Thompson JR, Rivera HE, Closek CJ, Medina M. Microbes in the coral holobiont: partners through evolution, development, and ecological interactions. Front Cell Infect Microbiol. 2014;4:176.
Google Scholar
Pogoreutz C, Voolstra CR, Rädecker N, Weis V, Cardenas A, Raina J-B. The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes. In: Bosch TCG, Hadfield MG, editors. Cellular dialogues in the holobiont. CRC Press; 2020. p. 91–118.
Stanley GD, van de Schootbrugge B. The evolution of the coral–algal symbiosis. In: van Oppen MJH, Lough JM, editors. Coral bleaching: patterns, processes, causes and consequences. Berlin, Heidelberg: Springer; 2009. p. 7–19.
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol. 2018;28:2570–80.e6.
Google Scholar
Muscatine L. The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs. 1990;25:75–87.
Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, Meibom A. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol Biol. 2011;11:316.
Google Scholar
Frankowiak K, Wang XT, Sigman DM, Gothmann AM, Kitahara MV, Mazur M, et al. Photosymbiosis and the expansion of shallow-water corals. Sci Adv. 2016;2:e1601122.
Google Scholar
Wild C, Hoegh-Guldberg O, Naumann MS, Colombo-Pallotta MF, Ateweberhan M, Fitt WK, et al. Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res. 2011;62:205–15.
Google Scholar
Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC. et al. Coral reefs in the Anthropocene. Nature. 2017;546:82–90.
Google Scholar
Kleypas J, Allemand D, Anthony K, Baker AC, Beck MW, Hale LZ, et al. Designing a blueprint for coral reef survival. Biol Conserv. 2021;257:109107.
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.
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science. 2018;359:80–83.
Google Scholar
Voolstra CR, Suggett DJ, Peixoto RS, John E, Parkinson KM, Quigley CB, Silveira M, et al. Extending the natural adaptive capacity of coral holobionts. Nat Rev Earth Environ. 2021;2:747–62; https://doi.org/10.1038/s43017-021-00214-3.
Google Scholar
Suggett DJ, Smith DJ. Coral bleaching patterns are the outcome of complex biological and environmental networking. Glob Chang Biol. 2020;26:68–79.
Google Scholar
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:e2022653118.
Google Scholar
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.
Google Scholar
Muscatine L, Porter JW. Reef Corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience. 1977;27:454–60.
Falkowski PG, Dubinsky Z, Muscatine L, Porter JW. Light and the bioenergetics of a symbiotic coral. Bioscience. 1984;34:705–9.
Google Scholar
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L. Population control in symbiotic corals. Bioscience. 1993;43:606–11.
Peng S-E, Chen C-S, Song Y-F, Huang H-T, Jiang P-L, Chen W-NU, et al. Assessment of metabolic modulation in free-living versus endosymbiotic Symbiodinium using synchrotron radiation-based infrared microspectroscopy. Biol Lett. 2012;8:434–7.
Google Scholar
Krueger T, Horwitz N, Bodin J, Giovani M-E, Escrig S, Fine M, et al. Intracellular competition for nitrogen controls dinoflagellate population density in corals. Proc R Soc B. 2020;287:20200049.
Google Scholar
Roberty S, Béraud E, Grover R, Ferrier-Pagès C. Coral croductivity is co-limited by bicarbonate and ammonium availability. Microorganisms. 2020;8:640
Google Scholar
Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N. Climate change promotes parasitism in a coral symbiosis. ISME J. 2018;12:921–30.
Google Scholar
Cunning R, Muller EB, Gates RD, Nisbet RM. A dynamic bioenergetic model for coral- Symbiodinium symbioses and coral bleaching as an alternate stable state. J Theor Biol. 2017;431:49–62.
Google Scholar
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.
Google Scholar
Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang. 2012;3:160–4.
Houlbrèque F, Ferrier-Pagès C. Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc. 2009;84:1–17.
Google Scholar
Fiore CL, Jarett JK, Olson ND, Lesser MP. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 2010;18:455–63.
Google Scholar
Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C. Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol. 2008;211:860–5.
Google Scholar
Lema KA, Willis BL, Bourne DG. Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl Environ Microbiol. 2012;78:3136–44.
Google Scholar
Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR. Nitrogen fixation aligns with nifH abundance and expression in two coral trophic functional groups. Front Microbiol. 2017;8:1187.
Google Scholar
Olson ND, Lesser MP. Diazotrophic diversity in the Caribbean coral, Montastraea cavernosa. Arch Microbiol. 2013;195:853–9.
Google Scholar
Lesser MP, Morrow KM, Pankey SM, Noonan SHC. Diazotroph diversity and nitrogen fixation in the coral Stylophora pistillata from the Great Barrier Reef. ISME J. 2018;12:813–24.
Google Scholar
Moynihan MA, Goodkin NF, Morgan KM, Kho PYY, dos Santos AL, Lauro FM, et al. Coral-associated nitrogen fixation rates and diazotrophic diversity on a nutrient-replete equatorial reef. ISME J. 2021; https://doi.org/10.1038/s41396-021-01054-1.
Tilstra A, Pogoreutz C, Rädecker N, Ziegler M, Wild C, Voolstra CR. Relative diazotroph abundance in symbiotic Red Sea corals decreases with water depth. Front Mar Sci. 2019;6:372.
Bednarz VN, Cardini U, van Hoytema N, Al-Rshaidat MMD, Wild C. Seasonal variation in dinitrogen fixation and oxygen fluxes associated with two dominant zooxanthellate soft corals from the northern Red Sea. Mar Ecol Prog Ser. 2015;519:141–52.
Rädecker N, Meyer FW, Bednarz VN, Cardini U, Wild C. Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix. Mar Ecol Prog Ser. 2014;511:297–302.
Cardini U, Bednarz VN, Naumann MS, van Hoytema N, Rix L, Foster RA, et al. Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc B. 2015;282:20152257.
Google Scholar
Bednarz VN, van de Water JAJM, Grover R, Maguer J-F, Fine M, Ferrier-Pagès C. Unravelling the importance of diazotrophy in corals – combined assessment of nitrogen assimilation, diazotrophic community and natural stable isotope signatures. Front Microbiol. 2021;12:1638.
Santos HF, Carmo FL, Duarte G, Dini-Andreote F, Castro CB, Rosado AS, et al. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. 2014;8:2272–9.
Google Scholar
Cardini U, van Hoytema N, Bednarz VN, Rix L, Foster RA, Al-Rshaidat MMD, et al. Microbial dinitrogen fixation in coral holobionts exposed to thermal stress and bleaching. Environ Microbiol. 2016;18:2620–33.
Google Scholar
Bednarz VN, van de Water JAJM, Rabouille S, Maguer J-F, Grover R, Ferrier-Pagès C. Diazotrophic community and associated dinitrogen fixation within the temperate coral Oculina patagonica. Environ Microbiol. 2019;21:480–95.
Google Scholar
Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Voolstra CR, Wild C. Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching. Glob Chang Biol. 2017;23:3838–48.
Google Scholar
Bednarz VN, Grover R, Maguer J-F, Fine M, Ferrier-Pagès C. The assimilation of diazotroph-derived nitrogen by scleractinian corals depends on their metabolic status. mBio. 2017;8:e02058–16.
Google Scholar
Petrou K, Nunn BL, Padula MP, Miller DJ, Nielsen DA. Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora. Sci Rep. 2021;11:19061.
Google Scholar
Roth F, Rädecker N, Carvalho S, Duarte CM, Saderne V, Anton A, et al. High summer temperatures amplify functional differences between coral‐ and algae‐dominated reef communities. Ecology. 2021;102:e03226.
Google Scholar
Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE. 2008;3:e2836.
Google Scholar
Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK, Mincer T, et al. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl Environ Microbiol. 2013;79:4759–62.
Google Scholar
Gaby JC, Buckley DH. A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE. 2012;7:e42149.
Google Scholar
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
Google Scholar
R Core Team. R: a language and environment for statistical computing computer program. Vienna, Austria: R Foundation for Statistical Computing; 2021.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
Google Scholar
McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.
Google Scholar
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, et al. The vegan package. Community Ecol Package. 2007;10:631–7.
Roesch LFW, Dobbler PT, Pylro VS, Kolaczkowski B, Drew JC, Triplett EW. pime: A package for discovery of novel differences among microbial communities. Mol Ecol Resour. 2020;20:415–28.
Google Scholar
Guo K. microbial: do 16s data analysis and generate figures. R package version 1.14.4. 2021.
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–12.
Wang Q, Quensen JF, 3rd, Fish JA, Lee TK, Sun Y, Tiedje JM. et al. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio. 2013;4:e00592–13.
Google Scholar
Meunier V, Geissler L, Bonnet S, Rädecker N, Perna G, Grosso O, et al. Microbes support enhanced nitrogen requirements of coral holobionts in a high CO2 environment. Mol Ecol. 2021;30:5888–99 .
Angel R, Nepel M, Panhölzl C, Schmidt H, Herbold CW, Eichorst SA, et al. Evaluation of primers targeting the diazotroph functional gene and development of NifMAP – a bioinformatics pipeline for analyzing nifH amplicon data. Front Microbiol. 2018;9:703.
Google Scholar
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.
Google Scholar
Frank IE, Turk-Kubo KA, Zehr JP. Rapid annotation of nifH gene sequences using classification and regression trees facilitates environmental functional gene analysis. Environ Microbiol Rep. 2016;8:905–16.
Google Scholar
Berger SA, Krompass D, Stamatakis A. Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol. 2011;60:291–302.
Google Scholar
Hardy RW, Holsten RD, Jackson EK, Burns RC. The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol. 1968;43:1185–207.
Google Scholar
Breitbarth E, Mills MM, Friedrichs G, LaRoche J. The Bunsen gas solubility coefficient of ethylene as a function of temperature and salinity and its importance for nitrogen fixation assays: Bunsen coefficient and N2fixation. Limnol Oceanogr Methods 2004;2:282–8.
Zehr JP, Montoya JP. Measuring N2 fixation in the field. In: Bothe H, Ferguson SJ, Newton WE, editors. Biology of the nitrogen cycle. Elsevier; 2007. p. 193–205.
Soper FM, Simon C, Jauss V. Measuring nitrogen fixation by the acetylene reduction assay (ARA): is 3 the magic ratio?. Biogeochemistry. 2021;152:345–51.
Google Scholar
Lavy A, Eyal G, Neal B, Keren R, Loya Y, Ilan M. A quick, easy and non‐intrusive method for underwater volume and surface area evaluation of benthic organisms by 3D computer modelling. Methods Ecol Evol. 2015;6:521–31.
Wilson ST, Böttjer D, Church MJ, Karl DM. Comparative assessment of nitrogen fixation methodologies, conducted in the oligotrophic North Pacific Ocean. Appl Environ Microbiol. 2012;78:6516–23.
Google Scholar
Hoppe P, Cohen S, Meibom A. NanoSIMS: Technical aspects and applications in cosmochemistry and biological geochemistry. Geostand Geoanal Res. 2013;37:111–54.
Google Scholar
Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG, Apprill A, et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 2017;11:186–200.
Google Scholar
Savary R, Barshis DJ, Voolstra CR, Cárdenas A, Evensen NR, Banc-Prandi G, et al. Fast and pervasive transcriptomic resilience and acclimation of extremely heat tolerant coral holobionts from the northern Red Sea. Proc Natl Acad Sci USA. 2021;118:e2023298118.
Google Scholar
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG. Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science. 2004;305:997–1000.
Google Scholar
Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Iglesias-Prieto R. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser. 2007;346:143–52.
Google Scholar
Tilstra A, El-Khaled YC, Roth F, Rädecker N, Pogoreutz C, Voolstra CR, et al. Denitrification aligns with N2 fixation in Red Sea corals. Sci Rep. 2019;9:19460.
Google Scholar
Rädecker N, Pogoreutz C, Ziegler M, Ashok A, Barreto MM, Chaidez V, et al. Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa. Ecol Evol. 2017;7:6614–21.
Google Scholar
Ainsworth TD, Fine M, Blackall LL, Hoegh-Guldberg O. Fluorescence in situ hybridization and spectral imaging of coral-associated bacterial communities. Appl Environ Microbiol. 2006;72:3016–20.
Google Scholar
van de Water JAJM, Ainsworth TD, Leggat W, Bourne DG, Willis BL, van Oppen MJH. The coral immune response facilitates protection against microbes during tissue regeneration. Mol Ecol. 2015;24:3390–404.
Google Scholar
Wada N, Ishimochi M, Matsui T, Pollock FJ, Tang S-L, Ainsworth TD, et al. Characterization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. Sci Rep. 2019;9:14662.
Google Scholar
Udvardi M, Poole PS. Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol. 2013;64:781–805.
Google Scholar
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.
Google Scholar
Shashar N, Cohen Y, Loya Y, Sar N. Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions. Mar Ecol Prog Ser. 1994;111:259–64.
Google Scholar
Inomura K, Bragg J, Riemann L, Follows MJ. A quantitative model of nitrogen fixation in the presence of ammonium. PLoS ONE. 2018;13:e0208282.
Google Scholar
Agawin NSR, Rabouille S, Veldhuis MJW, Servatius L, Hol S, van Overzee HMJ, et al. Competition and facilitation between unicellular nitrogen-fixing cyanobacteria and non-nitrogen-fixing phytoplankton species. Limnol Oceanogr. 2007;52:2233–48.
Google Scholar
El-Khaled YC, Roth F, Tilstra A, Rädecker N, Karcher DB, Kürten B, et al. In situ eutrophication stimulates dinitrogen fixation, denitrification, and productivity in Red Sea coral reefs. Mar Ecol Prog Ser. 2020;645:55–66.
Google Scholar
Fine M, Loya Y. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc B. 2002;269:1205–10.
Google Scholar
Sangsawang L, Casareto BE, Ohba H, Vu HM, Meekaew A, Suzuki T, et al. 13C and 15N assimilation and organic matter translocation by the endolithic community in the massive coral Porites lutea. R Soc Open Sci. 2017;4:171201.
Google Scholar
Fine M, Roff G, Ainsworth TD, Hoegh-Guldberg O. Phototrophic microendoliths bloom during coral “white syndrome. Coral Reefs. 2006;25:577–81.
Fine M, Steindler L, Loya Y. Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Freshw Res. 2004;55:115–21.
Google Scholar
Meunier V, Bonnet S, Benavides M, Ravache A, Grosso O, Lambert C, et al. Diazotroph-derived nitrogen assimilation strategies differ by scleractinian coral species. Front Mar Sci. 2021;8:1018.
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