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. 1996 Apr;62(4):1342–1346. doi: 10.1128/aem.62.4.1342-1346.1996

The effect of growth and starvation on the lysis of the ruminal cellulolytic bacterium Fibrobacter succinogenes.

J E Wells 1, J B Russell 1
PMCID: PMC167900  PMID: 8919795

Abstract

Growing cultures of Fibrobacter succinogenes assimilated more ammonia than could be accounted for by cellular protein, RNA, or DNA and released large amounts of nonammonia nitrogen. The difference between net and true growth was most dramatic at low dilution rates, but mathematical derivations indicated that the lysis rate was a growth rate-independent function. The lysis rate was sevenfold greater than the true maintenance rate (0.07 h-1 versus 0.01 h-1). Because slowly growing cells had as much proton motive force and ATP as fast-growing cells, lysis was not a starvation response per se. Stationary-phase cells had a lysis rate that was 10-fold less than that of growing cells. Rapidly growing cells were not susceptible to phenylmethylsulfonyl fluoride, but phenylmethylsulfonyl fluoride increased the lysis rate of the cultures when they reached the stationary phase. This latter result indicated that autolysins of stationary-phase cells were being inactivated by a serine proteinase. When growing cells were treated with the glycolytic inhibitor iodoacetate, the proteinase-dependent transition to the stationary phase was circumvented, and the rate of lysis could be increased by as much as 50-fold.

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Selected References

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  1. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Bryant M. P. Nutritional requirements of the predominant rumen cellulolytic bacteria. Fed Proc. 1973 Jul;32(7):1809–1813. [PubMed] [Google Scholar]
  4. Bryant M. P., Robinson I. M. Studies on the Nitrogen Requirements of Some Ruminal Cellulolytic Bacteria. Appl Microbiol. 1961 Mar;9(2):96–103. doi: 10.1128/am.9.2.96-103.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CHANEY A. L., MARBACH E. P. Modified reagents for determination of urea and ammonia. Clin Chem. 1962 Apr;8:130–132. [PubMed] [Google Scholar]
  6. Doyle R. J., Chaloupka J., Vinter V. Turnover of cell walls in microorganisms. Microbiol Rev. 1988 Dec;52(4):554–567. doi: 10.1128/mr.52.4.554-567.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Doyle R. J., Koch A. L. The functions of autolysins in the growth and division of Bacillus subtilis. Crit Rev Microbiol. 1987;15(2):169–222. doi: 10.3109/10408418709104457. [DOI] [PubMed] [Google Scholar]
  8. Harrison D. G., Beever D. E., Thomson D. J., Osbourn D. F. Manipulation of fermentation in the rumen. J Sci Food Agric. 1976 Jul;27(7):617–620. doi: 10.1002/jsfa.2740270706. [DOI] [PubMed] [Google Scholar]
  9. Howlett M. R., Mountfort D. O., Turner K. W., Roberton A. M. Metabolism and growth yields in Bacteroides ruminicola strain b14. Appl Environ Microbiol. 1976 Aug;32(2):274–283. doi: 10.1128/aem.32.2.274-283.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jolliffe L. K., Doyle R. J., Streips U. N. Extracellular proteases modify cell wall turnover in Bacillus subtilis. J Bacteriol. 1980 Mar;141(3):1199–1208. doi: 10.1128/jb.141.3.1199-1208.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jolliffe L. K., Doyle R. J., Streips U. N. The energized membrane and cellular autolysis in Bacillus subtilis. Cell. 1981 Sep;25(3):753–763. doi: 10.1016/0092-8674(81)90183-5. [DOI] [PubMed] [Google Scholar]
  12. Koch A. L., Doyle R. J. Inside-to-outside growth and turnover of the wall of gram-positive rods. J Theor Biol. 1985 Nov 7;117(1):137–157. doi: 10.1016/s0022-5193(85)80169-7. [DOI] [PubMed] [Google Scholar]
  13. Koch A. L. The surface stress theory of microbial morphogenesis. Adv Microb Physiol. 1983;24:301–366. doi: 10.1016/s0065-2911(08)60388-4. [DOI] [PubMed] [Google Scholar]
  14. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  15. Leng R. A., Nolan J. V. Nitrogen metabolism in the rumen. J Dairy Sci. 1984 May;67(5):1072–1089. doi: 10.3168/jds.S0022-0302(84)81409-5. [DOI] [PubMed] [Google Scholar]
  16. Pirt S. J. Maintenance energy: a general model for energy-limited and energy-sufficient growth. Arch Microbiol. 1982 Dec 3;133(4):300–302. doi: 10.1007/BF00521294. [DOI] [PubMed] [Google Scholar]
  17. Pirt S. J. The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci. 1965 Oct 12;163(991):224–231. doi: 10.1098/rspb.1965.0069. [DOI] [PubMed] [Google Scholar]
  18. Russell J. B., Cook G. M. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev. 1995 Mar;59(1):48–62. doi: 10.1128/mr.59.1.48-62.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Russell J. B., Strobel H. J. ATPase-dependent energy spilling by the ruminal bacterium, Streptococcus bovis. Arch Microbiol. 1990;153(4):378–383. doi: 10.1007/BF00249009. [DOI] [PubMed] [Google Scholar]
  20. Wallace R. J., McPherson C. A. Factors affecting the rate of breakdown of bacterial protein in rumen fluid. Br J Nutr. 1987 Sep;58(2):313–323. doi: 10.1079/bjn19870098. [DOI] [PubMed] [Google Scholar]
  21. Yang C. M., Russell J. B. Resistance of proline-containing peptides to ruminal degradation in vitro. Appl Environ Microbiol. 1992 Dec;58(12):3954–3958. doi: 10.1128/aem.58.12.3954-3958.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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