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Novel green sulfur bacteria phylotypes detected in saline environments: ecophysiological characters versus phylogenetic taxonomy

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Abstract

The taxonomic significance of salt tolerance or requirements in green sulfur bacteria has been analyzed with environmental populations and enrichment cultures from several saline systems (inland and coastal water bodies) with different salinities (salt composition and concentration). Novel phylotypes of green sulfur bacteria have been found in hypersaline and brackish environments and 16S rRNA gene sequence analysis affiliated them into phylogenetic groups in which neither halotolerant nor halophilic species have been known to date. Therefore, salt tolerance does not seem to be restricted to members of any specific subgroup but is widespread among all the different phylogenetic branches of the green sulfur bacteria group, and closely-related phylotypes can have dissimilar salt tolerance capacities. Thus the phenotypic characteristics and phylogenetic structure of the green sulfur bacteria present some incongruities. Phenotypic traits should be studied further in order to determine the ecophysiological features of green sulfur bacteria phylotypes.

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Fig. 1

Abbreviations

BChl:

Bacteriochlorophyll

Car:

Carotene

Cba.:

Chlorobaculum

Cbt:

Chlorobactene

Chl.:

Chlorobium

DGGE:

Denaturing gradient gel electrophoresis

GSB:

Green sulfur bacteria

Isr:

Isorenieratene

Ptc.:

Prosthecochloris

References

  • Achenbach LA, Carey J, Madigan MT (2001) Photosynthetic and phylogenetic primers for detection of anoxygenic phototrophs in natural environments. Appl Environ Microbiol 67:2922–2926

    Article  CAS  PubMed  Google Scholar 

  • Alexander B, Imhoff JF (2006) Communities of green sulfur bacteria in marine and saline habitats analyzed by gene sequences of 16S rRNA and Fenna–Matthews–Olson protein. Int Microbiol 9:259–266

    CAS  PubMed  Google Scholar 

  • Alexander B, Andersen JH, Cox RP, Imhoff JF (2002) Phylogeny of green sulfur bacteria on the basis of gene sequences of 16S rRNA and of the Fenna–Matthews–Olson protein. Arch Microbiol 178:131–140

    Article  CAS  PubMed  Google Scholar 

  • Anil Kumar P, Srinivas TNR, Sasikala C, Ramana CV, Süling J, Imhoff J (2009) Prosthecochloris indica sp. nov., a novel green sulfur bacterium from a marine aquaculture pond, Kakinada, India. J Gen Appl Microbiol 55:163–169

    Article  PubMed  Google Scholar 

  • Borrego C, Garcia-Gil LJ (1994) Separation of bacteriochlorophyll homologues from green photosynthetic sulfur bacteria by reversed-phase HPLC. Photosynth Res 41:157–163

    Article  CAS  Google Scholar 

  • Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM et al (2002) The comparative RNA web (CRW) site: and online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2 (Correction: BMC Bioinformatics 3:15)

    Article  PubMed  Google Scholar 

  • Caumette P (1993) Ecology and physiology of phototrophic bacteria and sulfate-reducing bacteria in marine salterns. Experientia 49:473–481

    Article  CAS  Google Scholar 

  • Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM et al (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443

    Article  CAS  PubMed  Google Scholar 

  • Coolen MJ, Overmann J (2007) 217000-year-old DNA sequences of green sulfur bacteria in Mediterranean sapropels and their implications for the reconstruction of the paleoenvironment. Environ Microbiol 9:238–249

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP, phylogeny inference package version 3.6. Cladistics 5:164–166

    Google Scholar 

  • Figueras JB, Garcia-Gil LJ, Abella CA (1997) Phylogeny of the genus Chlorobium based on 16S rRNA gene sequence. FEMS Microbiol Lett 152:31–36

    Article  CAS  PubMed  Google Scholar 

  • Figueras JB, Cox RP, Hojrup P, Permentier HP, Miller M (2002) Phylogeny of the PscB reaction center protein from green sulfur bacteria. Photosynth Res 71:155–164

    Article  CAS  PubMed  Google Scholar 

  • Fofonoff P, Millard RCJ (1983) Algorithms for computation of fundamental properties of seawater. Unesco Technical Papers in Marine Science 44:53

    Google Scholar 

  • Garcia-Gil LJ, Gich FB, Fuentes-Garcia X (2003) A comparative study of bchG from green photosynthetic bacteria. Arch Microbiol 179:108–115

    CAS  PubMed  Google Scholar 

  • Glaeser J, Overmann J (2004) Biogeography, evolution, and diversity of epibionts in phototrophic consortia. Appl Environ Microbiol 70:4821–4830

    Article  CAS  PubMed  Google Scholar 

  • Guerrero MC, Balsa J, Pascual M, Martínez B, Montes C (1991) Caracterización limnológica de la laguna Salada de Chiprana (Zaragoza, España) y sus comunidades de bacterias fototróficas. Limnetica 7:83–96

    Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  CAS  PubMed  Google Scholar 

  • Hugenholtzt P, Huber T (2003) Chimeric 16S rRNA gene sequences of diverse origin are accumulating in the public databases. Int J Syst Evol Microbiol 53:289–293

    Article  PubMed  CAS  Google Scholar 

  • Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–254

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF (2003) Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna–Matthews–Olson protein) gene sequences. Int J Syst Evol Microbiol 53:941–951

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen BB, Kuenen JG, Cohen Y (1979) Microbial transformation of sulfur compounds in a stratified lake (Solar Lake, Sinai). Limnol Oceanogr 24:799–822

    Article  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro H (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Kimura M (1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  PubMed  Google Scholar 

  • Mendez-Alvarez S, Ramirez-Moreno S, Gaju N (2001) Molecular taxonomy of the genus Chlorobium. Crit Rev Microbiol 27:9–24

    Article  CAS  PubMed  Google Scholar 

  • Montes C, Martino P (1987) Bases Científicas Para La Protección De Los Humedales En España. In: Real Academia de Ciencias Exactas FyN (ed) Las lagunas salinas españolas. Madrid, pp 95–146

  • Moore DD (1996) Purification and concentration of DNA from aqueous solutions. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocol in molecular biology. Wiley, New York

    Google Scholar 

  • Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  Google Scholar 

  • Overmann J (2000) The family Chlorobiaceae. In: Dworkin M (ed) The prokaryotes. An evolving electronic resource for the microbiological community, vol release 3.1. Springer, New York

    Google Scholar 

  • Overmann J (2001) Green sulfur bacteria. In: Garrity GM, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 601–623

    Google Scholar 

  • Overmann J, Tuschak C (1997) Phylogeny and molecular fingerprinting of green sulfur bacteria. Arch Microbiol 167:302–309

    Article  CAS  PubMed  Google Scholar 

  • Overmann J, Coolen MJL, Tuschak C (1999) Specific detection of different phylogenetic groups of chemocline bacteria based on PCR and denaturing gradient gel electrophoresis of 16S rRNA gene fragments. Arch Microbiol 172:83–96

    Article  CAS  PubMed  Google Scholar 

  • Pfennig N, Trüper HG (1989) Green bacteria. In: Stanley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 3. Williams & Wilkins, Baltimore, pp 1682–1707

    Google Scholar 

  • Pfennig N, Trüper HG (1992) Isolation of members of the families Chromatiaceae and Chlorobiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes: a handbook on the biology of bacteria: ecophysiology, isolation, identification, application. Springer,  New York

    Google Scholar 

  • Riera XG, Abella CA (1991) Limnological cycle of the coastal lagoon La Massona (Girona, NE Spain). Origin, dynamics and influence of the sporadic seawater infalls on the meromixis. Verh Internat Verein Limnol 24:1029–1031

    CAS  Google Scholar 

  • Siefert E, Pfennig N (1984) Convenient method to prepare neutral sulfide solution for cultivation of phototrophic sulfur bacteria. Arch Microbiol 139:100–101

    Article  CAS  Google Scholar 

  • Stakebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Trüper HG, Schlegel HG (1964) Sulphur metabolism in Thiorhodaceae I. Quantiative measurements on growing cells of Chromatium okenii. Antonie van Leeuwenhoek 30:225–238

    Article  Google Scholar 

  • Van Niel CB (1971) Techniques for the enrichment, isolation and maintenance of the photosynthetic bacteria. A: San Pietro (ed). Methods Enzimol 23:3–28

    Google Scholar 

  • Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438

    CAS  PubMed  Google Scholar 

  • Vila X, Guyoneaud R, Cristina XP, Figueras JB, Abella CA (2002) Green sulfur bacteria from hypersaline Chiprana Lake (Monegros, Spain): habitat description and phylogenetic relationship of isolated strains. Photosynth Res 71:165–172

    Article  CAS  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) SSU ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank our colleagues from the Laboratory of Molecular Microbiology of the University of Girona for helpful discussions of the results and further advice on data sequence analysis. X. Triadó-Margarit was the recipient of a doctoral scholarship (2001 FI 00702) from the Autonomous Government of Catalonia. We would like to thank the reviewers of the manuscript for their corrections and comments.

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Authors and Affiliations

  1. Laboratory of Microbiology, Institute of Aquatic Ecology, University of Girona, Campus Montilivi, 17071, Girona, Spain

    Xavier Triadó-Margarit, Xavier Vila & Charles A. Abella

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  1. Xavier Triadó-Margarit
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  2. Xavier Vila
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  3. Charles A. Abella
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Correspondence to Xavier Triadó-Margarit.

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Triadó-Margarit, X., Vila, X. & Abella, C.A. Novel green sulfur bacteria phylotypes detected in saline environments: ecophysiological characters versus phylogenetic taxonomy. Antonie van Leeuwenhoek 97, 419–431 (2010). https://doi.org/10.1007/s10482-010-9420-x

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