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

Current Biology, Journal Year: 2018, Volume and Issue: 28(16), P. 2570 - 2580.e6

Published: Aug. 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.

Language: Английский

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

Frontiers in Microbiology, Journal Year: 2017, Volume and Issue: 8

Published: March 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

Language: Английский

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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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Acute microplastic exposure raises stress response and suppresses detoxification and immune capacities in the scleractinian coral Pocillopora damicornis

Environmental Pollution, Journal Year: 2018, Volume and Issue: 243, P. 66 - 74

Published: Aug. 20, 2018

Language: Английский

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A genomic view of the reef-building coral Porites lutea and its microbial symbionts

Nature Microbiology, Journal Year: 2019, Volume and Issue: 4(12), P. 2090 - 2100

Published: Sept. 23, 2019

Language: Английский

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Bioengineering of Microalgae: Recent Advances, Perspectives, and Regulatory Challenges for Industrial Application

Frontiers in Bioengineering and Biotechnology, Journal Year: 2020, Volume and Issue: 8

Published: Sept. 3, 2020

Microalgae, due to their complex metabolic capacity, are being continuously explored for nutraceuticals, pharmaceuticals and other industrially important bioactives. However, suboptimal yield productivity of the bioactive interest in local robust wild-type strains perennial concerns industrial applications. To overcome such limitations, strain improvement through genetic engineering could play a decisive role. Though advanced tools have emerged at greater pace, they still remains under-used microalgae as compared microorganisms. Pertaining this, we reviewed progress made so far development molecular techniques, deployment engineering. The recent availability genome sequences omics datasets form diverse species remarkable potential guide strategic momentum program. This review focuses on significant improvements resources, mutant libraries high throughput screening methodologies helpful augment research model non-model microalgae. Authors also summarized case studies genetically engineered microalgae, highlight opportunities challenges that emerging from current application genome-editing facilitate microalgal improvement. Towards end, regulatory biosafety issues use commercial applications described.

Language: Английский

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Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

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

Published: July 11, 2018

Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms trophic foundation world's coral reef ecosystems. Here we present first draft genome goreaui (Clade C, type C1: 1.03 Gbp), one most ubiquitous endosymbionts associated with corals, an improved kawagutii F, strain CS-156: 1.05 Gbp) to further elucidate genomic signatures this symbiosis. Comparative analysis four available genomes against other dinoflagellate led identification 2460 nuclear gene families (containing 5% genes) that show evidence positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis modification amino acids glycoproteins, stress response. Further, identify extensive sets for meiosis response light stress. These provide a foundational resource advancing our understanding biology coral-algal

Language: Английский

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The Vulnerability and Resilience of Reef-Building Corals

Current Biology, Journal Year: 2017, Volume and Issue: 27(11), P. R528 - R540

Published: June 1, 2017

Language: Английский

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Extending the natural adaptive capacity of coral holobionts

Nature Reviews Earth & Environment, Journal Year: 2021, Volume and Issue: 2(11), P. 747 - 762

Published: Oct. 12, 2021

Language: Английский

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