian corals, which engineer biodiverse ecosystems on Earth. Corals’ sensitivity is a consequence their evolutionary investment in symbiosis with dinoflagellate alga, Symbiodinium. Together, coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association reduces fitness. It been theorized that, when reefs become mutualistic Symbiodinium sequester more resources for own growth, thus parasitizing hosts nutrition. Here, we tested hypothesis that sub-bleaching temperature excess promotes symbiont parasitism by measuring respiration (costs) assimilation translocation both carbon (energy) (growth; benefits) within Orbicella faveolata hosting one two phylotypes using dual stable isotope tracer incubation at ambient (26 °C) (31 temperatures under elevated nitrate. Warming 31 °C reduced net primary productivity (NPP) 60% due increased decreased host %carbon 15% no apparent cost symbiont. Concurrently, 14 32%, respectively while increasing mitotic index 15%, whereas did not gain proportional increase translocated photosynthates. We conclude disparity benefits costs partners evidence major implications resilience threat global change.

Language: Английский

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The microbiome in threatened species conservation

Biological Conservation, Journal Year: 2018, Volume and Issue: 229, P. 85 - 98

Published: Nov. 24, 2018

Language: Английский

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