Skip to main content
SpringerLink
Log in

A new purple sulfur bacterium isolated from a littoral microbial mat, Thiorhodococcus drewsii sp. nov.

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

A new strain of purple sulfur bacterium was isolated from a marine microbial mat sampled in Great Sippewissett Salt Marsh at the Atlantic coast (Woods Hole, Mass., USA). Single cells of strain AZ1 were coccus-shaped, highly motile by means of a single flagellum, and did not contain gas vesicles. Intracellular membranes were of the vesicular type. However, additional concentric membrane structures were present. The photosynthetic pigments were bacteriochlorophyll a and carotenoids of the normal spirilloxanthin series, with rhodopin as the dominant carotenoid. Hydrogen sulfide (up to 11 mM), sulfur, thiosulfate, and molecular hydrogen were used as electron donors during anaerobic phototrophic growth. During growth on sulfide, elemental sulfur globules were transiently stored inside the cells. Strain AZ1 is much more versatile than most other Chromatiaceae with respect to electron donor and organic substrates. In the presence of CO2, it is capable of assimilating C1–C5 fatty acids, alcohols, and intermediates of the tricarboxylic acid cycle. Strain AZ1 could also grow photoorganotrophically with acetate as the sole photosynthetic electron donor. Chemotrophic growth in the dark under microoxic conditions was not detected. Optimum growth occurred at pH 6.5–6.7, 30–35 °C, ≥50 µmol quanta m−2 s−1, and 2.4–2.6% NaCl. The DNA base composition was 64.5 mol% G+C. Comparative sequence analysis of the 16S rRNA gene confirmed that the isolate is a member of the family Chromatiaceae. Sequence similarity to the most closely related species, Thiorhodococcus minor DSMZ 11518T, was 97.8%; however, the value for DNA-DNA hybridization between both strains was only 20%. Because of the low genetic similarity and since strain AZ1 physiologically differs considerably from all other members of the Chromatiaceae, including Trc. minor, the new isolate is described as a new species of the genus Thiorhodococcus, Thiorhodococcus drewsii sp. nov.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–C.
Fig. 2A–C.
Fig. 3.
Fig. 4.

Similar content being viewed by others

Abbreviations

Ach. :

Allochromatium

Amb. :

Amoebobacter

BChl :

Bacteriochlorophyll

Lpc. :

Lamprocystis

PDA :

Photodiode array

Tba. :

Thiobaca

Tca. :

Thiocapsa

Tcs. :

Thiocystis

Trc. :

Thiorhodococcus

References

  • Albert DB, Martens CS (1997) Determination of low-molecular-weight organic acid concentrations in seawater and pore-water samples via HPLC. Mar Chem 56:27–37

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402

    Google Scholar 

  • Baas Becking LGM (1925) Studies on the sulphur bacteria. Ann Bot 39:613–650

    Google Scholar 

  • Bauld J, Chambers LA (1983) Carbon flow in microbial mats. Aust Microbiol 4:92

    Google Scholar 

  • Bryantseva I, Gorlenko VM, Kompantseva EI, Imhoff JF, Süling J, Mityushina L (1999) Thiorhodospira sibirica gen. nov., sp. nov. a new alkaliphilic purple sulfur bacterium from a Siberian soda lake. Int J Syst Bacteriol 49:697–703

    Google Scholar 

  • Cashion P, Hodler-Franklin MA, McCully J, Franklin M (1977) A rapid method for base ratio determination of bacterial DNA. Anal Biochem 81:461–466

    CAS  PubMed  Google Scholar 

  • Caumette P, Matheron R, Raymond N, Relexans J-C (1994) Microbial mats in the hypersaline ponds of Mediterranean salterns (Salins-de-Giraud, France). FEMS Microbiol Ecol 13:273–286

    Article  CAS  Google Scholar 

  • De Ley J, Cattoir H, Reynaerts A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142

    PubMed  Google Scholar 

  • De Wit R, Jonkers HM, van den Ende FP, van Gemerden H (1989) In situ fluctuations of oxygen and sulfide in marine microbial sediment ecosystems. Neth J Sea Res 23:271–281

    Google Scholar 

  • Dilling W, Liesack W, Pfennig N (1995) Rhabdochromatium marinum gen. nom. rev., sp. nov., a purple sulfur bacterium form a salt marsh microbial mat. Arch Microbiol 164:125–131

    Article  CAS  Google Scholar 

  • Eichler B, Pfennig N (1986) Characterization of a new platelet-forming purple sulfur bacterium, Amoebobacter pedioformis sp. nov. Arch Microbiol 146:295–300

    CAS  Google Scholar 

  • Eichler B, Pfennig N (1988) A new purple sulfur bacterium from stratified freshwater lakes, Amoebobacter purpureus sp. nov. Arch Microbiol 149:395–400

    CAS  Google Scholar 

  • Eichler B, Pfennig N (1991) Isolation and characteristics of Thiopedia rosea. Arch Microbiol 155:210–216

    CAS  Google Scholar 

  • Escara JF, Hutton JR (1980) Thermal stability and renaturation of DNA in dimethoxysulphoxide solutions: acceleration of renaturation rate. Biopolymeres 19:1315–1327

    CAS  Google Scholar 

  • Fox GE, Wisotzkey JD, Jurtshuk P (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170

    CAS  PubMed  Google Scholar 

  • Garcia AF, Venturoli G, Gad'on N, Fernandez-Velasco JG, Melandri BA, Drews G (1987) The adaption of the electron transfer chain of Rps. capsulata to different light intensities. Biochem Biophys Acta 890:335–345

    CAS  Google Scholar 

  • Giblin AE, Howarth RW (1984) Porewater evidence for a dynamic sedimentary iron cycle in salt marshes. Limnol Oceanogr 29:47–63

    CAS  Google Scholar 

  • Glaeser J, Overmann J (1999) Selective enrichment and characterization of Roseospirillum parvum, gen. nov. and sp. nov., a new purple nonsulfur bacterium with unusual light absorption properties. Arch Microbiol 171:405–16

    CAS  PubMed  Google Scholar 

  • Golecki JR (1988a) Analysis of structure and development of bacterial membranes (outer cytoplasmic, and intracytoplasmic membranes). Methods Microbiol 20:61–77

    Google Scholar 

  • Golecki JR (1988b) Electron microscopy of isolated microbial membranes. Methods Microbiol 20:261–282

    Google Scholar 

  • Gorlenko VM, Krasil´nikova EN, Kikina OG, Tatarinova NY (1979) The new motile purple sulfur bacterium Lamprobacter modestohalophilus nov. gen., nov. sp. with gas vacuoles. Izv. Akad. Nauk. S.S.S.R. Ser. Biol. 5, 755–767 (in Russian)

  • Guyoneaud R, Matheron R, Liesack W, Imhoff JF, Caumette P (1997) Thiorhodococcus minus, gen. nov., sp. nov., a new purple sulfur bacterium isolated from coastal lagoon sediments. Arch Microbiol 168:16–23

    Article  CAS  PubMed  Google Scholar 

  • Harwood C, Buchhardt G, Herrmann H, Fuchs G (1999) Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microb Rev 22:439–458

    Article  Google Scholar 

  • Huss VAR, Festl H, Schleifer KH (1983) Studies on the spectrometric determination of DNA hybridisation from renaturation rates. J Syst Appl Microbiol 4:184–192

    CAS  Google Scholar 

  • Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–54

    CAS  PubMed  Google Scholar 

  • Jahnke K-D (1992) Basic computer program for evaluation of spectroscopic DNA renaturation data from GILFORD System 2600 spectrometer on a PC/XT/AT type personal computer. J Microbiol Methods 15:61–73

    Article  Google Scholar 

  • Jørgensen BB (1982) Ecology of the bacteria of the sulphur cycle with special reference to the anoxic-oxic interface. Phil Trans R Soc London 298:543–561

    Google Scholar 

  • Ludwig W, Strunk O, Klugbauer N, Weizenegger M, Neumann J, Bachleitner M, Schleifer KH (1998) Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19:554–568

    PubMed  Google Scholar 

  • Maidak BL, Cole JR, Parker CT Jr, Garrity GM, Larsen N Li B, Lilburn TG, McCaughey MJ, Olsen GJ, Overbeek R, Pramanik S, Schmidt TM, Tiedje JM, Woese CR (1999) A new version of the RDP (Ribosomal Database Projekt). Nucl Acids Res 27:171–173.

    Article  CAS  Google Scholar 

  • Mesbah M, Premachandran U, Whitman W (1989) Precise measurement of G+C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bact 39:159–167

    CAS  Google Scholar 

  • Nicholson JAM, Stolz JF, Pierson BK (1987) Structure of a microbial mat at Great Sippewissett March, Cape Cod, Massachusetts. FEMS Microbiol Ecol 45:343–364.

    Article  Google Scholar 

  • Odum EP (1973) Fundamentals of ecology, 3rd edn. Saunders, Philadelphia

  • Overmann J (1997) Mahoney Lake: a case study of the ecological significance of phototrophic sulfur bacteria. Adv Microbial Ecol 15:251–288

    CAS  Google Scholar 

  • Overmann J, Pfennig N (1989) Pelodictyon phaeoclathratiforme sp. nov., a new brown-colored member of the Chlorobiaceae forming net-like colonies. Arch Microbiol 152:401–406

    CAS  Google Scholar 

  • Overmann J, Fischer U, Pfennig N (1992) A new purple sulfur bacterium from saline littoral sediments Thiorhodovibrio winogradskyi gen. nov. and sp. nov. Arch Microbiol 157:329–335

    CAS  Google Scholar 

  • Overmann J, Beatty JT, Krouse HR, Hall KJ (1996) The sulfur cycle in the chemocline of a meromictic salt lake. Limnol Oceanogr 41:147–156

    CAS  Google Scholar 

  • Parkes RJ, Gibson GR, Mueller-Harvey I, Buckingham WJ, Herbert RA (1989) Determination of the substrates for sulphate-reducing bacteria within marine and estuarine sediments with different rates of sulphate reduction. J Gen Microbiol 135:175–187

    CAS  Google Scholar 

  • Peterson BJ, Howarth RW, Lipschultz F, Ashendorf D (1980) Salt marsh detritus: an alternative interpretation of stable carbon isotope ratios and the fate of Spartina alterniflora. Oikos 34:173–177

    CAS  Google Scholar 

  • Pfennig N (1978) Rhodocyclus purpureus gen.nov. and sp. nov., a ring shaped, vitamin B12-requiring member of the family Rhodospirillaceae. Int J Syst Bacteriol 28:283–288.

    CAS  Google Scholar 

  • Pfennig N (1989) Metabolic diversity among the dissimilatory sulfate-reducing bacteria. Albert Jan Kluyver memorial lecture. Antonie Van Leeuwenhoek 56:127–38

    CAS  PubMed  Google Scholar 

  • Pfennig N, Wagener S (1986) An improved method of preparing wet mounts for the photomicrography of microorganisms. J Microbial Methods 4:303–306

    Article  Google Scholar 

  • Pfennig N, Trüper HG (1989) Anoxygenic phototrophic bacteria. In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds), Bergey´s Manual of Systematic Bacteriology, Vol 3, Williams and Wilkins, Baltimore. pp 1635–1709

  • Pfennig N, Trüper HG (1992) The family Chromatiaceae. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, Berlin Heidelberg New York, pp 3200–3221

  • Pfennig N, Markham MC, Liaaen-Jensen S (1968) Carotenoids of Thiorhodaceae. 8. Isolation and characterization of a Thiothece, Lamprocystis and Thiodictyon strain and their carotenoid pigments. Arch Microbiol 62:178–191

    CAS  Google Scholar 

  • Pfennig N, Lunsdorf H, Suling J, Imhoff JF (1997) Rhodospira trueperi gen. nov., spec. nov., a new phototrophic Proteobacterium of the alpha group. Arch Microbiol 168:39–45

    CAS  PubMed  Google Scholar 

  • Pierson BK, Sands VM, Frederick JL (1990) Spectral irradiance and distribution of pigments in a highly layered marine microbial mat. Appl Environ Microbiol 56:2327–2340

    CAS  Google Scholar 

  • Puchkova NN, Imhoff JF, Gorlenko VM (2000) Thiocapsa litoralis sp. nov., a new purple sulfur bacterium from microbial mats from the White Sea. Int J Syst Evol Microbiol 50:1441–1447

    Google Scholar 

  • Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092

    CAS  PubMed  Google Scholar 

  • Rees, GN, Harfoot CG, Janssen PH, Schoenborn L, Kuever J, Lünsdorf H (2002) Thiobaca trueperi gen. nov., sp. nov., a phototrophic purple sulfur bacterium isolated from freshwater lake sediment. Int J Syst Evol Microbiol 52:671–678

    CAS  PubMed  Google Scholar 

  • Sørensen J, Christensen D, Jørgensen BB (1981) Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl Environ Microbiol 42:5–11

    Google Scholar 

  • Stackebrandt 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

    CAS  Google Scholar 

  • Thiele HH (1968) Die Verwertung einfacher organischer Substrate durch Thiorhodaceae. Arch Microbiol 60:124–138

    CAS  Google Scholar 

  • Van Gemerden H, Tughan CS, de Wit R, Herbert RA (1989) Laminated microbial ecosystems on sheltered beaches in Scapa Flow, Orkney Islands. FEMS Microbiol Ecol 62:87–102

    Google Scholar 

  • Widdel F, Kohring GW, Mayer F (1983) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov. Arch Microbiol 134:286–294

    CAS  Google Scholar 

  • Zuber H, Cogdell RJ (1995) Structure and organization of purple bacterial antenna complexes. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 315–348

  • Züllig H (1985) Pigmente phototropher Bakterien in Seesedimenten und ihre Bedeutung für die Seenforschung. Schweiz Z Hydrol 47, 87–126

Download references

Acknowledgements

This research was supported by the Deutsche Forschungsgemeinschaft and the Fonds der Chemischen Industrie. Thanks are due to Caroline Harwood, University of Iowa, and Alfred Spormann, Stanford University, for their help and stimulating discussions during the Microbial Diversity Course (2000) at Woods Hole, and to Manuel Kraft and Marius Banholzer for their help with the growth experiments. Karin Schubert and Jens Glaeser helped with HPLC determinations of bacterial pigments.

Author information

Authors and Affiliations

  1. Mikrobiologie, Institut für Biologie II, Universtität Freiburg, Schänzlestrasse 1, 79104 , Freiburg, Germany

    Annette Zaar, Georg Fuchs & Jochen R. Golecki

  2. Bereich Mikrobiologie, Ludwig-Maximilians-Universität München, Maria-Ward Strasse 1a, 80638 , Munich, Germany

    Jörg Overmann

Authors
  1. Annette Zaar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Georg Fuchs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jochen R. Golecki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jörg Overmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Annette Zaar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zaar, A., Fuchs, G., Golecki, J.R. et al. A new purple sulfur bacterium isolated from a littoral microbial mat, Thiorhodococcus drewsii sp. nov.. Arch Microbiol 179, 174–183 (2003). https://doi.org/10.1007/s00203-002-0514-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-002-0514-3

Keywords

Search

Navigation