Meta-organism gene expression reveals that the impact of nitrate enrichment on coral larvae is mediated by their associated Symbiodiniaceae and prokaryotic assemblages
Tóm tắt
Coral meta-organisms consist of the coral, and its associated Symbiodiniaceae (dinoflagellate algae), bacteria, and other microbes. Corals can acquire photosynthates from Symbiodiniaceae, whilst Symbiodiniaceae uses metabolites from corals. Prokaryotic microbes provide Symbiodiniaceae with nutrients and support the resilience of corals as meta-organisms. Eutrophication is a major cause of coral reef degradation; however, its effects on the transcriptomic response of coral meta-organisms remain unclear, particularly for prokaryotic microbes associated with corals in the larval stage. To understand acclimation of the coral meta-organism to elevated nitrate conditions, we analyzed the physiological and transcriptomic responses of Pocillopora damicornis larvae, an ecologically important scleractinian coral, after 5 days of exposure to elevated nitrate levels (5, 10, 20, and 40 µM). The major differentially expressed transcripts in coral, Symbiodiniaceae, and prokaryotic microbes included those related to development, stress response, and transport. The development of Symbiodiniaceae was not affected in the 5 and 20 µM groups but was downregulated in the 10 and 40 µM groups. In contrast, prokaryotic microbe development was upregulated in the 10 and 40 µM groups and downregulated in the 5 and 20 µM groups. Meanwhile, coral larval development was less downregulated in the 10 and 40 µM groups than in the 5 and 20 µM groups. In addition, multiple larval, Symbiodiniaceae, and prokaryotic transcripts were significantly correlated with each other. The core transcripts in correlation networks were related to development, nutrient metabolism, and transport. A generalized linear mixed model, using least absolute shrinkage and selection operator, demonstrated that the Symbiodiniaceae could both benefit and cost coral larval development. Furthermore, the most significantly correlated prokaryotic transcripts maintained negative correlations with the physiological functions of Symbiodiniaceae. Results suggested that Symbiodiniaceae tended to retain more nutrients under elevated nitrate concentrations, thereby shifting the coral-algal association from mutualism towards parasitism. Prokaryotic microbes provided Symbiodiniaceae with essential nutrients and may control Symbiodiniaceae growth through competition, whereby prokaryotes can also restore coral larval development inhibited by Symbiodiniaceae overgrowth.
Tài liệu tham khảo
Bellwood DR, Hughes TP, Folke C, Nystrom M. Confronting the coral reef crisis. Nature. 2004;429:827–33.
Hughes TP, Huang H, Young MA. The wicked problem of China’s disappearing coral reefs. Conserv Biol. 2013;27:261–9.
Fabricius KE. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull. 2005;50:125–46.
D’Angelo C, Wiedenmann J. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain. 2014;7:82–93.
Duprey NN, Yasuhara M, Baker DM. Reefs of tomorrow: eutrophication reduces coral biodiversity in an urbanized seascape. Glob Chang Biol. 2016;22:3550–65.
Vega Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Chang Biol. 2014;20:544–54.
Shantz AA, Burkepile DE. Context-dependent effects of nutrient loading on the coral–algal mutualism. Ecology. 2014;95:1995–2005.
Beraud E, Gevaert F, Rottier C, Ferrier-Pagès C. The response of the scleractinian coral Turbinaria reniformis to thermal stress depends on the nitrogen status of the coral holobiont. J Exp Biol. 2013;216:2665–74.
Ezzat L, Maguer J-F, Grover R, Ferrier-Pagès C. Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean. Sci Rep. 2016;6:31768.
Ezzat L, Maguer J-F, Grover R, Rottier C, Tremblay P, Ferrier-Pagès C. Nutrient starvation impairs the trophic plasticity of reef-building corals under ocean warming. Funct Ecol. 2019;33:643–53.
Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol. 2009;23:539–50.
Hoogenboom M, Beraud E, Ferrier-Pagès C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs. 2010;29:21–9.
Morris LA, Voolstra CR, Quigley KM, Bourne DG, Bay LK. Nutrient availability and metabolism affect the stability of coral–Symbiodiniaceae symbioses. Trends Microbiol. 2019;27:678–89.
Benavides M, Bednarz VN, Ferrier-Pagès C. Diazotrophs: overlooked key players within the coral symbiosis and tropical reef ecosystems? Front Mar Sci. 2017;4:10.
Tong H, Cai L, Zhou G, Zhang W, Huang H, Qian P-Y. Correlations between prokaryotic microbes and stress-resistant algae in different corals subjected to environmental stress in Hong Kong. Front Microbiol. 2020;11:686.
Cunning R, Baker AC. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang. 2012;3:259.
Bourne DG, Morrow KM, Webster NS. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol. 2016;70:317–40.
Ainsworth TD, Thurber RV, Gates RD. The future of coral reefs: a microbial perspective. Trends Ecol Evol. 2010;25:233–40.
Hillyer KE, Dias D, Lutz A, Roessner U, Davy SK. 13C metabolomics reveals widespread change in carbon fate during coral bleaching. Metabolomics. 2017;14:12.
Rädecker N, Pogoreutz C, Voolstra CR, Wiedenmann J, Wild C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 2015;23:490–7.
Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, et al. A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis. ISME J. 2012;6:1314–24.
Lapointe BE. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr. 1997;42:1119–31.
Schaffelke B, Klumpp DW. Nutrient-limited growth of the coral reef macroalga Sargassum baccularia and experimental growth enhancement by nutrient addition in continuous flow culture. Mar Ecol Prog Ser. 1998;164:199–211.
Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, et al. A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Pollut Bull. 2012;65:320–32.
Hallock P, Schlager W. Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios. 1986;1:389–98.
Bruno JF, Petes LE, Harvell CD, Hettinger A. Nutrient enrichment can increase the severity of coral diseases. Ecol Lett. 2003;6:1056–61.
Voss JD, Richardson LL. Nutrient enrichment enhances black band disease progression in corals. Coral Reefs. 2006;25:569–76.
Haas AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA, et al. Global microbialization of coral reefs. Nat Microbiol. 2016;1:16042.
Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret FE, Postle AD, et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang. 2013;3:160–4.
Wooldridge SA. Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences. 2013;10:1647–58.
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L. Population control in symbiotic corals. Bioscience. 1993;43:606–11.
Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, et al. Metagenomic analysis of stressed coral holobionts. Environ Microbiol. 2009;11:2148–63.
Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol Evol. 2018;8:2240–52.
Rivest EB, Kelly MW, DeBiasse MB, Hofmann GE. Host and symbionts in Pocillopora damicornis larvae display different transcriptomic responses to ocean acidification and warming. Front Mar Sci. 2018;5:186.
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS. Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol. 2010;25:633–42.
Kitchen RM, Piscetta M, de Souza MR, Lenz EA, Schar DWH, Gates RD, et al. Symbiont transmission and reproductive mode influence responses of three Hawaiian coral larvae to elevated temperature and nutrients. Coral Reefs. 2020;39:419–31.
Serrano XM, Miller MW, Hendee JC, Jensen BA, Gapayao JZ, Pasparakis C, et al. Effects of thermal stress and nitrate enrichment on the larval performance of two Caribbean reef corals. Coral Reefs. 2018;37:173–82.
Bassim K, Sammarco P. Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigosa). Mar Biol. 2003;142:241–52.
Fan TY, Li JJ, Ie SX, Fang LS. Lunar periodicity of larval release by pocilloporid corals in southern Taiwan. Zool Stud. 2002;41:288–94.
Lin SJ, Cheng SF, Song B, Zhong X, Lin X, Li WJ, et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science. 2015;350:691–4.
Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, et al. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature. 2011;476:320-U382.
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438:90–3.
Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.
Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.
Noga Stambler NP, Zvy Dubinsky, and John Stimson. Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pac Sci. 1991;45:299–307.
Loya Y, Lubinevsky H, Rosenfeld M, Kramarsky-Winter E. Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar Pollut Bull. 2004;49:344–53.
Szmant AM. Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries. 2002;25:743–66.
Dunn JG, Sammarco PW, LaFleur G. Effects of phosphate on growth and skeletal density in the scleractinian coral Acropora muricata: a controlled experimental approach. J Exp Mar Biol Ecol. 2012;411:34–44.
Bongiorni L, Shafir S, Angel D, Rinkevich B. Survival, growth and gonad development of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar Ecol Prog Ser. 2003;253:137–44.
Maor-Landaw K, van Oppen MJH, McFadden GI. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae). Ecol Evol. 2020;10:451–66.
Kenkel CD, Bay LK. Novel transcriptome resources for three scleractinian coral species from the Indo-Pacific. GigaScience. 2017;6:gix074.
Tanaka Y, Suzuki A, Sakai K. The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system. ISME J. 2018;12:860–8.
Gates RD, Hoegh-Guldberg O, McFall-Ngai MJ, Bil KY, Muscatine L. Free amino acids exhibit anthozoan “host factor” activity: they induce the release of photosynthate from symbiotic dinoflagellates in vitro. Proc Natl Acad Sci USA. 1995;92:7430–4.
Cook CB, Davy SK. Are free amino acids responsible for the ‘host factor’ effects on symbiotic zooxanthellae in extract. Hydrobiologia. 2001;461:71–8.
Titlyanov EA, Titlyanova TV, Leletkin VA, Tsukahara J, van Woesik R, Yamazato K. Degradation of zooxanthellae and regulation of their density in hermatypic corals. Mar Ecol Prog Ser. 1996;139:167–78.
Xiang T, Lehnert E, Jinkerson RE, Clowez S, Kim RG, DeNofrio JC, et al. Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations. Nat Commun. 2020;11:108.
Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N. Climate change promotes parasitism in a coral symbiosis. ISME J. 2018;12:921–30.
Rädecker N, Pogoreutz C, Gegner HM, Cárdenas A, Roth F, Bougoure J, et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc Natl Acad Sci USA. 2021;118(5):e2022653118.
Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism–parasitism continuum*. New Phytol. 1997;135:575–85.
Douglas AE. Conflict, cheats and the persistence of symbioses. New Phytol. 2008;177:849–58.
Neuhauser C, Fargione JE. A mutualism–parasitism continuum model and its application to plant–mycorrhizae interactions. Ecol Modell. 2004;177:337–52.
Ezzat L, Maguer JF, Grover R, Ferrier-Pagès C. New insights into carbon acquisition and exchanges within the coral - dinoflagellate symbiosis under NH4+ and NO3- supply. Proc Royal Soc B. 2015;282:142–50.
Lawson CA, Raina J-B, Kahlke T, Seymour JR, Suggett DJ. Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium. Environ Microbiol Rep. 2018;10:7–11.
Frommlet JC, Sousa ML, Alves A, Vieira SI, Suggett DJ, Serôdio J. Coral symbiotic algae calcify ex hospite in partnership with bacteria. Proc Natl Acad Sci USA. 2015;112:6158–63.
Seymour JR, Amin SA, Raina J-B, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:17065.
Zhang X, Tian X, Ma L, Feng B, Liu Q, Yuan L, et al. Biodiversity of the symbiotic bacteria associated with toxic marine dinoflagellate Alexandrium tamarense. J Biosci Med. 2015;3:6.
Peixoto RS, Rosado PM, Leite DCDA, Rosado AS, Bourne DG. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front Microbiol. 2017;8:341.
Bernasconi R, Stat M, Koenders A, Huggett MJ. Global networks of Symbiodinium-bacteria within the coral holobiont. Microb Ecol. 2019;77:794–807.
Raina J-B, Clode PL, Cheong S, Bougoure J, Kilburn MR, Reeder A, et al. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. eLife. 2017;6:e23008.
Curson ARJ, Liu J, Martinez AB, Green RT, Chan YH, Carrion O, et al. Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat Microbiol. 2017;2:17009.
Raina JB, Tapiolas D, Motti CA, Foret S, Seemann T, Tebben J, et al. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals. PeerJ. 2016;4:e2275.
Jones GB, King S. Dimethylsulphoniopropionate (DMSP) as an indicator of bleaching tolerance in scleractinian corals. J Mar Sci Eng. 2015;3:444–65.
Cole JJ. Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Evol Syst. 1982;13:291–314.
Fuentes JL, Garbayo I, Cuaresma M, Montero Z, González-Del-Valle M, Vílchez C. Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar Drugs. 2016;14:100.
He L, Lin Z, Wang Y, He X, Zhou J, Guan M, et al. Facilitating harmful algae removal in fresh water via joint effects of multi-species algicidal bacteria. J Hazard Mater. 2021;403:123662.
Littman RA, Bourne DG, Willis BL. Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol Ecol. 2010;19:1978–90.
Cao D, Cao W, Yu K, Wu G, Yang J, Su X, et al. Evaluation of anthropogenic influences on the Luhuitou fringing reef via spatial and temporal analyses (from isotopic values). J Geophys Res-Oceans. 2017;122:4431–43.
Roff G, Mumby PJ. Global disparity in the resilience of coral reefs. Trends Ecol Evol. 2012;27:404–13.
Guo J, Yu KF, Wang YH, Xu DQ, Huang XY, Zhao MX, et al. Nutrient distribution in coral reef degraded areas within Sanya Bay, South China Sea. J Coast Res. 2017;33:1148–60.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29:644–52.
Cunning R, Gates RD, Edmunds PJ. Using high-throughput sequencing of ITS2 to describe Symbiodinium metacommunities in St. John, US Virgin Islands. PeerJ. 2017;5:e3472.
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674–6.
Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
Fabregat A, Jupe S, Matthews L, Sidiropoulos K, Gillespie M, Garapati P, et al. The reactome pathway knowledgebase. Nucleic Acids Res. 2018;46:D649–55.
Naithani S, Gupta P, Preece J, D’Eustachio P, Elser JL, Garg P, et al. Plant Reactome: a knowledgebase and resource for comparative pathway analysis. Nucleic Acids Res. 2020;48:D1093–103.
Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:323.
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102:15545–50.
Groll A, Tutz G. Variable selection for generalized linear mixed models by L1-penalized estimation. Stat Comput. 2014;24:137–54.