Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention

Applied and Environmental Microbiology

Volumn 65, Issue 6, 1999, Pages 2471-2477

  Tappe, W ^a   Laverman, A ^b   Bohland, M ^a,c   Braster, M ^b   Rittershaus, S ^a   Groeneweg, J ^a   Van Verseveld, H W ^b  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c Zeneca GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; NITRITE; OXYGEN;

ARTICLE; BACTERIAL GROWTH; BIOMASS; CHEMOSTAT; GROWTH RATE; MATHEMATICAL MODEL; NITROBACTER; NITROSOMONAS; NONHUMAN; OXYGEN CONSUMPTION; STARVATION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; NITROBACTER WINOGRADSKYI; NITROSOMONAS EUROPAEA;

EID: 0032974710     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/aem.65.6.2471-2477.1999     Document Type: Article

References (42)

1. Arbige, M., and W. R. Chesbro. 1982. Very slow growth of Bacillus polymyxa: stringent response and maintenance energy. Arch. Microbiol. 132:338-344.
2. Azov, Y., and T. Tregubova. 1995. Nitrification processes in stabilisation reservoirs. Water Sci. Technol. 31:313-319.
3. Bakken, L. R. 1997. Culturable and nonculturable bacteria in soil, p. 47-61. In J. D. van Elsas, J. T. Trevors, and E. M. H. Wellington (ed.), Modern soil microbiology. Marcel Dekker, New York, N.Y.
4. Balmelle, B., K. M. Nguyen, B. Capdeville, J. C. Cornier, and A. Deguin. 1992. Study of factors controlling nitrite build-up in biological processes for water nitrification. Water Sci. Technol. 24:1017-1025.
5. Batchelor, S. E., M. Cooper, S. R. Chabra, L. A. Glover, G. S. A. B. Stewart, P. Williams, and J. I. Prosser. 1997. Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria. Appl. Environ. Microbiol. 63:2281-2286.
6. Beyeler, W., P. L. Rogers, and A. Fiechter. 1984. A simple technique for the direct determination of maintenance energy coefficient: an example with Zymomonas mobilis. Appl. Microbiol. Biotechnol. 19:277-280.
7. Bock, E., H.-P. Koops, H. Harms, and B. Ahlers. 1991. The biochemistry of nitrifying organisms, p. 171-199. In J. M. Shively and L. L. Barton (ed.), Variations in autotrophic life. Academic Press, Ltd., London, England.
8. Bock, E., and G. Heinrich. 1971. Struktur-und Funktionsänderungen in reaktivierenden Zellen von Nitrobacter winogradskyi Buch. Arch. Mikrobiol. 77:349-365.
9. - pair of Bacillus licheniformis and associated morphological and physiological characteristics. Antonie Leeuwenhoek 54:95-111.
10. Bulthuis, B. A., G. M. Koningstein, A. H. Stouthamer, and H. W. van Verseveld. 1989. A comparison between aerobic growth of Bacillus licheniformis in continuous culture and partial-recycling fermentor, with contributions to the discussion on maintenance energy demand. Arch. Microbiol. 152:499-507.
11. Chesbro, W. R., T. Evans, and R. Eifert. 1979. Very slow growth of Escherichia coli. J. Bacteriol. 139:625-638.
12. Chesbro, W. 1988. The domains of slow bacterial growth. Can. J. Microbiol. 34:427-435.
13. Csanady, M. 1992. Nitrite formation and bacteriolog cal deterioration of water quality in distribution networks. Water Supply 10:39-53.
14. Egli, T. 1995. The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates. Adv. Microbial Ecol. 14:305-386.
15. Frankena, J., H. W. van Verseveld, and A. H. Stouthamer. 1988. Substrate and energy costs of the production of exocellular enzymes by Bacillus licheniformis. Biotechnol. Bioeng. 32:803-812.
16. Helder, W., and R. T. P. De Vries. 1983. Estuarine nitrite maxima and nitrifying bacteria (Ems-Dollard Estuary). Neth. J. Sea Res. 17:1-18.
17. Keen, G. A., and J. I. Prosser. 1987. Steady state transient growth of autotrophic nitrifying bacteria. Arch. Microbiol. 147:73-79.
18. 2O. 15:562-573.
19. Laanbroek, H. J., and S. Gerards. 1993. Competition for limiting amounts of oxygen between Nitrosomonas europaea and Nitrobacter winogradskyi grown in mixed continuous cultures. Arch. Microbiol. 159:453-459.
20. Mason, C. A., and T. Egli. 1993. Dynamics of microbial growth in the decelerating and stationary phase of batch culture, p. 81-98. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
21. Moriarty, D. J. W., and R. T. Bell. 1993. Bacterial growth and starvation in aquatic environments, p. 25-53. In S. Kjelleberg (ed.), Starvation in bacteria, Plenum Press, New York, N.Y.
22. Müller, R. H., and W. Babel. 1996. Measurement of growth at very low rates (μ=0), an approach to study the energy requirement for the survival of Alcaligenes eutrophus JMP 134. Appl. Environ. Microbiol. 62:147-151.
23. Neijssel, O. M., and D. W. Tempest. 1976. Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture. Arch. Microbiol. 107:215-221.
24. Panikov, N. S. 1995. Microbial growth kinetics, p. 141-143. Chapman & Hall, London, England.
25. Pirt, S. J. 1965. The maintenance energy of bacteria in growing cultures. Proc. R. Soc. London Ser. B 163:223-231.
26. Randall, C. W., and D. Buth. 1984. Nitrite build-up in activated sludge resulting from temperature effects. J. Water Pollut. Control Fed. 56:1039-1049.
27. Schrickx, J. M., A. S. Krave, J. C. Verdoes, C. A. M. J. J. van den Hondel, A. H. Stouthamer, and H. W. van Verseveld. 1993. Growth and product formation in chemostat and recycling cultures by Aspergillus niger N402 and a glucamylase overproducing transformant, provided with multiple copies of a glaA gene. J. Gen. Microbiol. 139:2801-2810.
28. Schut, F., R. A. Prins, and J. C. Gottschal. 1997. Oligotrophy and pelagic marine bacteria: facts and fiction. Aquat. Microb. Ecol. 12:177-202.
29. Smith, R. V., L. C. Burns, R. M. Doyle, S. D. Lennox, B. H. L. Kelso, R. H. Foy, and R. J. Stevens. 1997. Free ammonia inhibition of nitrification in river sediments leading to nitrite accumulation. J. Environ. Qual. 26:1049-1055.
30. Stein, L. Y., and D. J. Arp. 1998. Ammonium limitation results in loss of ammonia-oxidizing activity in Nitrosomonas europaea. Appl. Environ. Microbiol. 64:1514-1521.
31. Stouthamer, A. H., B. A. Bulthuis, and H. W. van Verseveld. 1990. Energetics of growth at low growth rates and its relevance for the maintenance concept, p. 85-102. In R. K. Poole, M. J. Bazin, and C. W. Keevil (ed.), Microbial growth dynamics. IRL Press, Oxford, United Kingdom.
32. Tappe, W., C. Tomaschewski, S. Rittershaus, and J. Groeneweg. 1996. Cultivation of nitrifying bacteria in the retentostat, a simple fermentor with internal biomass retention. FEMS Microbiol. Ecol. 19:47-52.
33. Tomaschewski, C. 1997. Erhaltungsstoffwechsel und Überlebensfähigkeit des Ammoniak oxidierenden Bakteriums Nitrosomonas europaea. Ph.D. thesis. Technical University of Aachen, Aachen, Germany.
34. min) in a recycling fermentor and its prediction from the kinetic parameters of Pseudomonas sp. strain B13 from batch and chemostat cultures. Appl. Environ. Microbiol. 62:3655-3661.
35. van Elsas, J. D., and L. S. van Overbeek. 1993. Bacterial responses to soil stimuli, p. 55-79. In S. Kjelleberg (ed.), Starvation in bacteria. Plenum Press, New York, N.Y.
36. van Verseveld, H. W., M. Arbige, and W. R. Chesbro. 1984. Continuous culture of bacteria with biomass retention. Trends Biotechnol. 2:8-12.
37. van Verseveld, H. W., W. R. Chesbro, M. Braster, and A. H. Stouthamer. 1984. Eubacteria have 3 growth modes keyed to nutrient flow - consequences for the concept of maintenance and maximal growth yield. Arch. Microbiol. 137:176-184.
38. van Verseveld, H. W., J. A. de Hollander, J. Frankena, M. Braster, F. J. Leeuwerik, and A. H. Stouthamer. 1986. Modelling of microbial substrate conversion, growth and product formation in a recycling fermentor. Antonie Leeuwenhoek 52:325-342.
39. van Verseveld, H. W., M. Metwally, M. el Sayed, M. Osman, J. M. Schrickx, and A. H. Stouthamer. 1991. Determination of the maximum product yield from glucoamylase-producing Aspergillus niger grown in the recycling fermentor. Antonie Leeuwenhoek 60:313-323.
40. Verhagen, F. J. M., H. Duyts, and H. J. Laanbroek. 1992. Competition for ammonium between nitrifying and heterotrophic bacteria in continuously percolated soil columns. Appl. Environ. Microbiol. 58:1962-1969.
41. Verhagen, F. J. M., and H. J. Laanbroek. 1992. Effects of grazing by flagellates on competition for ammonium between nitrifying and heterotrophic bacteria in chemostats. Appl. Environ. Microbiol. 58:1962-1969.
42. Wilhelm, R., O. Heller, M. Bohland, C. Tomaschewski, I. Klein, W. Tappe, J. Groeneweg, and C. J. Soeder. 1998. Biometric analysis of physiologically structured pure bacterial cultures recovering from starvation. Can. J. Microbiol. 44:399-404.