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Dominance of green sulfur bacteria in the chemocline of the meromictic Lake Suigetsu, Japan, as revealed by dissimilatory sulfite reductase gene analysis

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Abstract

This study investigated the spatiotemporal abundance and diversity of the α-subunit of the dissimilatory sulfite reductase gene (dsrA) in the meromictic Lake Suigetsu for assessing the sulfur-oxidizing bacterial community. The density of dsrA in the chemocline reached up to 3.1 × 106 copies ml−1 in summer by means of quantitative real-time PCR and it was generally higher than deeper layers. Most of the dsrA clones sequenced were related to green sulfur bacteria such as Chlorobium phaeovibrioides, C. limicola, and C. luteolum. Below the chemocline of the lake, we also detected other dsrA clones related to the purple sulfur bacterium Halochromatium salexigens and some branching lineages of diverse sequences that were related to chemotrophic sulfur bacterial species such as Magnetospirillum gryphiswaldense, Candidatus Ruthia magnifica, and Candidatus Thiobios zoothamnicoli. The abundance and community compositions of sulfur-oxidizing bacteria changed depending on the water depth and season. This study indicated that the green sulfur bacteria dominated among sulfur-oxidizing bacterial population in the chemocline of Lake Suigetsu and that certain abiotic environmental variables were important factors that determined sulfur bacterial abundance and community structure.

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References

  • Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic Bacteria. Kluwer Academic Publishers, Netherlands, pp 847–870

    Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99:9509–9514

    Article  PubMed  CAS  Google Scholar 

  • Eisenlord SD, Zak DR (2010) Simulated atmosphere nitrogen deposition alters actinobacterial community composition in forest soil. Soil Biol Biochem 74:1157–1166

    CAS  Google Scholar 

  • Finlay BJ, Clarke KJ, Vicente E, Miracle MR (1991) Anaerobic ciliates from a sulphide-rich solution lake in Spain. Europ J Protistol 27:148–159

    Article  CAS  Google Scholar 

  • Galand PE, Bourrain M, De Maistre E, Catala P, Desdevises Y, Elifantz H, Kirchman DL, Lebaron P (2012) Phylogenetic and functional diversity of bacteria and archaea in a unique stratified lagoon, the clipperton atoll (N pacific). FEMS Microbiol Ecol 79:203–217

    Article  PubMed  CAS  Google Scholar 

  • Gregersen LH, Habicht KS, Peduzzi S, Tonolla M, Canfield DE, Miller M, Cox RP, Frigaard NU (2009) Dominance of a clonal green sulfur bacterial population in a stratified lake FEMS. Microbial Ecol 70:30–41

    Article  CAS  Google Scholar 

  • Gruber-Vodicka HR, Dirks U, Leisch N, Baranyi C, Stoecker K, Bulgheresi S, Heindl NR, Horn M, Lott C, Loy A, Wagner M, Ott J (2011) Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. Proc Natl Acad Sci USA 108:12078–12083

    Article  PubMed  CAS  Google Scholar 

  • Harada M, Yoshida T, Kuwahara H, Shimamura S, Takai Y, Kato C, Miwa T, Miyake H, Maruyama T (2009) Expression of genes for sulfur oxidation in the intracellular chemoautotrophic symbiont of the deep-sea bivalve Calyptogena okutanii. Extremophiles 13:895–903

    Article  PubMed  CAS  Google Scholar 

  • Hoeft SE, Blum JS, Stolz JF, Tabita FR, Witte B, King GM, Santini JM, Oremland RS (2007) Alkalilimnicola ehrlichii sp. nov., a novel, arsenite-oxidizing haloalkaliphilic gammaproteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Bacteriol 57:504–512

    CAS  Google Scholar 

  • Imhoff JF (1995) Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Netherlands, pp 1–15

    Google Scholar 

  • Imhoff JF (2006) The family Chromatiaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, New York, pp 846–873

    Google Scholar 

  • Koizumi Y, Kojima H, Fukui M (2004) Dominant microbial composition and its vertical distribution in saline meromictic lake Kaiike (Japan) as revealed by quantitative oligonucleotide probe membrane hybridization. Appl Environ Microbiol 70:4930–4940

    Article  PubMed  CAS  Google Scholar 

  • Kondo R, Kasashima N, Matsuda H, Hata Y (2000) Determination of thiosulfate in a meromictic lake. Fish Sci 66:1076–1081

    Article  CAS  Google Scholar 

  • Kondo R, Nakagawa A, Mochizuki L, Osawa K, Fujioka Y, Butani J (2009) Dominant bacterioplankton populations in the meromictic Lake Suigetsu as determined by denaturing gradient gel electrophoresis of 16S rRNA gene fragments. Limnology 10:63–69

    Article  CAS  Google Scholar 

  • Lindstrom ES, Tove SR, Wilson PW (1950) Nitrogen fixation by the green and purple sulfur bacteria. Science 112:197–198

    Article  PubMed  CAS  Google Scholar 

  • Loy A, Duller S, Baranyi C, Mumann M, Ott J, Sharon I, Beja O, Pasiler DL, Dahl C, Wagner M (2009) Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ Microbiol 11:289–299

    Article  PubMed  CAS  Google Scholar 

  • Ludwig W, Stunk O, Westram R, Richter L, Meier H, Yadhukumar H, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüßmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmass N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Lunina ON, Bryantseva IA, Akimov VN, Rusanov II, Rogozin DY, Barinova ES, Lysenko AM, Pimenov NV (2007) Seasonal changes in the structure of the anoxygenic photosynthetic bacterial community in Lake Shunet, Khakassia. Microbiology 76:368–379

    Article  CAS  Google Scholar 

  • Madigan MT (1988) Microbiology, physiology, and ecology of phototrophic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 39–111

    Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton

    Book  Google Scholar 

  • Manske AK, Glaeser J, Kuypers MM, Overmann J (2005) Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 meters in the Black Sea. Appl Environ Microbiol 71:8049–8060

    Article  PubMed  CAS  Google Scholar 

  • Massana R, Pedrós-Alió C (1994) Role of anaerobic ciliates in planktonic food webs: abundance, feeding, and impact on bacteria in the field. Appl Environ Microbiol 60(4):1325–1334

    PubMed  CAS  Google Scholar 

  • Matsuyama M, Saijo Y (1971) Studies on biological metabolism in a meromictic lake Suigetsu. J Oceanog Soc Jpn 27:197–206

    Article  Google Scholar 

  • Meyer B, Kuever J (2007) Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5′-phosphosulfate (APS) reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153:3478–3498

    Article  PubMed  CAS  Google Scholar 

  • Mori Y, Purdy KJ, Oakley BB, Kondo R (2010) Comprehensive detection of Phototrophic sulfur bacteria using PCR primers that target reverse dissimilatory sulfite reductase gene. Microbes Environ 25:190–196

    Article  PubMed  Google Scholar 

  • Mullins TD, Britschgi TB, Krest RL, Diovannoni ST (1995) Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol Oceanogr 40:148–158

    Article  CAS  Google Scholar 

  • Nagatani H, Shimizu M, Valentine RC (1971) The mechanism of ammonia assimilation in nitrogen fixing bacteria. Arch Microbiol 79:164–175

    CAS  Google Scholar 

  • Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM (2007) The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315:998–1000

    Article  PubMed  CAS  Google Scholar 

  • Ng C, DeMaere MZ, Williams TJ, Lauro FM, Raftery M, Gibson JA, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Thomas T, Cavicchiolo R (2010) Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica. ISME J 4:1002–1019

    Article  PubMed  CAS  Google Scholar 

  • Ohkouchi N, Nakajima Y, Okada H, Ogawa ON, Suga H, Oguri K, Kitazato H (2005) Biogeochemical processes in the saline meromictic Lake Kaiike, Japan: implications from molecular isotopic evidences of photosynthetic pigments. Environ Microbiol 7:1009–1016

    Article  PubMed  CAS  Google Scholar 

  • Okamura T, Mori Y, Nakano S, Kondo R (2012) Abundance and bacterivory of heterotrophic nanoflagellates in the meromictic Lake Suigetsu, Japan. Aquat Microb Ecol 66:149–158

    Article  Google Scholar 

  • Overmann J (2006) The family Chlorobiaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, New York, pp 359–380

    Google Scholar 

  • Parkin TB, Brock TD (1980) Photosynthetic bacterial production in lakes: the effects of light intensity. Limnol Oceanogr 25:711–718

    Article  Google Scholar 

  • Raymond JC, Sistrom WR (1969) Ectothiorhodospira halophila: a new species of the genus Ectothiorhodospira. Arch Mikrobiol 69:121–126

    Article  PubMed  CAS  Google Scholar 

  • Rinke C, Schmitz-Esser S, Stoecker K, Nussbaumer AD, Molnár DA, Vanura K, Wagner M, Horn M, Ott JA, Bright M (2006) “Candidatus Thiobios zoothamnicoli”, an Ectosymbiotic Bacterium covering the giant marine ciliate Zoothamnium niveum. Appl Environ Microbiol 72:2014–2021

    Article  PubMed  CAS  Google Scholar 

  • Singleton D, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376

    Article  PubMed  CAS  Google Scholar 

  • Sirevåg R (1995) Carbon metabolism in green bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria, Kluwer Academic Publishers, The Netherlands, pp 871–883

  • Takahashi M, Ichimura S (1968) Vertical distribution and organic matter production of photosynthetic sulfur bacteria in Japanese lakes. Limnol Oceanogr 13:644–655

    Article  Google Scholar 

  • Tonolla M, Peduzzi S, Hahn D, Peduzzi R (2003) Spatio-temporal distribution of phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno (Switzerland). FEMS Microbiol Ecol 43:89–98

    Article  PubMed  CAS  Google Scholar 

  • Tonolla M, Peduzzi R, Hahn D (2005) Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Appl Environ Microbiol 71:3544–3550

    Article  PubMed  CAS  Google Scholar 

  • Tourova PT, Spiridonova ME, Berg AI, Slobodova VN, Boulygina SE, Sorokin YD (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57:2387–2398

    Article  PubMed  CAS  Google Scholar 

  • Van Gemerden H, Mas J (1995) Ecology of phototrophic sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, The Netherlands, pp 49–85

    Google Scholar 

  • Van Gemerden H, De Wit R, Tughan CS, Herbert RA (1989) Development of mass blooms of Thiocapsa roseopersicina on sheltered beaches on the Orkney Islands. FEMS Microbial Ecol 62:111–118

    Google Scholar 

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Acknowledgments

We thank S. Yoshikawa and Y. Takao of Fukui Prefectural University, S. Nakano of Kyoto University, and K. Fujita of Ehime University for their assistance during field sampling. We also gratefully acknowledge useful comments by anonymous reviewers and the editor. This study was supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science and Fukui Prefectural Fund for the Promotion of Science to RK.

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Correspondence to Ryuji Kondo.

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Communicated by Theo Hansen.

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Mori, Y., Kataoka, T., Okamura, T. et al. Dominance of green sulfur bacteria in the chemocline of the meromictic Lake Suigetsu, Japan, as revealed by dissimilatory sulfite reductase gene analysis. Arch Microbiol 195, 303–312 (2013). https://doi.org/10.1007/s00203-013-0879-5

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