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. 1981 Nov;148(2):541–550. doi: 10.1128/jb.148.2.541-550.1981

Long-term nutrient starvation of continuously cultured (glucose-limited) Selenomonas ruminantium.

R W Mink, R B Hespell
PMCID: PMC216238  PMID: 6170629

Abstract

Selenomonas ruminantium, a strictly anaerobic ruminal bacterium, was grown at various dilution rates (D = 0.05, 0.25, and 0.35 h-1) under glucose-limited continuous culture conditions. Suspensions of washed cells prepared anaerobically in mineral buffer were subjected to nutrient starvation (24 to 36 h; 39 degrees C; N2 atmosphere). Regardless of growth rate, viability declined logarithmically, and within about 2.5 h, about 50% of the populations were nonviable. After 24 h of starvation, the numbers of viable cells appeared to be inversely related to growth rate, the highest levels occurring with the slowest grown population. Cell dry weight, carbohydrate, protein, ribonucleic acid (RNA), and deoxyribonucleic acid declined logarithmically during starvation, and the decline rates of each were generally greater with cells grown at higher D values. Both cellular carbohydrate and RNA declined substantially during the first 12 h of starvation. Most of the cellular RNA that disappeared was found in the suspending buffer as low-molecular-weight, orcinol-positive materials. During growth, S. ruminantium made a variety of fermentation acids from glucose, but during starvation, acetate was the only acid made from catabolism of cellular material. Addition of glucose or vitamins to starving cell suspensions did not decrease loss of viability, whereas a starvation in the spent culture medium resulted in a slight decrease in the rate of viability loss. Overall, the data indicate that S. ruminantium strain D has very little survival capacity under the conditions tested compared with other bacterial species that have been studied.

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Selected References

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  1. Alton T. H., Koch A. L. Unused protein synthetic capacity of Escherichia coli grown in phosphate-limited chemostats. J Mol Biol. 1974 Jun 15;86(1):1–9. doi: 10.1016/s0022-2836(74)80002-1. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Bentley C. M., Dawes E. A. The energy-yielding reactions of Peptococcus prévotii, their behaviour on starvation and the role and regulation of threonine dehydratase. Arch Microbiol. 1974;100(4):363–387. doi: 10.1007/BF00446329. [DOI] [PubMed] [Google Scholar]
  4. Breuil C., Patel G. B. Viability and depletion of cell constituents of Methanospirillum hungatii GP1 during starvation. Can J Microbiol. 1980 Aug;26(8):887–892. doi: 10.1139/m80-154. [DOI] [PubMed] [Google Scholar]
  5. Breznak J. A., Potrikus C. J., Pfennig N., Ensign J. C. Viability and endogenous substrates used during starvation survival of Rhodospirillum rubrum. J Bacteriol. 1978 May;134(2):381–388. doi: 10.1128/jb.134.2.381-388.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bryant M. P. Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr. 1972 Dec;25(12):1324–1328. doi: 10.1093/ajcn/25.12.1324. [DOI] [PubMed] [Google Scholar]
  7. Burleigh I. G., Dawes E. A. Studies on the endogenous metabolism and senescence of starved Sarcina lutea. Biochem J. 1967 Jan;102(1):236–250. doi: 10.1042/bj1020236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. CHANEY A. L., MARBACH E. P. Modified reagents for determination of urea and ammonia. Clin Chem. 1962 Apr;8:130–132. [PubMed] [Google Scholar]
  9. Chapman A. G., Fall L., Atkinson D. E. Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol. 1971 Dec;108(3):1072–1086. doi: 10.1128/jb.108.3.1072-1086.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DAWES E. A., RIBBONS D. W. STUDIES ON THE ENDOGENOUS METABOLISM OF ESCHERICHIA COLI. Biochem J. 1965 May;95:332–343. doi: 10.1042/bj0950332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DAWES E. A., RIBBONS D. W. The endogenous metabolism of microorganisms. Annu Rev Microbiol. 1962;16:241–264. doi: 10.1146/annurev.mi.16.100162.001325. [DOI] [PubMed] [Google Scholar]
  12. Ensign J. C. Long-term starvation survival of rod and spherical cells of Arthrobacter crystallopoietes. J Bacteriol. 1970 Sep;103(3):569–577. doi: 10.1128/jb.103.3.569-577.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GRONLUND A. F., CAMPBELL J. J. NITROGENOUS SUBSTRATES OF ENDOGENOUS RESPIRATION IN PSEUDOMONAS AERUGINOSA. J Bacteriol. 1963 Jul;86:58–66. doi: 10.1128/jb.86.1.58-66.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HARRISON A. P., Jr, LAWRENCE F. R. PHENOTYPIC, GENOTYPIC, AND CHEMICAL CHANGES IN STARVING POPULATIONS OF AEROBACTER AEROGENES. J Bacteriol. 1963 Apr;85:742–750. doi: 10.1128/jb.85.4.742-750.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HUNGATE R. E. The anaerobic mesophilic cellulolytic bacteria. Bacteriol Rev. 1950 Mar;14(1):1–49. doi: 10.1128/br.14.1.1-49.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hespell R. B., Miozzari G. F., Rittenberg S. C. Ribonucleic acid destruction and synthesis during intraperiplasmic growth of Bdellovibrio bacteriovorus. J Bacteriol. 1975 Aug;123(2):481–491. doi: 10.1128/jb.123.2.481-491.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hespell R. B., Thomashow M. F., Rittenberg S. C. Changes in cell composition and viability of Bdellovibrio bacteriovorus during starvation. Arch Microbiol. 1974 May 20;97(4):313–327. doi: 10.1007/BF00403070. [DOI] [PubMed] [Google Scholar]
  18. Isaacson H. R., Hinds F. C., Bryant M. P., Owens F. N. Efficiency of energy utilization by mixed rumen bacteria in continuous culture. J Dairy Sci. 1975 Nov;58(11):1645–1659. doi: 10.3168/jds.S0022-0302(75)84763-1. [DOI] [PubMed] [Google Scholar]
  19. John A., Isaacson H. R., Bryant M. P. Isolation and characteristics of a ureolytic strain of Selenomonas ruminatium. J Dairy Sci. 1974 Sep;57(9):1003–1014. doi: 10.3168/jds.s0022-0302(74)85001-0. [DOI] [PubMed] [Google Scholar]
  20. Johnson R. R. Influence of carbohydrate solubility on non-protein nitrogen utilization in the ruminant. J Anim Sci. 1976 Jul;43(1):184–191. doi: 10.2527/jas1976.431184x. [DOI] [PubMed] [Google Scholar]
  21. Kafkewitz D., Iannotti E. L., Wolin M. J., Bryant M. P. An anaerobic chemostat that permits the collection and measurement of fermentation gases. Appl Microbiol. 1973 Apr;25(4):612–614. doi: 10.1128/am.25.4.612-614.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Koch A. L. The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microb Physiol. 1971;6:147–217. doi: 10.1016/s0065-2911(08)60069-7. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Leedle J. A., Hespell R. B. Differential carbohydrate media and anaerobic replica plating techniques in delineating carbohydrate-utilizing subgroups in rumen bacterial populations. Appl Environ Microbiol. 1980 Apr;39(4):709–719. doi: 10.1128/aem.39.4.709-719.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mathison G. W., Milligan L. P. Nitrogen metabolism in sheep. Br J Nutr. 1971 May;25(3):351–366. doi: 10.1079/bjn19710100. [DOI] [PubMed] [Google Scholar]
  26. Montague M. D., Dawes E. A. The survival of Peptococcus prévotii in relation to the adenylate energy charge. J Gen Microbiol. 1974 Jan;80(1):291–299. doi: 10.1099/00221287-80-1-291. [DOI] [PubMed] [Google Scholar]
  27. Nolan J. V., Norton B. W., Leng R. A. Nitrogen cycling in sheep. Proc Nutr Soc. 1973 Sep;32(2):93–98. doi: 10.1079/pns19730021. [DOI] [PubMed] [Google Scholar]
  28. POSTGATE J. R., HUNTER J. R. The survival of starved bacteria. J Gen Microbiol. 1962 Oct;29:233–263. doi: 10.1099/00221287-29-2-233. [DOI] [PubMed] [Google Scholar]
  29. Pilgrim A. F., Weller R. A., Gray F. V., Belling C. B. Synthesis of microbial protein from ammonia in the sheep's rumen and the proportion of dietary nitrogen converted into microbial nitrogen. Br J Nutr. 1970 Jun;24(2):589–598. doi: 10.1079/bjn19700057. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. RIBBONS D. W., DAWES E. A. Environmental and growth conditions affecting the endogenous metabolism of bacteria. Ann N Y Acad Sci. 1963 Jan 21;102:564–586. doi: 10.1111/j.1749-6632.1963.tb13661.x. [DOI] [PubMed] [Google Scholar]
  32. Reece P., Toth D., Dawes E. A. Fermentation of purines and their effect on the adenylate energy charge and viability of starved Peptococcus prévotii. J Gen Microbiol. 1976 Nov;97(1):63–71. doi: 10.1099/00221287-97-1-63. [DOI] [PubMed] [Google Scholar]
  33. Russell J. B., Baldwin R. L. Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Appl Environ Microbiol. 1979 Mar;37(3):531–536. doi: 10.1128/aem.37.3.531-536.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. SIERRA G., GIBBONS N. E. Role and oxidation pathway of poly-beta-hydroxybutyric acid in Micrococcus halodenitrificans. Can J Microbiol. 1962 Apr;8:255–269. doi: 10.1139/m62-032. [DOI] [PubMed] [Google Scholar]
  35. Salanitro J. P., Muirhead P. A. Quantitative method for the gas chromatographic analysis of short-chain monocarboxylic and dicarboxylic acids in fermentation media. Appl Microbiol. 1975 Mar;29(3):374–381. doi: 10.1128/am.29.3.374-381.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sobek J. M., Charba J. F., Foust W. N. Endogenous metabolism of Azotobacter agilis. J Bacteriol. 1966 Sep;92(3):687–695. doi: 10.1128/jb.92.3.687-695.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stokes J. L., Parson W. L. Role of poly-beta-hydroxybutyrate in survival of Sphaerotilus discophorus during starvation. Can J Microbiol. 1968 Jul;14(7):785–789. doi: 10.1139/m68-130. [DOI] [PubMed] [Google Scholar]
  38. Strange R. E. Bacterial "glycogen" and survival. Nature. 1968 Nov 9;220(5167):606–607. doi: 10.1038/220606a0. [DOI] [PubMed] [Google Scholar]
  39. Thomas T. D., Batt R. D. Degradation of cell constituents by starved Streptococcus lactis in relation to survival. J Gen Microbiol. 1969 Nov;58(3):347–362. doi: 10.1099/00221287-58-3-347. [DOI] [PubMed] [Google Scholar]
  40. Thomas T. D., Batt R. D. Survival of Streptococcus lactis in starvation conditions. J Gen Microbiol. 1968 Mar;50(3):367–382. doi: 10.1099/00221287-50-3-367. [DOI] [PubMed] [Google Scholar]
  41. Wallace R. J. Cytoplasmic reserve polysaccharide of Selenomonas ruminantium. Appl Environ Microbiol. 1980 Mar;39(3):630–634. doi: 10.1128/aem.39.3.630-634.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. de Vries W., Kapteijn W. M., van der Beek E. G., Stouthamer A. H. Molar growth yields and fermentation balances of Lactobacillus casei L3 in batch cultures and in continuous cultures. J Gen Microbiol. 1970 Nov;63(3):333–345. doi: 10.1099/00221287-63-3-333. [DOI] [PubMed] [Google Scholar]
  43. van Houte J., Jansen H. M. Role of glycogen in survival of Streptococcus mitis. J Bacteriol. 1970 Mar;101(3):1083–1085. doi: 10.1128/jb.101.3.1083-1085.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]

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