Abstract
Marine Beggiatoa strains MS-81-6 and MS-81-1c are filamentous gliding bacteria that use hydrogen sulfide and thiosulfate as electron donors for chemolithotrophic energy generation. They are known to be capable of chemolithoautotrophic growth in sulfide gradient media; here we report the first successful bulk cultivation of these strains in a defined liquid medium. To investigate their nutritional versatilities, strains MS-81-6 and MS-81-1c were grown in sulfide-oxygen gradient media supplemented with single organic compounds. Respiration rates and biomass production relative to those of controls grown in unsupplemented sulfide-limited media were monitored to determine whether organic compounds were utilized as sources of energy and/or cell carbon. With cells grown in sulfide gradient and liquid media, we showed that strain MS-81-6 strongly regulates two enzymes, the tricarboxylic acid cycle enzyme 2-oxoglutarate dehydrogenase and the Calvin cycle enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase, in response to the presence of organic carbon (acetate) in the growth medium. In contrast, strain MS-81-1c lacked 2-oxoglutarate dehydrogenase activity and regulated ribulose-1,5-bisphosphate carboxylase/oxygenase activity only slightly in response to organic substrates. Tracer experiments with radiolabeled acetate showed that strain MS-81-1c did not oxidize acetate to CO(inf2) but could synthesize approximately 20% of its cell carbon from acetate. On the basis of these results, we conclude that Beggiatoa strain MS-81-1c is an obligate chemolithoautotroph, while strain MS-81-6 is a versatile facultative chemolithoautotroph.
Full Text
The Full Text of this article is available as a PDF (227.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- BRAUN A. C., WOOD H. N. On the activation of certain essential biosynthetic systems in cells of Vinca rosea L. Proc Natl Acad Sci U S A. 1962 Oct 15;48:1776–1782. doi: 10.1073/pnas.48.10.1776. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Brown J. P., Perham R. N. Selective inactivation of the transacylase components of the 2-oxo acid dehydrogenase multienzyme complexes of Escherichia coli. Biochem J. 1976 May 1;155(2):419–427. doi: 10.1042/bj1550419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Güde H., Strohl W. R., Larkin J. M. Mixotrophic and heterotrophic growth of Beggiatoa alba in continuous culture. Arch Microbiol. 1981 Jul;129(5):357–360. doi: 10.1007/BF00406462. [DOI] [PubMed] [Google Scholar]
- Jorgensen B. B., Des Marais D. J. Competition for sulfide among colorless and purple sulfur bacteria in cyanobacterial mats. FEMS Microbiol Ecol. 1986;38:179–186. doi: 10.1111/j.1574-6968.1986.tb01727.x. [DOI] [PubMed] [Google Scholar]
- Jørgensen B. B., Revsbech N. P. Colorless Sulfur Bacteria, Beggiatoa spp. and Thiovulum spp., in O(2) and H(2)S Microgradients. Appl Environ Microbiol. 1983 Apr;45(4):1261–1270. doi: 10.1128/aem.45.4.1261-1270.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuenen J. G., Beudeker R. F. Microbiology of thiobacilli and other sulphur-oxidizing autotrophs, mixotrophs and heterotrophs. Philos Trans R Soc Lond B Biol Sci. 1982 Sep 13;298(1093):473–497. doi: 10.1098/rstb.1982.0093. [DOI] [PubMed] [Google Scholar]
- Kuenen J. G., Veldkamp H. Effects of organic compounds on growth of chemostat cultures of Thiomicrospira pelophila, Thiobacillus thioparus and Thiobacillus neapolitanus. Arch Mikrobiol. 1973 Dec 21;94(2):173–190. doi: 10.1007/BF00416691. [DOI] [PubMed] [Google Scholar]
- Larkin J. M., Strohl W. R. Beggiatoa, Thiothrix, and Thioploca. Annu Rev Microbiol. 1983;37:341–367. doi: 10.1146/annurev.mi.37.100183.002013. [DOI] [PubMed] [Google Scholar]
- Matin A. Organic nutrition of chemolithotrophic bacteria. Annu Rev Microbiol. 1978;32:433–468. doi: 10.1146/annurev.mi.32.100178.002245. [DOI] [PubMed] [Google Scholar]
- Nelson D. C., Castenholz R. W. Organic nutrition of Beggiatoa sp. J Bacteriol. 1981 Jul;147(1):236–247. doi: 10.1128/jb.147.1.236-247.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson D. C., Castenholz R. W. Use of reduced sulfur compounds by Beggiatoa sp. J Bacteriol. 1981 Jul;147(1):140–154. doi: 10.1128/jb.147.1.140-154.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson D. C., Jørgensen B. B., Revsbech N. P. Growth Pattern and Yield of a Chemoautotrophic Beggiatoa sp. in Oxygen-Sulfide Microgradients. Appl Environ Microbiol. 1986 Aug;52(2):225–233. doi: 10.1128/aem.52.2.225-233.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson D. C., Revsbech N. P., Jørgensen B. B. Microoxic-Anoxic Niche of Beggiatoa spp.: Microelectrode Survey of Marine and Freshwater Strains. Appl Environ Microbiol. 1986 Jul;52(1):161–168. doi: 10.1128/aem.52.1.161-168.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SORBO B. A colorimetric method for the determination of thiosulfate. Biochim Biophys Acta. 1957 Feb;23(2):412–416. doi: 10.1016/0006-3002(57)90346-3. [DOI] [PubMed] [Google Scholar]
- Strohl W. R., Cannon G. C., Shively J. M., Güde H., Hook L. A., Lane C. M., Larkin J. M. Heterotrophic carbon metabolism by Beggiatoa alba. J Bacteriol. 1981 Nov;148(2):572–583. doi: 10.1128/jb.148.2.572-583.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strohl W. R., Larkin J. M. Enumeration, isolation, and characterization of beggiatoa from freshwater sediments. Appl Environ Microbiol. 1978 Nov;36(5):755–770. doi: 10.1128/aem.36.5.755-770.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]