Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis DOI Creative Commons
Laura Baldassarre, Hua Ying, Adam M. Reitzel

et al.

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: July 1, 2022

Abstract At the current rate of climate change, it is unlikely that multicellular organisms will be able to adapt changing environmental conditions through genetic recombination and natural selection alone. Thus, critical understand alternative mechanisms allow cope with rapid changes. Here, we use sea anemone Nematostella vectensis , which has evolved capability surviving in a wide range temperatures salinities, as model investigate microbiota source adaptation. We long-term acclimate polyps low, medium, high temperatures, test impact microbiota-mediated plasticity on animal acclimation. Using same clonal line, propagated from single polyp, allows us eliminate effects host genotype. The higher thermal tolerance animals acclimated temperature can transferred non-acclimated transplantation. offspring fitness highest F0 females specific members are transmitted next generation. These results indicate contribute acclimation its transmission generation may represent mechanism for

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

Rapid adaptive responses to climate change in corals DOI Open Access
Gergely Torda, Jennifer M. Donelson, Manuel Aranda

et al.

Nature Climate Change, Journal Year: 2017, Volume and Issue: 7(9), P. 627 - 636

Published: Sept. 1, 2017

Language: Английский

Citations

384

Nutrient Availability and Metabolism Affect the Stability of Coral–Symbiodiniaceae Symbioses DOI Creative Commons
Luke A. Morris, Christian R. Voolstra, Kate M. Quigley

et al.

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

Citations

269

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

Turbid reefs moderate coral bleaching under climate‐related temperature stress DOI Creative Commons
Shannon Sully, Robert van Woesik

Global Change Biology, Journal Year: 2020, Volume and Issue: 26(3), P. 1367 - 1373

Published: Jan. 8, 2020

Thermal-stress events that cause coral bleaching and mortality have recently increased in frequency severity. Yet few studies explored conditions moderate bleaching. Given high light ocean temperature together bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal-stress than other localities. We analyzed temperature, turbidity data from 3,694 sites worldwide a Bayesian model found Kd 490, measurement positively related turbidity, between 0.080 0.127 events. Approximately 12% of the world's reefs exist within this "moderating turbidity" range, 30% moderating Coral Triangle. suggest these nearshore environments may provide some refuge through climate change, but will need conservation status sustain them close dense human populations.

Language: Английский

Citations

146

A framework for understanding gene expression plasticity and its influence on stress tolerance DOI Open Access
Hanny E. Rivera, Hannah E. Aichelman, James E. Fifer

et al.

Molecular Ecology, Journal Year: 2021, Volume and Issue: 30(6), P. 1381 - 1397

Published: Jan. 27, 2021

Phenotypic plasticity can serve as a stepping stone towards adaptation. Recently, studies have shown that gene expression contributes to emergent stress responses such thermal tolerance, with tolerant and susceptible populations showing distinct transcriptional profiles. However, given the dynamic nature of expression, interpreting transcriptomic results in way elucidates functional connection between observed response is challenging. Here, we present conceptual framework guide interpretation reaction norms context tolerance. We consider evolutionary adaptive potential discuss influence sampling timing, resilience, well complexities related life history when dynamics how these patterns relate host highlight corals case study demonstrate value this for non-model systems. As species face rapidly changing environmental conditions, modulating mechanistic link from genetic cellular processes physiological allow organisms thrive under novel conditions. Interpreting or whether employ ensure short-term survival will be critical understanding global impacts climate change across diverse taxa.

Language: Английский

Citations

121

Coral‐bleaching responses to climate change across biological scales DOI
Robert van Woesik, Tom Shlesinger, Andréa G. Grottoli

et al.

Global Change Biology, Journal Year: 2022, Volume and Issue: 28(14), P. 4229 - 4250

Published: April 27, 2022

Abstract The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one the greatest challenges this epiphenomenon is linking information across scientific disciplines spatial temporal scales. Here we review some seminal recent coral‐bleaching discoveries from an ecological, physiological, molecular perspective. We also evaluate which data processes can improve predictive models provide a conceptual framework that integrates measurements biological Taking integrative approach scales, using for example hierarchical estimate major coral‐reef processes, will not only rapidly advance science but necessary guide decision‐making conservation efforts. To conserve encourage implementing mesoscale sanctuaries (thousands km 2 ) transcend national boundaries. Such networks protected reefs reef connectivity, through larval dispersal transverse thermal environments, genotypic repositories may become essential units selection environmentally diverse locations. Together, multinational be best chance corals persist change, while humanity struggles reduce emissions greenhouse gases net zero.

Language: Английский

Citations

103

Characterization, costs, cues and future perspectives of phenotypic plasticity DOI Creative Commons
Hannah Schneider

Annals of Botany, Journal Year: 2022, Volume and Issue: 130(2), P. 131 - 148

Published: June 30, 2022

Abstract Background Plastic responses of plants to the environment are ubiquitous. Phenotypic plasticity occurs in many forms and at biological scales, its adaptive value depends on specific interactions with other plant traits organisms. Even though is norm rather than exception, complex nature has been a challenge characterizing expression plasticity, for fitness environmental cues that regulate expression. Scope This review discusses characterization costs approaches, considerations, promising research directions studying plasticity. genetically controlled heritable; however, little known about how organisms perceive, interpret respond cues, genes pathways associated Not every genotype plastic trait, not infinite, suggesting trade-offs, limits The timing, specificity duration critical their fitness. Conclusions There opportunities advance our understanding phenotypic New methodology technological breakthroughs enable study across scales multiple environments. Understanding mechanisms phenotypes influences ranges would benefit areas science ranging from basic applied breeding crop improvement.

Language: Английский

Citations

78

CRISPR/Cas9-mediated genome editing in a reef-building coral DOI Open Access
Phillip A. Cleves, Marie E. Strader, Line K. Bay

et al.

Proceedings of the National Academy of Sciences, Journal Year: 2018, Volume and Issue: 115(20), P. 5235 - 5240

Published: April 25, 2018

Significance Coral reefs are biodiversity hotspots of great ecological, economic, and aesthetic importance. Their global decline due to climate change other anthropogenic stressors has increased the urgency understand molecular bases various aspects coral biology, including interactions with algal symbionts responses stress. Recent genomic transcriptomic studies have yielded many hypotheses about genes that may be important in such processes, but rigorous testing these will require generation mutations affecting genes. Here, we demonstrate efficient production three target using recently developed CRISPR/Cas9 gene-editing technique. By clarifying basic genetic approaches should also provide a more solid foundation for coral-conservation efforts.

Language: Английский

Citations

147

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa DOI Creative Commons
Luke Thomas, Noah H. Rose, Rachael A. Bay

et al.

Frontiers in Marine Science, Journal Year: 2018, Volume and Issue: 4

Published: Feb. 1, 2018

Environmental heterogeneity gives rise to phenotypic variation through a combination of plasticity and fixed genetic effects. For reef-building corals, understanding the relative roles acclimatization adaptation in generating thermal tolerance is fundamental predicting future response coral populations climate change. The temperature mosaic lagoon Ofu Island, American Samoa, represents an ideal natural laboratory for studying corals. Two adjacent back-reef pools 500 meters apart have different profiles: highly variable (HV) pool experiences temperatures that range from 24.5°C 35°C, whereas moderately (MV) ranges 25°C 32°C. Standardized heat stress tests shown corals native HV consistently higher levels bleaching resistance than those MV pool. In this review, we summarize research into mechanisms underlying resistance, focusing on important genus Acropora. Both occur strongly define differences between pools. Most individual shift physiology become more resistant when moved warmer Lab based show these shifts begin as little week are equally sparked by exposure periodic high constant temperatures. Genome-wide data gene expression wide variety genes co-regulated modules change after experimental stress, acclimatization, even short term environmental fluctuations. Population scans associations corals' its alleles at 100s 1000s nuclear no single confers strong effects within or species. Symbionts also tend differ species, reflection host genotype specific symbiont types. We conclude review placing work context parallel going other reefs ecosystems around world broader framework reef resilience face near

Language: Английский

Citations

144