Heat stress destabilizes symbiotic nutrient cycling in corals

Proceedings of the National Academy of Sciences, Journal Year: 2021, Volume and Issue: 118(5)

Published: Jan. 26, 2021

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While symptoms and consequences this breakdown coral-algal symbiosis have been extensively characterized, our understanding underlying causes remains incomplete. Here, we investigated nutrient fluxes physiological as well molecular responses widespread Stylophora pistillata heat stress prior onset identify processes involved in symbiosis. We show that altered cycling during is a primary driver functional Heat increased metabolic energy demand host, which was compensated by catabolic degradation amino acids. The resulting shift from net uptake release ammonium holobiont subsequently promoted growth algal symbionts retention photosynthates. Together, these form feedback loop will gradually lead decoupling carbon translocation symbiont host. Energy limitation symbiotic thus key factors early response, directly contributing Interpreting stability light its interactions provides missing link environmental drivers may ultimately help uncover fundamental underpinning functioning endosymbioses general.

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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Microbial evolution and transitions along the parasite–mutualist continuum

Nature Reviews Microbiology, Journal Year: 2021, Volume and Issue: 19(10), P. 623 - 638

Published: April 19, 2021

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts evolve rapidly, resulting in drastic transitions along parasite–mutualist continuum. In this Review, we integrate theoretical empirical findings discuss mechanisms underpinning these evolutionary shifts, as well ecological drivers why some host–microorganism may stuck at end of addition having biomedical consequences, understanding dynamic life microorganisms reveals how symbioses shape an organism's biology entire community, particularly a changing world. for organisms. Drew, Stevens King continuum, underlying changes, selective pressures involved common approaches studying them.

Language: Английский

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Impacts of nitrogen pollution on corals in the context of global climate change and potential strategies to conserve coral reefs

The Science of The Total Environment, Journal Year: 2021, Volume and Issue: 774, P. 145017 - 145017

Published: Feb. 1, 2021

Language: Английский

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Anthropogenic temperature fluctuations and their effect on aquaculture: A comprehensive review

Aquaculture and Fisheries, Journal Year: 2022, Volume and Issue: 7(3), P. 223 - 243

Published: Jan. 5, 2022

The reliance of aquaculture production on the ambient environment suggests its vulnerability to climate change. Global warming has led increase in water temperatures hence exerting a direct and indirect effect several species. Temperature is one major abiotic driving factors growth survival aquatic organisms. Extreme above their thermal threshold tend lower performance, health, productivity. This paper, therefore, aims give detailed comprehensive review influence anthropogenic temperature general animal physiology, survival, reproduction, digestive enzyme activity, immunity, differential expression microRNAs apoptosis-associated genes as well gut skin microbiome Likewise, impacts increasing ecosystems with regards pathogen-associated disease outbreaks, parasites, vaccine efficacy toxicity, uptake heavy metals pesticides are presented. To provide examples how will impact global trends production, couple freshwater, euryhaline, marine species, cold-water warm have been chosen broader perspective different species respond fluctuations threshold. In same regard, mitigation strategies for change adaptation context such nutrition, genetics, selective breeding, biotechnology, nanotechnology, bacteriophage therapy management husbandry practices discussed ensure sustainable continued

Language: Английский

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Triggers, cascades, and endpoints: connecting the dots of coral bleaching mechanisms

Biological reviews/Biological reviews of the Cambridge Philosophical Society, Journal Year: 2024, Volume and Issue: 99(3), P. 715 - 752

Published: Jan. 12, 2024

ABSTRACT The intracellular coral–dinoflagellate symbiosis is the engine that underpins success of coral reefs, one most diverse ecosystems on planet. However, breakdown and loss microalgal symbiont (i.e. bleaching) due to environmental changes are resulting in rapid degradation reefs globally. There an urgent need understand cellular physiology bleaching at mechanistic level help develop solutions mitigate reef crisis. Here, unprecedented scope, we present novel models integrate putative mechanisms within a common framework according triggers (initiators bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, photoinhibition, unfolded protein response, nitric oxide), endpoints (mechanisms loss, apoptosis, necrosis, exocytosis/vomocytosis). supported by direct evidence from cnidarian systems, indirectly through comparative evolutionary analyses non‐cnidarian systems. With this approach, new have been established between initiated different triggers. In particular, provide insights into poorly understood connections highlight role mechanism i.e. ‘symbiolysosomal digestion’, which symbiophagy. This review also increases approachability for specialists non‐specialists mapping vast landscape atlas comprehensible detailed models. We then discuss major knowledge gaps how future research may improve understanding cascade pathways (endpoints).

Language: Английский

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Cell Biology of Coral Symbiosis: Foundational Study Can Inform Solutions to the Coral Reef Crisis

Integrative and Comparative Biology, Journal Year: 2019, Volume and Issue: 59(4), P. 845 - 855

Published: May 24, 2019

Abstract Coral reefs are faced with almost complete destruction by the end of century due to global warming unless humanity can cap temperature rise. There is now a race develop diverse set solutions save coral reefs. In this perspective, case made for understanding cell biology coral–dinoflagellate symbiosis help inform development saving Laboratory model systems study symbiosis, including sea anemone Exaiptasia pallida, featured as valuable tools in fight corals. The roles host innate immunity and inter-partner nutrient dynamics onset, ongoing maintenance, dysregulation reviewed discussed. Key immune genes pathways, such glycan–lectin interactions, sphingosine rheostat, cytokine transforming growth factor beta shown modulate response symbiotic state. An upset homeostatic inorganic balance during heat stress high exogenous availability credited driving partnership toward bleaching. Specific examples given where knowledge informing solutions, studies showing clear limitations value partner switching acclimatization protocols. Finally, emphasis placed on rapid advancement try meet urgent need solutions. This includes real-time open communication colleagues successes failures, sharing resources information, working together spirit collective mission

Language: Английский

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Host-associated microbiomes drive structure and function of marine ecosystems

PLoS Biology, Journal Year: 2019, Volume and Issue: 17(11), P. e3000533 - e3000533

Published: Nov. 11, 2019

The significance of symbioses between eukaryotic hosts and microbes extends from the organismal to ecosystem level underpins health Earth's most threatened marine ecosystems. Despite rapid growth in research on host-associated microbes, individual microbial symbionts consortia significantly relevant taxa, little is known about their interactions with vast majority host species. We outline priorities strengthen our current knowledge host-microbiome how they shape argue that such advances will help predict responses species, communities, ecosystems stressors driven by human activity inform future management strategies.

Language: Английский

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Toxicological effects of two organic ultraviolet filters and a related commercial sunscreen product in adult corals

Environmental Pollution, Journal Year: 2018, Volume and Issue: 245, P. 462 - 471

Published: Nov. 13, 2018

Language: Английский

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Nitrogen Identity Drives Differential Impacts of Nutrients on Coral Bleaching and Mortality

Ecosystems, Journal Year: 2019, Volume and Issue: 23(4), P. 798 - 811

Published: Sept. 11, 2019

Language: Английский

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