Abstract
Both bacteria and algal symbionts (genus Symbiodinium), the two major microbial partners in the coral holobiont, respond to fluctuations in the environment, according to current reports; however, little evidence yet indicates that both populations have any direct interaction with each other in seasonal fluctuation. In this study, we present field observations of a compositional change in bacteria and Symbiodinium in the coral Isopora palifera in three separate coral colonies following monthly sampling from February to November in 2008. Using massively parallel pyrosequencing, over 200 000 bacterial V6 sequences were classified to build the bacterial community profile; in addition, the relative composition and quantity of Symbiodinium clades C and D were determined by real-time PCR. The results showed that coral-associated bacterial and Symbiodinium communities were highly dynamic and dissimilar among the tagged coral colonies, suggesting that the effect of host specificity was insignificant. The coral-associated bacterial community was more diverse (Shannon index up to 6.71) than previous estimates in other corals and showed rapid seasonal changes. The population ratios between clade C and D groups of Symbiodinium varied in the tagged coral colonies through the different seasons; clade D dominated in most of the samples. Although significant association between bacteria and symbiont was not detected, this study presents a more detailed picture of changes in these two major microbial associates of the coral at the same time, using the latest molecular approaches.
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References
Abrego D, Ulstrup KE, Willis BL, van Oppen MJH . (2008). Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B 275: 2273–2282.
Acinas SG, Klepac-Ceraj V, Hunt DE, Pharino C, Ceraj I, Distel DL et al. (2004). Fine-scale phylogenetic architecture of a complex bacteria community. Nature 430: 551–554.
Amann RI, Ludwig W, Schleifer KH . (1995). Phylogenetic identification and in situ detection of individual cells without cultivation. Microbiol Rev 59: 143–169.
Andersson AF, Riemann L, Bertilsson S . (2010). Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4: 171–181.
Baker AC . (2001). Reef corals bleach to survive change. Nature 411: 765–766.
Baker AC . (2003). Flexibility and specificity in coral algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Evol Syst 34: 661–689.
Barriuso J, Marin S, Mellado RP . (2010). Effect of the herbicide glyphosate on glyphosate-tolerant maize rhizobacterial communities: a comparison with pre-emergency applied herbicide consisting of a combination of acetochlor and terbutylazine. Environ Microbiol 12: 1021–1030.
Berman-Frank I, Lundgern P, Falkowski P . (2003). Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154: 157–164.
Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, Nielsen R et al. (2007). The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE 2: e197.
Chen CA, Wang JT, Fang LS, Yang YW . (2005). Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295: 113–121.
Chen JS, Toth J, Kasap M . (2001). Nitrogen-fixation genes and nitrogenase activity in Clostridium acetobutylicum and Clostridium beijerinckii. J Ind Microbiol Biotechnol 27: 281–286.
de Hoon MJL, Imoto S, Nolan J, Miyano S . (2004). Open source clustering software. Bioinformatics 20: 1453–1454.
Díez B, Bauer K, Bergman B . (2007). Epilithic cyanobacterial communities of a marine tropical beach rock (Heron Island, Great Barrier Reef): diversity and diazotrophy. Appl Environ Microbiol 73: 3656–3668.
Feng P, Weagant S, Grant M . (2002). Enumeration of Escherichia coli and the coliform bacteria. In: Merker RI (ed.). Bacteriological Analytical Manual, 8th edn., revision A. U.S. Food and Drug Administration: College Park, MD.
Frade PR, Jongh FDE, Vermeulen F, Bleijswijk JV, Bak RPM . (2008). Variation in symbiont distribution between closely related coral species over large depth ranges. Mol Ecol 17: 691–703.
Garren M, Raymoundo L, Guest J, Harvell CD, Azam F . (2009). Resilience of coral associated bacterial communities exposed to fish farm effluent. PLoS ONE 4: e7391.
Goh F, Michelle AA, Leuko S, Kawaguchi T, Decho AW, Burns BP et al. (2009). Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. ISME J 3: 383–396.
Grover R . (2002). Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding light, and ammonium concentrations. Limnol Oceanogr 47: 782–790.
Grover R . (2003). Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48: 2266–2274.
Hong MJ, Yu YT, Chen ACL, Chiang PW, Tang SL . (2009). Influence of species specificity and other factors on bacteria associated with Stylophora pistillata in Taiwan. Appl Environ Microbiol 75: 7797–7806.
Huber JA, Welch DBM, Morrison HG, Huse SM, Neal PR, Butterfield DA et al. (2007). Microbial population structures in the deep marine biosphere. Science 318: 97–100.
Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML . (2008). Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS ONE 4: e1000255.
Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W . (2008). A community change in the algal endosymbionts of coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B 275: 1359–1365.
Kenkel NC, Orlóci L . (1986). Applying metric and nonmetric multidimensional scaling to ecological studies: some new results. Ecology 67: 919–928.
Klaus JS, Janse I, Heikoop JM, Sanford RA, Fouke BW . (2007). Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol 9: 1291–1305.
Kneip C, Lockhart P, Voß C, Maier U-G . (2007). Nitrogen fixation in eukaryotes: new models for symbiosis. BMC Evol Biol 7: 55.
Knowlton N, Rohwer F . (2003). Multispecies microbial mutualisms on coral reefs: the host as a holobiont. Am Nat 162: S51–S62.
Koren O, Rosenberg E . (2006). Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72: 5254–5259.
Lajeunesse TC, Bhagooli R, Hidaka M, de Vantier L, Done T, Schmidt GW et al. (2004). Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284: 147–161.
Lajeunesse TC, Bonilla HR, Warner ME, Willis M, Schmidt GW, Fitt WK . (2008). Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53: 719–727.
Lampert Y, Kelman D, Nitzan Y, Dubinsky Z, Behar A, Hill RT . (2008). Phylogenetic diversity of bacteria associated with the mucus of red sea corals. FEMS Microbiol Ecol 64: 187–198.
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG . (2004). Discovery of symbiotic nitrogen fixing cyanobacteria in coral. Science 305: 997–1000.
Little AF, van Oppen MJH, Willis B . (2004). Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492–1494.
Littman RA, Willis BL, Pfeffer C, Bourne DG . (2009). Diversity of coral associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef. FEMS Microbiol Ecol 68: 152–163.
Marhaver KL, Edwards RA, Rohwer F . (2008). Viral communities associated with healthy and bleaching corals. Environ Microbiol 10: 2277–2286.
Meeks JC . (1998). Symbiosis between nitrogen-fixing cyanobacteria and plants. BioScience 48: 266–276.
Meng PJ, Lee HJ, Wang JT, Chen CC, Lin HJ, Tew KS et al. (2008). A long-term survey on anthropogenic impacts to the water quality of coral reefs, southern Taiwan. Environ Pollut 156: 67–75.
Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ . (2009). The roles and interactions of symbionts, host, and environment in defining coral fitness. PLoS ONE 4: e6364.
Muscatine L, Porter JW . (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environment. Bioscience 27: 454–460.
Paoli GC, Tabita FR . (1998). Aerobic chemolithoautotrophic growth and RubisCO function in Rhodobacter capsulatus and a spontaneous gain of function mutant of Rhodobacter sphaeroides. Arch Microbial 170: 8–17.
Reimer JD, Ono S, Tsukahrara J, Takishita K, Maruyama T . (2007). Non-seasonal clade-specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan. Phycological Res 55: 58–65.
Reis AMM, Araújo Jr SD, Moura RL, Francini-Filho RB, Pappas Jr G, Coelho AMA et al. (2009). Bacterial diversity associated with the Brazilian endemic reef coral Mussismilia. J Appl Microbiol 106: 1378–1387.
Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E . (2006). The coral probiotic hypothesis. Environ Microbiol 8: 2068–2073.
Roesch LFW, Fulthorpe RR, Rive A, Casella G, Hadwin AKM, Kent AD et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283–290.
Rohwer F, Seguritan V, Azam F, Knowlton N . (2002). Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1–10.
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I . (2007). The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5: 355–362.
Rowen R . (2004). Thermal adaptation in reef coral symbionts. Nature 430: 742.
Sambrook J, Russell DW . (2001). Recovery of DNA from agarose and polyacrylamide gels: electroelution into dialysis bags. Molecular Cloning. CSHL Press: Cold Spring Harbor, NY. vol. 1, pp 5.23–5.25.
Schloss PD, Handelsman J . (2005). Introducing DOTUR, a computer program for defining operational taxonomic unit and estimating species richness. Appl Environ Microbiol 71: 1501–1506.
Seshadri R, Adrian L, Fouts DE, Eisen JA, Phillippy AM, Methe BA et al. (2005). Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes. Science 307: 105–108.
Shashar N, Cohen Y, Loya Y, Sar N . (1994). Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111: 259–264.
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR et al. (2006). Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci USA 103: 12115–12120.
Stat M, Morris E, Gates RD . (2008). Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105: 9256–9261.
Takahashi S, Whitney SM, Badger MR . (2009). Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci USA 106: 3237–3242.
Toller WW, Rowan R, Knowlton N . (2001). Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201: 348–359.
Wahlund TM, Madigan MT . (1993). Nitrogen-fixation by the thermophilic green sulfur bacterium chlorobium-tepidum. J Bacteriol 175: 474–478.
Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F . (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707–2719.
Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE . (2000). Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730.
Acknowledgements
We thank Garmin Hsu and the colleagues of Allen CL Chen for assistance with providing samples and seawater temperature data. This study was supported by thematic project funding of Academia Sinica, Taiwan, and by the Biodiversity Research Center, Academia Sinica, Taiwan.
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Chen, CP., Tseng, CH., Chen, C. et al. The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5, 728–740 (2011). https://doi.org/10.1038/ismej.2010.151
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DOI: https://doi.org/10.1038/ismej.2010.151
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