Skip to main content

New insights on old bacteria: diversity and function of morphologically conspicuous sulfur bacteria in aquatic systems

  • Chapter
  • 350 Accesses

Part of the book series: Developments in Hydrobiology ((DIHY,volume 138))

Abstract

Colourless sulfur bacteria were among the first groups of biogeochemically important bacteria to be studied by microbial ecologists. This was in part due to the fact that several species are large and often produce macroscopically visible structures such as mats. Although some of these sulfur bacteria have been studied for over a century, few have been obtained in axenic culture and thus, until recently, relatively little was known regarding their relationship to other bacteria or their role in the environment. The introduction of molecular biological methods to microbial ecology has allowed many of these distinctive uncultured bacteria to be characterized phylogenetically and in situ measurements have revealed aspects of their behaviour and their involvement in specific biogeochemical processes. Culture based studies of some morphologically distinctive sulfur bacteria, principally isolates of different Beggia- toa species, have revealed that they exhibit a wide range of metabolic activities that span heterotrophy to obligate chemolithautotrophy. This knowledge has informed studies of uncultured sulfur bacteria such as Thioploca and Achromatium. The combination of molecular biological analyses, chemical and process measurements, and culture based studies that have allowed the ecology of these bacteria to be interrogated are discussed.

Author for correspondence.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ahmad, A. D. & C. Nelson, 1998. A newly isolated strain of freshwater Beggiatoa sp. (AA5A) exhibits a mixotrophic mode of nutrition. Abstracts of the Eight International Symposium on Microbial Ecology, Halifax, Nova Scotia. August 9-14, 86pp.

    Google Scholar 

  • Amann, R., J. Snaidr, M. Wagner, W. Ludwig & K-H. Schleifer, 1996. In situ visualization of high genetic diversity in a natural microbial community. J. Bact. 178: 3496–3500.

    PubMed  CAS  Google Scholar 

  • Andreasen, K. & P. H. Nielsen, 1997. Application of microauto-radiography to the study of substrate uptake by filamentous microorganisms in activated sludge. Appl. envir. Microbiol. 63: 3662–3668.

    CAS  Google Scholar 

  • Babenzien, H-D., 1991. Achromatium oxaliferum and its ecological niche. Zentralbl. Mikrobiol. 146: 41–49.

    Google Scholar 

  • Bond, P. L., P. Hugenholtz, J. Keller & L. L. Blackall, 1995. Bacterial community structure of phosphate-removing and non-phosphate-removing activated sludges from sequencing batch reactors. Appl. envir. Microbiol. 61: 1910–1916.

    CAS  Google Scholar 

  • Canfield, D. E. & A. Teske, 1996. Late proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulfur-isotope studies. Nature 382: 127–132.

    Article  PubMed  CAS  Google Scholar 

  • De Boer, W. E., J. W. M. La Rivière & K. Schmidt, 1971. Some properties of Achromatium oxaliferum. Antonie van Leeuwen-hoek 37: 533–563.

    Google Scholar 

  • Field, K. G., D. Gordon, T. Wright, M. Rappé, E. Urbach, K. Ver-gin & S. J. Giovannoni, 1997. Diversity and depth distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl. envir. Microbiol. 63: 63–70.

    CAS  Google Scholar 

  • Fossing, H., V. A. Gallardo, B. B. JØrgensen, M. Hüttel, L. P. Nielsen, H. Schultz, D. E. Canfield, S. Forster, R. N. Glud, J. K. Gunderson, J. Kiiver, N. B. Ramsing, A. Teske, B. Tham-drup & O. Ulloa, 1995. Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374: 713–714.

    Article  CAS  Google Scholar 

  • Gallardo, V. A., 1977. Large benthic microbial communities in sulphide biota under Peru-Chile subsurface counter-current. Nature 268: 331–332

    Article  Google Scholar 

  • Gray, N. D., R. W. Pickup, J. G. Jones & I. M. Head, 1997. Ecophysiological evidence that Achromatium oxaliferum is responsible for the oxidation of reduced sulfur species to sulfate in a freshwater sediment, Appl. envir. Microbiol. 63: 1905–1910.

    CAS  Google Scholar 

  • Giovannoni, S. J., T. B. Britschgi, C. L. Moyer & K. G. Field, 1990. Genetic diversity in Sargasso sea bacterioplankton. Nature 345: 60–63.

    Article  PubMed  CAS  Google Scholar 

  • Giide, H., W. R. Strohl & J. M. Larkin, 1981. Mixotrophic and heterotrophic growth of Beggiatoa alba in continuous culture. Arch. Microbiol. 129: 357–360.

    Article  Google Scholar 

  • Hagen, K. D. & D. C. Nelson, 1996. Organic carbon utilisation by obligate and facultative autotrophic Beggiatoa strains in homogeneous and gradient cultures. Appl. envir. Microbiol. 62: 947–953.

    CAS  Google Scholar 

  • Hagen, K. D. & D. C. Nelson, 1997. Use of reduced sulfur species by Beggiatoa spp.: enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl. envir. Microbiol. 63: 3957–3964.

    CAS  Google Scholar 

  • Head, I. M., N. D. Gray, R. W. Pickup & J. G. Jones, 1995. The biogeochemical role of Achromatium oxaliferum. In Grimait J. O. & C. Dorronsoro (eds), Organic Geochemistry: Developments and Applications to Energy, Climate, Environment and Human History. Selected papers from the 17th International Meeting on Organic Geochemistry, 4th-8th September 1995. Donostia-San Sebastián. The Basque Country Spain. AIGOA, Donostia-San Sebastián: 895–898.

    Google Scholar 

  • Head, I. M., N. D. Gray, K. J. Clarke, R. W. Pickup & J. G. Jones, 1996. The phylogenetic position and ultrastructure of the uncultured bacterium Achromatium oxaliferum. Microbiology 142: 2341–2354.

    Article  PubMed  CAS  Google Scholar 

  • Howarth, R., 1995. An investigation into the biogeochemistry of Achromatium oxaliferum. M.Sc. Thesis, University of Newcastle.

    Google Scholar 

  • Huettel, M., S. Forster, S. Klöser & H. Fossing, 1996. Vertical migration in sediment-dwelling sulfur bacteria Thioploca spp. in overcoming diffusion limitations. Appl. envir. Microbiol. 62: 1863–1872.

    CAS  Google Scholar 

  • Jorgensen, B. B., 1983. The Microbial Sulfur Cycle. In Krumbien W. E. (ed.), Microbial Geochemistry. Blackwell Scientific, Oxford: 91–124.

    Google Scholar 

  • Jorgensen, B. B., & N. P. Revsbech, 1983. Colourless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in O2and H2S micro-gradients. Appl. envir. Microbiol. 45: 1261–1270.

    CAS  Google Scholar 

  • Kuenen, J. G. & R. F. Beudecker, 1982. Microbiology of thioba-cilli and other sulfur oxidising autotrophs, mixotrophs and heterotrophs. Phil. trans. R. Soc, Lond. B 298: 473–497.

    Article  CAS  Google Scholar 

  • Lane, D. J., A. P. Harrison Jr., D. Stahl, B. Pace, S. J. Giovannoni, G. J. Olsen & N. R. Pace, 1992. Evolutionary relationships amoung sulfur-and iron-oxidizing eubacteria. J. Bacteriol. 174: 269–278.

    PubMed  CAS  Google Scholar 

  • Larkin, J. M. & W. R. Strohl, 1983. Beggiatoa, Thiothrix, and Thioploca. Annu. Rev. Microbiol. 37: 341–367.

    Article  PubMed  CAS  Google Scholar 

  • La Rivière, J. W. M. & K. Schmidt, 1989. The Genus Achromatium. In Staley J. T., M. P. Bryant, N. Pfennig & J. G. Holt (eds), Bergey’s Manual of Systematic Bacteriology, Williams & Wilkins, Baltimore 3: 2131–2133.

    Google Scholar 

  • La Rivière, J. W. M. & K. Schmidt, 1992. Morphologically conspicuous sulfur-oxidizing eubacteria. In Balows A., H. G. Triiper, M. Dworkin, W. Harder & K. H. Schleifer (eds), The Pro-karyotes, 2nd edn, Springer Verlag, New York: 3934–3947.

    Google Scholar 

  • Lauterborn, R., 1907. Eine neue Gattung der Schwefelbakterien (Thioploca schmidlei nov. gen. nov spec). Ber. Dtsch. Bot. Ges. 25: 238–242.

    Google Scholar 

  • Maier, S., 1984. Description of Thioploca ingrica sp. nov., nom. rev. Int. J. System. Bacteriol. 34: 344–355.

    Article  Google Scholar 

  • Maier, S., 1986. Diversity and ecology of the Thioploca group of aquatic bacteria. In Megusar F. & M. Gantar (eds), Perspectives in Microbial Ecology, Proceedings of the Fourth International Symposium on Microbial Ecology. Ljubljana 24-29 August 1986: 143–1

    Google Scholar 

  • Maier, S. & V. A Gallardo, 1984a. Description of Thioploca araucae sp. nov. and Thioploca chileae sp. nov.. Int. J. system. Bacteriol. 34: 414–418.

    Article  Google Scholar 

  • Maier, S. & V. A Gallardo, 1984b. Nutritional characteristics of two marine thioplocas determined by autoradiography. Arch. Microbiol. 139:218–220.

    Article  CAS  Google Scholar 

  • McHatton, S. C., J. P. Barry, H. W. Jannasch & D. C. Nelson, 1996. High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl. envir. Microbiol. 62: 954–958

    CAS  Google Scholar 

  • Møller, M. M., L. P. Nielsen & B. B. Jørgensen, 1985. Oxygen responses and mat formation by Beggiatoa spp. Appl. envir. Microbiol. 50: 373–382.

    Google Scholar 

  • Moore, L. R., G. Rocap & S. W. Chisholm, 1998. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.

    Article  PubMed  CAS  Google Scholar 

  • Muyzer, G., A. Teske, C. O. Wirsen & H. Jannasch, 1995. Phylogenetic relationships of Thiomicrospira species and their identification in deep sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch. Microbiol. 164: 165–172.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, D. C., 1989. Physiology and biochemistry of filamentous sulfur bacteria. In Schlegel H. G. and B. Bowien (eds), Autotrophic Bacteria, Science Tech. Publishers; Madison, WI, U.S.A.

    Google Scholar 

  • Nelson, D. C., 1992. The genus Beggiatoa. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K-H. Schleifer (eds), The Prokaryotes, 2nd edn, Springer-Verlag, New York: 3171–3180.

    Google Scholar 

  • Nelson, D. C. & R. W. Castenholz, 1981a. The use of reduced sulfur compounds by Beggiatoa sp. J. Bact. 147: 140–154.

    PubMed  CAS  Google Scholar 

  • Nelson, D. C. & R. W. Castenholz, 1981b. Organic nutrition of Beggiatoa sp. J. Bact. 147: 236–247.

    PubMed  CAS  Google Scholar 

  • Nelson, D. C. & R. W. Castenholz, 1982. Light responses of Beggiatoa spp.. Arch. Microbiol. 131: 146–155.

    Article  Google Scholar 

  • Nelson, D. C. & H. W. Jannasch, 1983. Chemoautotrophic growth of a marine Beggiatoa in sulfide gradient cultures. Arch. Microbiol. 136:262–269.

    Article  CAS  Google Scholar 

  • Nelson, D. C., B. B. Jørgensen & N. P. Revsbech, 1986. Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl. envir. Microbiol. 52: 225–233.

    CAS  Google Scholar 

  • Nelson, D. C., C. A. Williams, B. A. Farah, & J. M. Shively, 1989a. Occurrence and regulation of Calvin cycle enzymes in non-autotrophic Beggiatoa strains. Arch. Microbiol. 151: 15–19.

    Article  CAS  Google Scholar 

  • Nelson, D. C., C. O. Wirsen & H. W. Jannasch, 1989b. Characterization of large, autotrophic Beggiatoa spp. abundant at hydro-thermal vents of the Guaymas Basin. Appl. envir. Microbiol. 55: 2909–2917.

    CAS  Google Scholar 

  • Nubel, U., B. Engelen, A. Felske, J. Snaidr, A. Wieshuber, A. Amann, W. Ludwig & H. Backhaus, 1996. Sequence heterogeneities of genes encoding 16S ribosomal-RNAs in Paenibacillus-polymyxa detected by temperature-gradient gel-electrophoresis. J. Bact. 178: 5636–5643.

    PubMed  CAS  Google Scholar 

  • Polz, M. F., D. L. Distel, B. Zarda, R. Amann, H. Feibeck, J. A. Ott & C. M. Cavanaugh, 1994. Phylogenetic analysis of an highly specific association between ecto-symbiotic, sulfur-oxidizing bacteria and a marine nematode. Appl. envir. Microbiol. 60: 4461–4467.

    CAS  Google Scholar 

  • Polz, M. F., E. V. Odintsova & C. M. Cavanaugh, 1996. Phylogenetic relationships of the filamentous sulfur bacterium Thiothrix ramosa based on 16S ribosomal RNA sequence analysis. Int. J. System. Bacteriol. 46: 94–97.

    Article  CAS  Google Scholar 

  • Pringsheim, E. G., 1967. Die mixotrophie von Beggiatoa. Arch. Mikrobiol. 59:247–254.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, L. A. & J. G. Kuenen. 1992. The colorless sulfur bacteria., In Balows A., edH. G. Triiper, M. Dworkin, W. Harder & K. H. Schleifer (eds), The Prokaryotes, 2nd edn. Springer-Verlag, New York. 385–413.

    Google Scholar 

  • Rosenberg, R., W. E. Arntz, E. Chumán des Flores, L. A. Flores, G. Carbajal, I. Finger & J. Tarazona, 1983. Benthos biomass and oxygen deficiency in the upwelling system of Peru. J. Mar. Res. 41: 263–279.

    Article  CAS  Google Scholar 

  • Schedel, M. & H. Triiper, 1980. Anaerobic oxidation of thiosulfate and elemental sulfur in Thiobacillus denitrificans. Arch. Microbiol. 124: 205–210.

    Article  CAS  Google Scholar 

  • Schewiakoff, W,. 1893. Über einen neuen bakterienähnlichen Organismus des Süßwassers. Heidelberg: Habilitationsschrift.

    Google Scholar 

  • Schmidt, T. M., B. Arieli, Y. Cohen, E. Padan & W. R. Strohl, 1987. Sulfur metabolism in Beggiatoa alba. J. Bact. 169: 5466–5472.

    PubMed  CAS  Google Scholar 

  • Schultz, H. N., B. B. Jørgensen, H. A. Fossing & N. B. Ramsing, 1996. Community structure of filamentous, sheath building sulfur bacteria, Thioploca spp. off the coast of Chile. Appl. envir. Microbiol. 62: 1855–1862.

    Google Scholar 

  • Strohl, W. R., 1989. Genus I. Beggiatoa. In Staley J.T., M. P. Bryant, N. Pfennig & J. G. Holt. (eds), Bergey’s Manual of Systematic Bacteriology, Williams & Wilkins, Baltimore, 3: 2091–2097.

    Google Scholar 

  • Strohl, W. R., G. C. Cannon, J. M. Shively, H. Güde, L. A. Hook, C. M. Lane & J. M. Larkin, 1981. Heterotrophic carbon metabolism by Beggiatoa alba. J. Bact. 148: 572–583.

    PubMed  CAS  Google Scholar 

  • Stumm, W. & J. J. Morgan, 1981. Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Waters, Wiley-interscience, New York

    Google Scholar 

  • Sweerts, J. P. R. A., D. De Beer, L. P. Nielsen, H. Verdouw, J. C. Van Den Heuvel, Y. Cohen & T. E. Cappenberg, 1990. Denitrification by sulfur oxidizing Beggiatoa spp. mats on freshwater sediments. Nature 344: 762–763.

    Article  CAS  Google Scholar 

  • Teske, A. P., N. B. Ramsing, J. Kiiver & H. Fossing, 1995. Phylo-geny of Thioploca and related filamentous sulfide-oxidizing bacteria. Syst. Appl. Microbiol. 18: 517–526.

    Article  Google Scholar 

  • Thamdrup, B. & D. E. Canfield, 1996. Pathways of carbon oxidation in continental margin sediments off central Chile. Limnol. Oceanogr. 41: 1629–1650.

    Article  PubMed  CAS  Google Scholar 

  • Timmer-TenHoor, A., 1975. A new type of thiosulfate oxidizing, nitrate reducing organism: Thiomicrospira denitrificans sp. nov. Neth. J. Sea Res. 9: 344–350.

    Article  CAS  Google Scholar 

  • Van de Peer, Y. & R. De Wachter, 1994. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput. Appl. Biosci. 10: 569–570.

    PubMed  Google Scholar 

  • Ward, D. M., M. M. Bateson, R. Weiler & A. L. Ruff-Roberts, 1992. Ribosomal RNA analysis of microorganisms as they occur in nature. Adv. Microb. Ecol. 12: 219–286.

    Article  CAS  Google Scholar 

  • Whiteley, A. S., A. G. O’Donnell, S. J. MacNaughton & M. R. Barer, 1996. Cytochemical colocalization and quantitation of phenotypic and genotypic characteristics in individual bacterial-cells. Appl. envir. Microbiol. 62: 1873–1879.

    CAS  Google Scholar 

  • Winogradsky, S., 1887. Über Schwefelbacterien. Bot. Zeitung. 45: 489–610.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

J. P. Zehr M. A. Voytek

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Gray, N.D., Head, I.M. (1999). New insights on old bacteria: diversity and function of morphologically conspicuous sulfur bacteria in aquatic systems. In: Zehr, J.P., Voytek, M.A. (eds) Molecular Ecology of Aquatic Communities. Developments in Hydrobiology, vol 138. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4201-4_8

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-4201-4_8

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-5827-8

  • Online ISBN: 978-94-011-4201-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics