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Mutualistic growth of the sulfate-reducer Desulfovibrio vulgaris Hildenborough with different carbohydrates

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Abstract

Desulfovibrio vulgaris Hildenborough genome presents a phosphotransferase system putatively involved in the transport of carbohydrates. However, utilization of sugars by this sulfate-reducing bacterium has never been reported. Herein, we have observed proliferation of D. vulgaris Hildenborough with some carbohydrates, in mutualism with Stenotrophomonas maltophilia, a non-fermentative, gram-negative gammaproteobacterium, or Microbacterium, a gram-positive actinobacterium. These results suggest the importance of feedback interactions between different heterotrophic bacterial species including the alternative for D. vulgaris of exploiting additional organic resources and novel habitats. Thus, D. vulgaris strongly participates in the mineralization of carbohydrates both in complex natural and artificial systems.

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References

  1. Postgate, J.R. and Campbell, L.L., Classification of Desulfovibrio Species, the Nonsporulating Sulfate-Reducing Bacteria, Bacteriol. Rev., 1966, vol. 30, pp. 732–738.

    PubMed  CAS  Google Scholar 

  2. PanKhania, LP., Gow L.A., and Hamilton, W.A., The Effect of Hydrogen on the Growth of Desulfovibrio vulgaris (Hildenborough) on Lactate, J. Gen. Microbiol., 1986, vol. 132, pp. 3349–3356.

    CAS  Google Scholar 

  3. Voordouw, G., Carbon Monoxide Cycling by Desulfovibrio vulgaris Hildenborough, J. Bacteriol., 2002, vol. 184, pp. 5903–5911.

    Article  PubMed  CAS  Google Scholar 

  4. Tang, Y., Pingitore, F., Mukhopadhyay, A., Phan, R., Hazen, T.C., and Keasling, J.D., Pathway Confirmation and Flux Analysis of Central Metabolic Pathways in Desulfovibrio vulgaris Hildenborough Using Gas Chromatography-Mass Spectrometry and Fourier Transform-Ion Cyclotron Resonance Mass Spectrometry, J. Bacteriol., 2007, vol. 189, pp. 940–949.

    Article  PubMed  CAS  Google Scholar 

  5. Pfennig, N., Metabolic Diversity among the Dissimilatory Sulfate-Reducing Bacteria, Antonie van Leeuwenhoek, 1989, vol. 56, pp. 127–138.

    Article  PubMed  CAS  Google Scholar 

  6. Ollivier, B., Cord-Ruwisch, R., Hatchikian, E.C., and Garcia J.L., Characterization of Desulfovibrio fructosovorans, Arch. Microbiol., 1988, vol. 149, pp. 447–450.

    Article  CAS  Google Scholar 

  7. Nielsen J.T., Liesack, W., and Finster K., Desulfovibrio zosterae sp. nov., a New Sulfate-Reducer Isolated from Surface-Sterilized Roots of the Seagrass Zostera marina, Int. J. Syst. Bacteriol., 1999, vol. 49, pp. 859–865.

    Article  PubMed  CAS  Google Scholar 

  8. Sass, H. and Cypionka, H, Isolation of Sulfate-Reducing Bacteria from the Terrestrial Deep Subsurface and Description of Desulfovibrio cavernae sp. nov., Syst. Appl. Microbiol., 2004, vol. 27, pp. 541–548.

    Article  PubMed  Google Scholar 

  9. Heidelberg, J.F., Seshadri, R., Haveman, S.A., Hemme, C.L., et al., The Genome Sequence of the Anaerobic, Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough, Nat. Biotechnol., 2004, vol. 22, pp. 554–559.

    Article  PubMed  CAS  Google Scholar 

  10. Santana, M. and Mednansky M.-C., The Adaptive Genome of Desulfovibrio vulgaris Hildenborough, FEMS Microbiol. Lett., 2006, vol. 260, pp. 127–133.

    Article  PubMed  CAS  Google Scholar 

  11. Postgate, J.R., The Sulfate-Reducing Bacteria, 2nd ed., Cambridge University Press, Cambridge, UK, 1984.

    Google Scholar 

  12. Weller, D.M. and Thomashow, L.S., Current Challenges in Introducing Beneficial Microorganisms into the Rhizosphere, Molecular Ecology of Rhizosphere Microorganisms, O’Gara, F., Dowling, D.N., and Boesten, B., Eds., VCH, New York, NY. 1994, pp. l–18.

    Google Scholar 

  13. Santana, M., Presence and Expression of Terminal Oxygen Reductases in Strictly Anaerobic Sulfate-Reducing Bacteria Isolated from Salt-Marsh Sediments, Anaerobe, 2008, vol. 14, pp. 145–156.

    Article  PubMed  CAS  Google Scholar 

  14. Portillo, M.C. and Gonzalez, J.M., Statistical Differences between Relative Quantitative Molecular Fingerprints from Microbial Communities, Antonie van Leeuwenhoek, 2008, vol. 94, pp. 157–163.

    Article  PubMed  CAS  Google Scholar 

  15. Muyzer, G., de Waal, E.C., and Uitterlinden, A.G., Profiling of Complex Microbial Populations by Denaturing Gradient Gel Electrophoresis Analysis of Polymerase Chain Reaction-Amplified Genes Coding for 16S rRNA, Appl. Environ. Microbiol., 1993, vol. 59, pp. 695–700.

    PubMed  CAS  Google Scholar 

  16. Kitamura, M., Takayama, Y., Kojima, S., Kohno, K., Ogata, H., Higuchi, Y., and Inoue, H., Cloning and Expression of the Enolase Gene from Desulfovibrio vulgaris (Miyazaki F), Biochim. Biophys. Acta, 2004, vol. 20, pp. 172–181.

    Google Scholar 

  17. Debette, J. and Blondeau, R., Pre-sence de Pseudomonas maltophilia Dans la Rhizosphère de Quelques Plantes Cultivées, Can. J. Microbiol., 1980, vol. 26, pp. 460–463.

    Article  PubMed  CAS  Google Scholar 

  18. Berg, G., Roskot, N., and Smalla, K., Genotypic and Phenotypic Relationships between Cinical and Environmental Isolates of Stenotrophomonas maltophilia, J. Clin. Microbiol., 1999, vol. 37, pp. 3594–3600.

    PubMed  CAS  Google Scholar 

  19. Juhnke, M.E. and Des Jardin, E., Selective Medium for Isolation of Xanthomonas maltophilia from Soil and Rhizosphere Environments, Appl. Environ. Microbiol., 1989, vol. 155, pp. 747–750.

    Google Scholar 

  20. Soltmann, U., Wand, H., Müller, A., Kuschk, P., and Stottmeister, U., Exposure to Xenobiotics Deeply Affects the Bacteriocenosis in the Rhizosphere of Helophytes, Acta Biotechnol., 2002, vol. 22, pp. 161–166.

    Article  CAS  Google Scholar 

  21. Child, R., Miller, C.D., Liang, Y., Narasimham, G., Chatterton, J., Harrison, P., Sims, R.C., Britt, D., and Anderson, A.J., Polycyclic Aromatic Hydrocarbon-Degrading Mycobacterium Isolates: Their Association with Plant Roots, Appl. Microbiol. Biotechnol., 2007, vol. 75, pp. 655–663.

    Article  PubMed  CAS  Google Scholar 

  22. Denton, M. and Kerr, K.G., Microbiological and Clinical Aspects of Infection Associated with Stenotrophomonas maltophilia, Clin. Microbiol. Rev., 1998, vol. 11, pp. 57–80.

    PubMed  CAS  Google Scholar 

  23. Kaparullina, E., Doronina, N., Chistyakova, T., and Trotsenko, Y., Stenotrophomonas chelatiphaga sp. nov., a New Aerobic EDTA-Degrading Bacterium. Syst. Appl. Microbiol., 2009, vol. 32, pp. 157–162.

    Article  PubMed  CAS  Google Scholar 

  24. O’Toole, R., Smeulders, M.J., Blokpoel, M.C., Kay, E.J., Lougheed, K., and Williams, H.D., A Two-Component Regulator of Universal Stress Protein Expression and Adaptation to Oxygen Starvation in Mycobacterium smegmatis, J. Bacteriol., 2003, vol. 185, pp. 1543–1554.

    Article  PubMed  Google Scholar 

  25. Crossman, L.C., Gould, V.C., Dow J.M., Vernikos, G.S., et al., The Complete Genome, Comparative and Functional Analysis of Stenotrophomonas maltophilia Reveals an Organism Heavily Shielded by Drug Resistance Determinants, Genome Biol., 2008, 9, R74, doi: 1186/gb-2008-9-4-r74

    Article  PubMed  Google Scholar 

  26. Lamrabet, O., Pieulle, L., Aubert, C., Mouhamar, F., Stocker, P., Dolla, A., and Brasseur, G., Oxygen Reduction in the Strict Anaerobe Desulfovibrio vulgaris Hildenborough: Characterization of Two Membrane-Bound Oxygen Reductases, Microbiol., 2011, doi: 10.1099/mic.0.049171-0

  27. Deshusses, J.P.M., Myo-Inositol Transport in Bacteria: H+ Symport and Periplasmic Binding Protein Dependence, Annals NY Acad. Sci., 1985, vol. 456, pp. 351–360.

    Article  CAS  Google Scholar 

  28. Shyu, J.B.H., Lies, D.P., and Newman, D.K., Protective Role of tolC in Efflux of the Electron Shuttle Anthraquinone-2,6-Disulfonate, J. Bacteriol., 2002, vol. 184, pp. 1806–1810.

    Article  PubMed  CAS  Google Scholar 

  29. Trüper, H.G., Microorganisms and the Sulfur Cycle, Sulfur: Its Significance for Chemistry, for the Geo-, Bio- and Cosmosphere, and Technology, 5th ed., Müller, A. and Krebs, B., Eds., Elsevier, Amsterdam, 1984, pp. 351–365.

    Google Scholar 

  30. Mann, K.H., Production and Use of Detritus in Various Freshwater, Estuarine, and Coastal Marine Ecosystems, Limnol. Oceanogr., 1988, vol. 33, pp. 910–930.

    Article  CAS  Google Scholar 

  31. Skyring, G.W., Acetate as the Main Energy Substrate for the Sulfate-Reducing Bacteria in Lake Eliza (South Australia) Hypersaline Sediments, FEMS Microbiol. Ecol., 1988, vol. 53, pp. 87–94.

    Article  CAS  Google Scholar 

  32. Widdel, F. and Bak, F., Gram-Negative Mesophilic Sulfate-Reducing Bacteria, The Prokaryotes. Balows, A., Trüper, H.G., Dworkin, M. and Schleifer, K.-H., Eds., New York, Springer-Verlag, 1992, pp. 3352–3378.

    Google Scholar 

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Correspondence to M. M. Santana.

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Santana, M.M., Portillo, M.C. & Gonzalez, J.M. Mutualistic growth of the sulfate-reducer Desulfovibrio vulgaris Hildenborough with different carbohydrates. Microbiology 81, 663–668 (2012). https://doi.org/10.1134/S002626171206015X

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