1887

Abstract

Acetogens were enumerated from root homogenates of the black needlerush obtained from a nearly pristine salt marsh. An isolated colony, ST1, yielded acetogenic activity and was initially thought to be a pure culture; however, ST1 was subsequently found to be composed of an aerotolerant fermentative anaerobe (RC) and an acetogen (RS) ( indicates type strain). The two spore-forming mesophiles were separated by selective cultivation under conditions favouring the growth of either RC or RS. The 16S rRNA gene sequence of RC was 99 % similar to that of , indicating that RC was a new isolate of this clostridial species. The rRNA gene sequence most similar to that of RS was only 96 % similar to that of RS and was from a species of the acetogenic genus , indicating that RS was a new sporomusal species; the name sp. nov. is proposed. RC grew at the expense of saccharides. H-forming butyrate fermentation was the primary catabolism utilized by RC under anoxic conditions, while homolactate fermentation was the primary catabolism under oxic conditions. RC consumed O and tolerated 20 % O in the headspace of shaken broth cultures. In contrast, RS was acetogenic, utilized H, lactate and formate, did not utilize saccharides, and could not tolerate high concentrations of O. RS grew by trophic interaction with RC on saccharides via the uptake of H, and, to a lesser extent, lactate and formate produced by RC. Co-cultures of the two organisms yielded high amounts of acetate. These results indicate that (i) previously uncharacterized species of are associated with roots and (ii) trophic links to O-consuming aerotolerant anaerobes might contribute to the activities and survival strategies of acetogens in salt marsh rhizospheres, a habitat subject to gradients of plant-derived O.

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2006-04-01
2019-11-17
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References

  1. Alef, K. ( 1991; ). Methodenhandbuch Bodenmikrobiologie: Aktivitäten, Biomasse, Differenzierung, pp. 44–49. Landsberg/Lech, Germany: Ecomed.
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  3. Armstrong, W., Justin, S. H. F. W., Beckett, P. M. & Lythe, S. ( 1991; ). Root adaptation to soil water logging. Aquat Bot 39, 57–73.[CrossRef]
    [Google Scholar]
  4. Beauchamp, C. & Fridovich, I. ( 1971; ). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Ann Biochem 44, 276–287.[CrossRef]
    [Google Scholar]
  5. Beers, R. F. & Sizers, I. W. ( 1952; ). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195, 133.
    [Google Scholar]
  6. Bilofsky, H. S. & Burks, C. ( 1988; ). The GenBank genetic sequence data bank. Nucleic Acids Res 16, 1861–1864.[CrossRef]
    [Google Scholar]
  7. Blom, C. W. P. M. ( 1999; ). Adaptations to flooding stress: from plant community to molecule. Plant Biol 1, 261–273.[CrossRef]
    [Google Scholar]
  8. Boga, H. I. & Brune, A. ( 2003; ). Hydrogen-dependent oxygen reduction by homoacetogenic bacteria isolated from termite guts. Appl Environ Microbiol 69, 779–786.[CrossRef]
    [Google Scholar]
  9. Boga, H. I., Ludwig, W. & Brune, A. ( 2003; ). Sporomusa aerivorans sp. nov., an oxygen-reducing homoacetogenic bacterium from the gut of a soil-feeding termite. Int J Syst Bacteriol 53, 1397–1404.[CrossRef]
    [Google Scholar]
  10. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the priniciple of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  11. Breznak, J. A., Switzer, J. M. & Seitz, H.-J. ( 1988; ). Sporomusa termitida sp. nov., an H2/CO2-utilizing acetogen isolated from termites. Arch Microbiol 150, 282–288.[CrossRef]
    [Google Scholar]
  12. Brune, A., Emerson, D. & Breznak, J. A. ( 1995; ). The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61, 2681–2687.
    [Google Scholar]
  13. Buckel, W. ( 2005; ). Special clostridial enzymes and fermentation pathways. In Handbook on Clostridia, pp. 177–220. Edited by P. Dürre. Boca Raton, FL: CRC Press.
  14. Christensen, P. B., Revsbech, N. P. & Sand-Jensen, K. ( 1994; ). Microsensor analysis of oxygen in the rhizosphere of the aquatic macrophyte Littorella uniflora (L.) Ascherson. Plant Physiol 105, 847–852.
    [Google Scholar]
  15. Dame, R. F. & Kenny, P. D. ( 1986; ). Variability of Spartina alterniflora primary production in the euhaline North Inlet estuary. Mar Ecol Prog Ser 32, 71–80.[CrossRef]
    [Google Scholar]
  16. Dang, H. & Lovell, C. R. ( 2000; ). Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66, 467–475.[CrossRef]
    [Google Scholar]
  17. Daniel, S. L., Hsu, T., Dean, S. I. & Drake, H. L. ( 1990; ). Characterization of the H2- and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui. J Bacteriol 172, 4464–4471.
    [Google Scholar]
  18. Das, A., Coulter, E. D., Kurtz, D. M. & Ljungdahl, L. G. ( 2001; ). Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidoreductase-rubredoxin and rubrerythrin-type A flavoprotein-high-molecular-weight rubredoxin. J Bacteriol 183, 1560–1567.[CrossRef]
    [Google Scholar]
  19. Das, A., Silaghi-Dumitrescu, R., Ljungdahl, L. G. & Kurtz, D. M., Jr ( 2005; ). Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica. J Bacteriol 187, 2020–2029.[CrossRef]
    [Google Scholar]
  20. Drake, H. L. ( 1994; ). Acetogenesis, acetogenic bacteria, and the acetyl-CoA “Wood/Ljungdahl” pathway: past and current perspectives. In Acetogenesis, pp. 3–60. Edited by H. L. Drake. New York: Chapman & Hall.
  21. Drake, H. L. & Daniel, S. L. ( 2004; ). Physiology of the thermophilic acetogen Moorella thermoacetica. Res Microbiol 155, 869–883.[CrossRef]
    [Google Scholar]
  22. Drake, H. L. & Küsel, K. ( 2005; ). Acetogenic clostridia. In Handbook on Clostridia, pp. 719–746. Edited by P. Dürre. Boca Raton, FL: CRC Press.
  23. Drake, H. L., Küsel, K. & Matthies, C. ( 2002; ). Ecological consequences of the phylogenetic and physiological diversities of acetogens. Antonie van Leeuwenhoek 81, 203–213.[CrossRef]
    [Google Scholar]
  24. Drake, H. L., Küsel, K. & Matthies, C. ( 2004; ). Acetogenic Prokaryotes. In The Prokaryotes, 3rd edn, An Evolving Electronic Resource for the Microbiological Community, release 3.17, August 2004. http://springeronline.com. Edited by M. Dworkin and others. New York: Springer.
  25. Dürre, P. ( 2005; ). Formation of solvents in clostridia. In Handbook on Clostridia, pp. 671–693. Edited by P. Dürre. Boca Raton, FL: CRC Press.
  26. Fröstl, J. M., Seifritz, C. & Drake, H. L. ( 1996; ). Effect of nitrate on the autotrophic metabolism of the acetogens Clostridium thermoautotrophicum and Clostridium thermoaceticum. J Bacteriol 178, 4597–4603.
    [Google Scholar]
  27. Gibson, G. R. ( 1990; ). Physiology and ecology of the sulphate-reducing bacteria. J Appl Bacteriol 69, 769–797.[CrossRef]
    [Google Scholar]
  28. Gößner, A. S., Devereux, R., Ohnemüller, N., Acker, G., Stackebrandt, E. & Drake, H. L. ( 1999; ). Thermicanus aegyptius gen. nov., sp. nov., isolated from oxic soil, a fermentative microaerophile that grows commensally with the thermophilic acetogen Moorella thermoacetica. Appl Environ Microbiol 65, 5124–5133.
    [Google Scholar]
  29. Hippe, H., Andreesen, J. R. & Gottschalk, G. ( 1992; ). The genus Clostridium – nonmedical. In The Prokaryotes, 2nd edn, pp. 1800–1866. Edited by A. Balows, H. C. Trüper, M. Dworkin, W. Harder, & K.-H. Schleifer. New York: Springer.
  30. Hwang, Y.-H. & Morris, J. T. ( 1991; ). Evidence for hygrometric pressurization in the internal gas space of Spartina alterniflora. Plant Physiol 96, 166–171.[CrossRef]
    [Google Scholar]
  31. Jackson, M. B. & Armstrong, W. ( 1999; ). Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1, 274–287.[CrossRef]
    [Google Scholar]
  32. Jensen, N. B. S., Melchiorsen, C. R., Jokumsen, K. V. & Villadsen, J. ( 2001; ). Metabolic behavior of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Appl Environ Microbiol 67, 2677–2682.[CrossRef]
    [Google Scholar]
  33. Jones, D. T. & Keis, S. ( 2005; ). Species and strain identification methods. In Handbook on Clostridia, pp. 3–19. Edited by P. Dürre. Boca Raton, FL: CRC Press.
  34. Jorgensen, B. B. ( 1977; ). Bacterial sulfate reduction within reduced microniches of oxidized marine sediments. Mar Biol 41, 7–17.[CrossRef]
    [Google Scholar]
  35. Karnholz, A., Küsel, K., Gößner, A., Schramm, A. & Drake, H. L. ( 2002; ). Tolerance and metabolic response of acetogenic bacteria toward oxygen. Appl Environ Microbiol 68, 1005–1009.[CrossRef]
    [Google Scholar]
  36. Kraemer, G. P. & Alberte, R. S. ( 1995; ). Impact of daily photosynthetic period on protein synthesis and carbohydrate stores in Zostera marina L. (eelgrass) roots: implications for survival in light-limited environments. J Exp Mar Biol Ecol 185, 191–202.[CrossRef]
    [Google Scholar]
  37. Kuhner, C. H., Frank, C., Grießhammer, A., Schmittroth, M., Acker, G., Gößner, A. & Drake, H. L. ( 1997; ). Sporomusa silvacetica sp. nov., an acetogenic bacterium isolated from aggregated forest soil. Int J Syst Bacteriol 47, 352–358.[CrossRef]
    [Google Scholar]
  38. Kuhner, C. H., Matthies, C., Acker, G., Schmittroth, M., Gößner, A. S. & Drake, H. L. ( 2000; ). Clostridium akagii sp. nov. and Clostridium acidisoli sp. nov. acid-tolerant, N2-fixing clostridia isolated from acidic forest soil and litter. Int J Syst Evol Microbiol 50, 873–881.[CrossRef]
    [Google Scholar]
  39. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. ( 2001; ). mega2: Molecular Evolutionary Genetics Analysis software. Tempe, AZ: Arizona State University.
  40. Küsel, K. & Drake, H. L. ( 1995; ). Effects of environmental parameters on the formation and turnover of acetate by forest soils. Appl Environ Microbiol 61, 3667–3675.
    [Google Scholar]
  41. Küsel, K., Wagner, C. & Drake, H. L. ( 1999a; ). Enumeration and metabolic product profiles of the anaerobic microflora in the mineral soil and litter of a beech forest. FEMS Microbiol Ecol 29, 91–103.[CrossRef]
    [Google Scholar]
  42. Küsel, K., Pinkart, H. C., Drake, H. L. & Devereux, R. ( 1999b; ). Acetogenic and sulfate-reducing bacteria inhabiting the rhizoplane and deep cortex cells of the sea grass Halodule wrightii. Appl Environ Microbiol 65, 5117–5123.
    [Google Scholar]
  43. Küsel, K., Karnholz, A., Trinkwalter, T., Devereux, R., Acker, G. & Drake, H. L. ( 2001; ). Physiological ecology of Clostridium glycolicum RD-1, an aerotolerant acetogen isolated from sea grass roots. Appl Environ Microbiol 67, 4734–4741.[CrossRef]
    [Google Scholar]
  44. Laanbroek, H. J. & Pfennig, N. ( 1981; ). Oxidation of short-chain fatty acids by sulfate-reducing bacteria in freshwater and in marine sediments. Arch Microbiol 128, 330–335.[CrossRef]
    [Google Scholar]
  45. Lane, D. J. ( 1991; ). 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics, pp. 115–175. Edited by E. Stackebrandt & M. Goodfellow. Chichester, UK: Wiley.
  46. Leaphart, A. B., Friez, M. J. & Lovell, C. R. ( 2003; ). Formyltetrahydrofolate synthetase sequences from salt marsh plant roots reveal a diversity of acetogenic bacteria and other bacterial functional groups. Appl Environ Microbiol 69, 693–696.
    [Google Scholar]
  47. Lee, W.-K., Fujisawa, T., Kawamura, S., Itoh, K. & Mitsuoka, T. ( 1989; ). Clostridium intestinalis sp. nov., an aerotolerant species isolated from the feces of cattle and pigs. Int J Syst Bacteriol 39, 334–336.[CrossRef]
    [Google Scholar]
  48. Lovell, C. R. ( 1994; ). Development of DNA probes for the detection and identification of acetogenic bacteria. In Acetogenesis, pp. 236–253. Edited by H. L. Drake. New York: Chapman & Hall.
  49. Lovell, C. R. ( 2005; ). Belowground interactions among salt marsh plants and microorganisms. In Interactions Between Macro- and Microorganisms in Marine Sediments (Coastal and Estuarine Studies vol. 60), pp. 61–83. Edited by E. Kristensen, J. E. Kostka & R. H. Hease. Washington, DC: American Geophysical Union.
  50. Madigan, M. T. & Martinko, J. M. ( 2005; ). Brock Biology of Microorganisms, 11th edn. Upper Saddle River, NJ: Prentice Hall/Pearson Education.
  51. Matthies, C., Freiberger, A. & Drake, H. L. ( 1993; ). Fumarate dissimilation and differential reductant flow by Clostridium formicoaceticum and Clostridium aceticum. Arch Microbiol 160, 273–278.[CrossRef]
    [Google Scholar]
  52. Matthies, C., Gößner, A., Acker, G., Schramm, A. & Drake, H. L. ( 2004; ). Lactovum miscens gen. nov., sp. nov., an aerotolerant, psychrotolerant, mixed-fermentative anaerobe from acidic forest soil. Res Microbiol 155, 847–854.[CrossRef]
    [Google Scholar]
  53. Möller, B., Oßmer, R., Howard, B. H., Gottschalk, G. & Hippe, H. ( 1984; ). Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov. Arch Microbiol 139, 388–396.[CrossRef]
    [Google Scholar]
  54. Paerl, H. W. & Pinckney, J. L. ( 1996; ). A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb Ecol 31, 225–247.
    [Google Scholar]
  55. Peters, V. & Conrad, R. ( 1995; ). Methanogenic and other strictly anaerobic bacteria in desert soil and other oxic soils. Appl Environ Microbiol 61, 1673–1676.
    [Google Scholar]
  56. Piceno, Y. M., Noble, P. A. & Lovell, C. R. ( 1999; ). Spatial and temporal assessment of diazotrophy assemblage composition in vegetated salt marsh sediments using denaturing gradient gel electrophoresis analysis. Microb Ecol 38, 157–167.[CrossRef]
    [Google Scholar]
  57. Ragsdale, S. W. ( 1991; ). Enzymology of the acetyl-CoA pathway of CO2 fixation. Crit Rev Biochem Mol Biol 26, 261–300.[CrossRef]
    [Google Scholar]
  58. Silaghi-Dumitrescu, R., Coulter, E. D., Das, A., Ljungdahl, L. G., Jameson, G. N. L., Huynh, B. H. & Kurtz, D. M. ( 2003; ). A flavodiiron protein and high molecular weight rubredoxin from Moorella thermoacetica with nitric oxide reductase activity. Biochemistry 42, 2806–2815.[CrossRef]
    [Google Scholar]
  59. Sorensen, J., Christensen, D. & Jorgensen, B. B. ( 1981; ). Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl Environ Microbiol 42, 5–11.
    [Google Scholar]
  60. Sparling, R. & Daniels, L. ( 1987; ). The specificity of growth inhibition of methanogenic bacteria by bromoethanesulfonate. Can J Microbiol 33, 1132–1136.[CrossRef]
    [Google Scholar]
  61. Stanton, T. B. & Jensen, N. S. ( 1993; ). Purification and characterization of NADH oxidase from Serpulina (Treponema) hyodysenteriae. J Bacteriol 175, 2980–2987.
    [Google Scholar]
  62. Stellmach, B., Gottschick, W., Battermann, F. & Zabel, K. ( 1988; ). Bestimmungsmethoden Enzyme, pp. 222–223. Darmstadt, Germany: Steinkopff Verlag.
  63. Tholen, A. & Brune, A. ( 1999; ). Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl Environ Microbiol 65, 4497–4505.
    [Google Scholar]
  64. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  65. Valentine, R. C., Shapiro, B. M. & Stadtman, E. R. ( 1968; ). Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7, 2143–2152.[CrossRef]
    [Google Scholar]
  66. van Niel, E. W. J., Hofvendahl, K. & Hahn-Hägerdal, B. ( 2002; ). Formation and conversion of oxygen metabolites by Lactococcus lactis subsp. lactis ATCC 19435 under different growth conditions. Appl Envion Microbiol 68, 4350–4356.[CrossRef]
    [Google Scholar]
  67. Wagner, C., Grießhammer, A. & Drake, H. L. ( 1996; ). Acetogenic capacities and the anaerobic turnover of carbon in a Kansas prairie soil. Appl Environ Microbiol 62, 494–500.
    [Google Scholar]
  68. Wood, H. G. & Ljungdahl, L. G. ( 1991; ). Autotrophic character of acetogenic bacteria. In Variations in Autotrophic Life, pp. 201–250. Edited by J. M. Shively & L. L. Barton. San Diego, CA: Academic Press.
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