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Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats

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Abstract

We report the phylogenetic and physiological characterization of a mesophilic and halophilic member of the filamentous anoxygenic phototrophic (FAP) bacteria, provisionally named ‘Candidatus Chorothrix halophila’ gen. nov. sp. nov., that has been maintained in a highly enriched culture in our laboratory for over a decade. Phylogenetic analysis of small-subunit RNA-encoding sequences places ‘Candidatus Chlorothrix halophila’ in a clade that includes cultivated members of the genera Chloroflexus and Oscillochloris. Physiological studies demonstrated sulfide-dependent photosynthetic uptake of 14C-labeled bicarbonate. Enzymatic assays for the activity of propionyl-coenzyme A synthase indicated that ‘Candidatus Chlorothrix halophila’ does not use the 3-hydroxypropionate cycle of Chloroflexus aurantiacus OK-70-fl for autotrophic carbon assimilation. New concepts regarding the taxonomy and phylogeny of FAP bacteria have emerged from this work.

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Abbreviations

MCLO :

Marine Chloroflexus-like organism

FAP :

Filamentous anoxygenic phototroph

References

  • Alber BE, Fuchs G (2002) Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J Biol Chem 277:12137–12143

    Article  CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidman JG, Struhl K (1987) Current protocols in molecular biology. Wiley, New York

  • Beer M, Seviour EM, Kong Y, Cunningham MB, Blackall LL, Seviour RJ (2002) Phylogeny of the filamentous bacterium Eikelboom Type 1851, and design and applications of a 16S rRNA oligonucleotide probe for its fluorescence in situ identification in activated sludge. FEMS Microbiol Lett 207:179–183

    Article  CAS  PubMed  Google Scholar 

  • Boomer SM, Pierson BK, Austinhirst R, Castenholz RW (2000) Characterization of novel bacteriochlorophyll-a-containing red filaments from alkaline hot springs in Yellowstone National Park. Arch Microbiol 174:152–161

    Article  CAS  PubMed  Google Scholar 

  • Boomer SM, Lodge DP, Dutton BE, Pierson BK (2002) Molecular characterization of novel red green nonsulfur bacteria from five distinct hot spring communities in Yellowstone National Park. Appl Environ Microbiol 68:346–355

    Article  CAS  PubMed  Google Scholar 

  • Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Shang Z, Yu N, Gutell RR (2002) The Comparative RNA Web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BioMed Central Bioinformatics 3:15

    Article  PubMed  Google Scholar 

  • Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (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 

  • D’Amelio ED, Cohen Y, Des Marais DJ (1989) Comparative functional ultrastructure of two hypersaline submerged cyanobacterial mats: Guerrero Negro, Baja California Sur, Mexico, and Solar Lake Sinai, Egypt. In: Cohen Y, Rosenberg E (eds) Microbial mats: physiological ecology of benthic microbial communities. American Society of Microbiology, Washington, DC, pp 97–113

  • Des Marais DJ, D’Amelio ED, Farmer JD, Jorgensen BB, Palmisano AC, Pierson BK (1992) Case study of a modern microbial mat-building community: the submerged cyanobacterial mats Guerrero Negro, Baja California Sur, Mexico. In: Schopf JW, Klein C (eds) The proterozoic biosphere: a multidisciplinary study. Cambridge University Press, Cambridge, pp 324–333

  • Dubinina GA, Gorlenko VM (1975) New filamentous photosynthesizing green bacteria with gas vacuoles. Mikrobiologiya 44:511–517

    CAS  Google Scholar 

  • Felsenstein J (2002) PHYLIP (phylogeny inference package), version 3.6a, 3rd edn. Department of Genetics, University of Washington, Seattle, Washington

  • Garrity GM, Holt JG (2001) Phylum BVI. Chloroflexi phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin Heidelberg New York, pp 427–446

  • Garrity GM, Johnson KL, Bell JA, Searles DB (2002) Taxonomic outline of the procaryotes. Bergey’s manual of systematic bacteriology, 2nd edn. Release 3.0. DOI: 10.1007/bergeysoutline200210. Springer, Berlin Heidelberg New York

  • Gerhardt P, Murray GE, Costilow RN, Nester EW, Wood A, Krieg NR, Phillips GB (1981) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC

  • Gich F, Garcia-Gil J, Overmann J (2001) Previously unknown and phylogenetically diverse members of the green nonsulfur bacteria are indigenous to freshwater lakes. Arch Microbiol 177:1–10

    Article  CAS  PubMed  Google Scholar 

  • Hanada S, Pierson BK (2002) The Family Chloroflexaceae. In: Dworkin M (ed) The Prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. release 3.11, November 22, 2002, http://www.prokayotes.com. Springer, Berlin Heidelberg New York

  • Hanada S, Takaichi S, Matsuura K, Nakamura K (2002) Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int J Syst Bacteriol 52:187–193

    CAS  Google Scholar 

  • Herter S, Busch A, Fuchs G (2002) l-Malyl-coenzyme A lyase/β-methylmalyl-coenzyme A lyase from Chloroflexus aurantiacus, a bifunctional enzyme involved in autotrophic CO2 fixation. J Bacteriol 184:5999–6006

    Article  CAS  PubMed  Google Scholar 

  • Holt JG, Castenholz RW (2001) Genus I. Herpetosiphon. In: Garrity GM, Holt JG (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin Heidelberg New York, pp 445–446

  • Hugler M, Menendez C, Schagger H, Fuchs G (2002) Malonyl-coenzyme A reductase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J Bacteriol 184:2404–2410

    Article  Google Scholar 

  • Ivanovsky RN, Fal YI, Berg IA, Ugolkova NV, Krasilnikova EN, Keppen OI, Zakharchuc LM, Zyakun AM (1999) Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. Microbiology 145:1743–1748

    CAS  PubMed  Google Scholar 

  • Keppen OI, Tourova TP, Kuznetsov BB, Ivanovsky RN, Gorlenko VM (2000) Proposal of Oscillochloridaceae fam. nov. on the basis of a phylogenetic analysis of the filamentous anoxygenic phototrophic bacteria, and emended description of Oscillochloris and Oscillochloris trichoides in comparison with further new isolates. Int J Syst Bacteriol 50:1529–1537

    Google Scholar 

  • Kohno T, Sei K, Mori K (2002) Characterization of type 1851 organism isolated from activated sludge samples. Water Sci Technol 46:111–114

    CAS  Google Scholar 

  • Kuske CR, Banton KL, Adorada DL, Stark PC, Hill KK, Jackson PJ (1998) Small-scale DNA sample preparation method for field PCR detection of microbial cells and spores in soil. Appl Environ Microbiol 64:2463–2472.

    CAS  PubMed  Google Scholar 

  • Laguerre G, Allard M, Revoy F, Amarger N (1994) Rapid identification of Rhizobia by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Appl Environ Microbiol 60:56–63

    CAS  Google Scholar 

  • Lopez-Cortez A (1990) Microbial mats in tidal channels at San Carlos, Baja California Sur, Mexico. Geomicrobiol J 8:69--85

    Google Scholar 

  • Mack EE, Pierson BK (1988) Preliminary characterization of a temperate marine member of the Chloroflexaceae. In: Olson JM, Ormerod JG, Amexz J, Stackebrandt E, Trüper HG (eds) Green photosynthetic bacteria. Plenum, The Netherlands, pp 237–241

  • Murray RG, Stackebrandt E (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45:186–187

    CAS  PubMed  Google Scholar 

  • Nübel U, Bateson MM, Madigan MT, Kuhl M, Ward DM (2001) Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroflexus spp. Appl Environ Microbiol 67:4365–4371

    Article  PubMed  Google Scholar 

  • Nübel U, Bateson MM, Vandieken V, Wieland A, Kuhl M, Ward DM (2002) Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-related bacteria in hot spring microbial mats. Appl Environ Microbiol 68:4593–4603

    Article  PubMed  Google Scholar 

  • Pierson BK, Castenholz RW (1995) Taxonomy and physiology of filamentous anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, The Netherlands, pp 31–47

  • Pierson BK, Castenholz RW (2001) Filamentous anoxygenic phototrophic bacteria. In: Garrity GM, Holt JG (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin Heidelberg New York, pp 427–444

  • Pierson BK, Giovannoni SJ, Castenholz RW (1984) Physiological ecology of a gliding bacterium containing bacteriochlorophyll a. Appl Environ Microbiol 47:576–584

    CAS  Google Scholar 

  • Pierson BK, Giovannoni SJ, Stahl DA, Castenholz RW (1985) Heliothrix oregonensis, gen. nov., sp. nov, a phototrophic filamentours gliding bacterium containing bacteriochlorophyll a. Arch Microbiol 142:164–167

    CAS  PubMed  Google Scholar 

  • Pierson BK, Valdez D, Larsen M, Morgan E, Mack EE (1994) Chloroflexus-like organisms from marine and hypersaline environments: distribution and diversity. Photosynthesis Research 41:35–52

    CAS  Google Scholar 

  • Sambrook J, Russell DW, Sambrook J (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Stolz JF (1993) Distribution of phototrophic microbes in the flat laminated microbial mat at Laguna Figueroa, Baja California, Mexico. Biosystems 23:345–357

    Article  Google Scholar 

  • Strauss G, Fuchs G (1993) Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur J Biochem 215:633–643

    CAS  PubMed  Google Scholar 

  • Trüper HG (1976) Higher taxa of the phototrophic bacteria: Chloroflexaceae fam. nov., a family for the gliding, filamentous, phototrophic “green” bacteria. Int J Syst Bacteriol 26:74–75

    Google Scholar 

  • Ugolkova NV, Ivanovsky RN (2000) On the mechanism of autotrophic fixation of CO2 by Chloroflexus aurantiacus. Microbiology 69:139–142

    CAS  Google Scholar 

  • Venetskaya SL, Gerasimenko LM (1988) Electron-microscopic study of microorganisms in a halophilic cyanobacterial community. Mikrobiologiya 57:450–457

    Google Scholar 

  • Weller R, Bateson MM, Heimbuch BK, Kopczynski ED, Ward DM (1992) Uncultivated cyanobacteria, Chloroflexus-like inhabitants, and spirochete-like inhabitants of a hot spring microbial mat. Appl Environ Microbiol 58:3964–3969

    PubMed  Google Scholar 

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Acknowledgements

This work was supported by a NASA Astrobiology grant to Arizona State University with a sub-contract to BKP at the University of Puget Sound. We thank M.N. Parenteau, M. Lawrence, E. Morgan and E. Lilja for technical assistance; T.M. Schmidt for advice and use of laboratory equipment; and, the laboratory of N.R. Pace for preliminary work on phylogenetic identification.

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Authors and Affiliations

  1. Center for Microbial Ecology and Department of Microbiology and Molecular Genetics, Michigan State University, 540 Plant and Soil Sciences Bldg., East Lansing, Michigan , 48824–1325, USA

    Joel A. Klappenbach

  2. Department of Biology, University of Puget Sound, Tacoma, Washington , 98416, USA

    Beverly K. Pierson

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  1. Joel A. Klappenbach
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  2. Beverly K. Pierson
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Correspondence to Joel A. Klappenbach.

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Klappenbach, J.A., Pierson, B.K. Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats. Arch Microbiol 181, 17–25 (2004). https://doi.org/10.1007/s00203-003-0615-7

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  • DOI: https://doi.org/10.1007/s00203-003-0615-7

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