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. 1982 Jan;43(1):160–168. doi: 10.1128/aem.43.1.160-168.1982

Assimilatory Sulfur Metabolism in Marine Microorganisms: Considerations for the Application of Sulfate Incorporation into Protein as a Measurement of Natural Population Protein Synthesis †

Russell L Cuhel 1,‡, Craig D Taylor 1, Holger W Jannasch 1
PMCID: PMC241796  PMID: 16345919

Abstract

The sulfur content of residue protein was determined for pure cultures of Nitrosococcus oceanus, Desulfovibrio salexigens, 4 mixed populations of fermentative bacteria, 22 samples from mixed natural population enrichments, and 11 nutritionally and morphologically distinct isolates from enrichments of Sargasso Sea water. The average 1.09 ± 0.14% (by weight) S in protein for 13 pure cultures agrees with the 1.1% calculated from average protein composition. An operational value encompassing all mixed population and pure culture measurements has a coefficient of variation of only 15.1% (n = 41). Short-term [35S]sulfate incorporation kinetics by Pseudomonas halodurans and Alteromonas luteoviolaceus demonstrated a rapid appearance of 35S in the residue protein fraction which was well modelled by a simple exponential uptake equation. This indicates that little error in protein synthesis determination results from isotope dilution by endogenous pools of sulfur-containing compounds. Methionine effectively competed with sulfate for protein synthesis in P. halodurans at high concentrations (10 μM), but had much less influence at 1 μM. Cystine competed less effectively with sulfate, and glutathione did not detectably reduce sulfate-S incorporation into protein. [35S]sulfate incorporation was compared with [14C]glucose assimilation in a eutrophic brackish-water environment. Both tracers yielded similar results for the first 8 h of incubation, but a secondary growth phase was observed only with 35S. Redistribution of 14C from low-molecular-weight materials into residue protein indicated additional protein synthesis. [35S]sulfate incorporation into residue protein by marine bacteria can be used to quantitatively measure bacterial protein synthesis in unenriched mixed populations of marine bacteria.

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Selected References

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  1. Apontoweil P., Berends W. Glutathione biosynthesis in Escherichia coli K 12. Properties of the enzymes and regulation. Biochim Biophys Acta. 1975 Jul 14;399(1):1–9. doi: 10.1016/0304-4165(75)90205-6. [DOI] [PubMed] [Google Scholar]
  2. BRITTEN R. J., McCLURE F. T. The amino acid pool in Escherichia coli. Bacteriol Rev. 1962 Sep;26:292–335. doi: 10.1128/br.26.3.292-335.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Cuhel R. L., Taylor C. D., Jannasch H. W. Assimilatory Sulfur Metabolism in Marine Microorganisms: Sulfur Metabolism, Protein Synthesis, and Growth of Alteromonas luteo-violaceus and Pseudomonas halodurans During Perturbed Batch Growth. Appl Environ Microbiol. 1982 Jan;43(1):151–159. doi: 10.1128/aem.43.1.151-159.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cuhel R. L., Taylor C. D., Jannasch H. W. Assimilatory sulfur metabolism in marine microorganisms: characteristics and regulation of sulfate transport in Pseudomonas halodurans and Alteromonas luteo-violaceus. J Bacteriol. 1981 Aug;147(2):340–349. doi: 10.1128/jb.147.2.340-349.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Datko A. H., Mudd S. H., Giovanelli J., Macnicol P. K. Sulfur-containing Compounds in Lemna perpusilla 6746 Grown at a Range of Sulfate Concentrations. Plant Physiol. 1978 Oct;62(4):629–635. doi: 10.1104/pp.62.4.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fahey R. C., Brown W. C., Adams W. B., Worsham M. B. Occurrence of glutathione in bacteria. J Bacteriol. 1978 Mar;133(3):1126–1129. doi: 10.1128/jb.133.3.1126-1129.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fuhrman J. A., Azam F. Bacterioplankton secondary production estimates for coastal waters of british columbia, antarctica, and california. Appl Environ Microbiol. 1980 Jun;39(6):1085–1095. doi: 10.1128/aem.39.6.1085-1095.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giovanelli J., Owens L. D., Mudd S. H. beta-Cystathionase In Vivo Inactivation by Rhizobitoxine and Role of the Enzyme in Methionine Biosynthesis in Corn Seedlings. Plant Physiol. 1973 Mar;51(3):492–503. doi: 10.1104/pp.51.3.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Holmquist R. Evaluation of compositional nonrandomness in proteins. J Mol Evol. 1978 Oct 6;11(4):349–360. doi: 10.1007/BF01733842. [DOI] [PubMed] [Google Scholar]
  11. Jordan M. J. On counseling minority students in a university center. J Am Coll Health Assoc. 1974 Dec;23(2):146–150. [PubMed] [Google Scholar]
  12. Jukes T. H., Holmquist R., Moise H. Amino acid composition of proteins: Selection against the genetic code. Science. 1975 Jul 4;189(4196):50–51. doi: 10.1126/science.237322. [DOI] [PubMed] [Google Scholar]
  13. Karl D. M. Measurement of microbial activity and growth in the ocean by rates of stable ribonucleic Acid synthesis. Appl Environ Microbiol. 1979 Nov;38(5):850–860. doi: 10.1128/aem.38.5.850-860.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kredich N. M., Becker M. A., Tomkins G. M. Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem. 1969 May 10;244(9):2428–2439. [PubMed] [Google Scholar]
  15. Kredich N. M. Regulation of L-cysteine biosynthesis in Salmonella typhimurium. I. Effects of growth of varying sulfur sources and O-acetyl-L-serine on gene expression. J Biol Chem. 1971 Jun 10;246(11):3474–3484. [PubMed] [Google Scholar]
  16. Law A. T., Button D. K. Multiple-carbon-source-limited growth kinetics of a marine coryneform bacterium. J Bacteriol. 1977 Jan;129(1):115–123. doi: 10.1128/jb.129.1.115-123.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Schmidt A., Abrams W. R., Schiff J. A. Reduction of adenosine 5'-phosphosulfate to cysteine in extracts from Chlorella and mutants blocked for sulfate reduction. Eur J Biochem. 1974 Sep 16;47(3):423–434. doi: 10.1111/j.1432-1033.1974.tb03709.x. [DOI] [PubMed] [Google Scholar]
  18. Taylor C. D. Growth of a bacterium under a high-pressure oxy-helium atmosphere. Appl Environ Microbiol. 1979 Jan;37(1):42–49. doi: 10.1128/aem.37.1.42-49.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Taylor C. D., Jannasch H. W. Subsampling technique for measuring growth of bacterial cultures under high hydrostatic pressure. Appl Environ Microbiol. 1976 Sep;32(3):355–359. doi: 10.1128/aem.32.3.355-359.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tempest D. W., Meers J. L., Brown C. M. Influence of environment on the content and composition of microbial free amino acid pools. J Gen Microbiol. 1970 Dec;64(2):171–185. doi: 10.1099/00221287-64-2-171. [DOI] [PubMed] [Google Scholar]

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