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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Mapping coral reefs using consumer-grade drones and structure from motion photogrammetry techniques

Coral Reefs, Journal Year: 2016, Volume and Issue: 36(1), P. 269 - 275

Published: Nov. 28, 2016

Language: Английский

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Coral reef ecosystem functioning: eight core processes and the role of biodiversity

Frontiers in Ecology and the Environment, Journal Year: 2019, Volume and Issue: 17(8), P. 445 - 454

Published: July 30, 2019

Coral reefs are in global decline. Reversing this trend is a primary management objective but doing so depends on understanding what keeps desirable states (ie “functional”). Although there evidence that coral thrive under certain conditions (eg moderate water temperatures, limited fishing pressure), the dynamic processes promote ecosystem functioning and its internal drivers community structure) poorly defined explored. Specifically, despite decades of research suggesting positive relationship between biodiversity across biomes, few studies have explored reef systems. We propose practical definition functioning, centered eight complementary ecological processes: calcium carbonate production bioerosion, herbivory, secondary predation, nutrient uptake release. Connecting species niches, functional diversity communities, rates key can provide novel, quantitative dependence communities will chart transition Anthropocene. This contribute urgently needed guidance for these important ecosystems.

Language: Английский

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Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages

Biological Journal of the Linnean Society, Journal Year: 2016, Volume and Issue: unknown

Published: Nov. 1, 2016

Coral reef ecosystems are remarkable for their high productivity in nutrient-poor waters. A proportion of primary production is consumed by the dominant herbivore assemblage, teleost fishes, many which product recent and rapid diversification. Our review synthesis trophodynamics herbivorous fishes suggests that current models underestimate level resource partitioning, thus trophic innovation, this diverse assemblage. We examine several lines evidence including feeding observations, anatomy, biochemical analyses diet, tissue composition digestive processes to show prevailing view (including explicit models) parrotfishes as consumers macroscopic algae incompatible with available data. Instead, data consistent hypothesis most microphages target cyanobacteria other protein-rich autotrophic microorganisms live on (epilithic) or within (endolithic) calcareous substrata, epiphytic seagrasses, endosymbiotic sessile invertebrates. This novel parrotfish biology provides a unified explanation apparently disparate range substrata used parrotfishes, integrates nutrition ecological roles bioerosion sediment transport. Accelerated evolution can now be explained result (1) ability utilize food i.e. microscopic autotrophs; (2) partitioning habitat successional stage.

Language: Английский

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Climate Change, Coral Loss, and the Curious Case of the Parrotfish Paradigm: Why Don't Marine Protected Areas Improve Reef Resilience?

Annual Review of Marine Science, Journal Year: 2019, Volume and Issue: 11(1), P. 307 - 334

Published: Jan. 3, 2019

Scientists have advocated for local interventions, such as creating marine protected areas and implementing fishery restrictions, ways to mitigate stressors limit the effects of climate change on reef-building corals. However, in a literature review, we find little empirical support notion managed resilience. We outline some reasons why protection herbivorous fish (especially parrotfish) had effect coral One key explanation is that impacts (e.g., pollution fishing) are often swamped by much greater ocean warming Another sheer complexity (including numerous context dependencies) five cascading links assumed managed-resilience hypothesis. If reefs cannot be saved actions alone, then it time face reef degradation head-on, directly addressing anthropogenic change—the root cause global decline.

Language: Английский

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