Oxygen consumption rates of bacteria under nutrient-limited conditions

Applied and Environmental Microbiology

Volumn 79, Issue 16, 2013, Pages 4921-4931

  Riedel, Timothy ^a,b   Berelson, William ^a   Nealson, Kenneth ^a   Finkel, Steven ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Engineering IV   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POPULATION; ESCHERICHIA COLI K-12; HETEROTROPHIC BACTERIAS; NUTRIENT AVAILABILITY; NUTRIENT-LIMITED CONDITION; NUTRIENT-LIMITED ENVIRONMENT; OXYGEN CONSUMPTION RATE; SHEWANELLA ONEIDENSIS MR-1;

BACTERIA; BATCH CELL CULTURE; ESCHERICHIA COLI; POPULATION STATISTICS;

NUTRIENTS;

GENETIC ANALYSIS; GROWTH RATE; HETEROTROPHY; MICROBIAL ACTIVITY; NUTRIENT AVAILABILITY; OXYGEN CONSUMPTION; POPULATION DENSITY; RESPIRATION;

ARTICLE; ESCHERICHIA COLI K 12; FLUORESCENCE MICROSCOPY; MARINOBACTER; METABOLISM; MICROBIOLOGY; OXYGEN CONSUMPTION; SEDIMENT; SHEWANELLA;

ESCHERICHIA COLI K12; GEOLOGIC SEDIMENTS; MARINOBACTER; MICROSCOPY, FLUORESCENCE; OXYGEN CONSUMPTION; SHEWANELLA;

EID: 84880979310     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00756-13     Document Type: Article

References (71)

1. Rivkin RB, Legendre L. 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398-2400.
2. Sanderman J, Amundson R. 2003. Biogeochemistry of decomposition and detrital processing, p 249-316. In Holland HD, Turekian KK (ed), Treatise on geochemistry. Pergamon, Oxford, United Kingdom.
3. del Giorgio PA, Duarte CM. 2002. Respiration in the open ocean. Nature 420:379-384.
4. Duarte CM, Agusti S. 1998. The CO2 balance of unproductive aquatic ecosystems. Science 281:234-236.
5. Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5:782-791.
6. Molter TW, Holl MR, Dragavon JM, McQuaide SC, Anderson JB, Young AC, Burgess LW, Lidstrom ME, Meldrum DR. 2008. A new approach for measuring single-cell oxygen consumption rates. IEEE Trans. Autom. Sci. Eng. 5:32-42.
7. Molter TW, McQuaide SC, Suchorolski MT, Strovas TJ, Burgess LW, Meldrum DR, Lidstrom ME. 2009. A microwell array device capable of measuring single-cell oxygen consumption rates. Sens. Actuators B Chem. 135:678-686.
8. Røy H, Kallmeyer J, Adhikari RR, Pockalny R, Jørgensen D'Hondt BBS. 2012. Aerobic microbial respiration in 86-million-year-old deep-sea red clay. Science 336:922-925.
9. Calhoun MW, Oden KL, Gennis RB, de Mattos MJ, Neijssel OM. 1993. Energetic efficiency of Escherichia coli: effects of mutations in components of the aerobic respiratory chain. J. Bacteriol. 175:3020-3025.
10. Hempfling WP, Mainzer SE. 1975. Effects of varying the carbon source limiting growth on yield and maintenance characteristics of Escherichia coli in continuous culture. J. Bacteriol. 123:1076-1087.
11. Lin HY, Mathiszik B, Xu B, Enfors SO, Neubauer P. 2001. Determination of the maximum specific uptake capacities for glucose and oxygen in glucose-limited fed-batch cultivations of Escherichia coli. Biotechnol. Bioeng. 73:347-357.
12. Neijssel OM, Tempest DW. 1976. Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture. Arch. Microbiol. 107:215-221.
13. Neijssel OM, Tempest DW. 1975. The regulation of carbohydrate metabolism in Klebsiella aerogenes NCTC 418 organisms, growing in chemostat culture. Arch. Microbiol. 106:251-258.
14. Neijssel OM, Tempest DW. 1976. The role of energy-spilling reactions in the growth of Klebsiella aerogenes NCTC 418 in aerobic chemostat culture. Arch. Microbiol. 110:305-311.
15. Andersen KB, von Meyenburg K. 1980. Are growth rates of Escherichia coli in batch cultures limited by respiration? J. Bacteriol. 144:114-123.
16. Ballesteros M, Fredriksson A, Henriksson J, Nyström T. 2001. Bacterial senescence: protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes. EMBO J. 20:5280-5289.
17. Novitsky JA, Morita RY. 1977. Survival of a psychrophilic marine vibrio under long-term nutrient starvation. Appl. Environ. Microbiol. 33:635-641.
18. Iacobellis NS, Devay JE. 1986. Long-term storage of plant-pathogenic bacteria in sterile distilled water. Appl. Environ. Microbiol. 52:388-389.
19. Liao CH, Shollenberger LM. 2003. Survivability and long-term preservation of bacteria in water and in phosphate-buffered saline. Lett. Appl. Microbiol. 37:45-50.
20. Harrison AP, Lawrence FR. 1963. Phenotypic, genotypic, and chemical changes in starving populations of Aerobacter aerogenes. J. Bacteriol. 85: 742-750.
21. Hamer G. 1985. Lysis and "cryptic" growth in wastewater and sludge treatment processes. Acta Biotechnol. 5:117-127.
22. Mason CA, Hamer G. 1987. Cryptic growth in Klebsiella pneumoniae. Appl. Microbiol. Biotechnol. 25:577-584.
23. Rozen DE, Philippe N, Arjan de Visser J, Lenski RE, Schneider D. 2009. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol. Lett. 12:34-44.
24. Zambrano MM, Kolter R. 1993. Escherichia coli mutants lacking NADH dehydrogenase I have a competitive disadvantage in stationary phase. J. Bacteriol. 175:5642-5647.
25. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760.
26. Finkel SE, Kolter R. 1999. Evolution of microbial diversity during prolonged starvation. Proc. Natl. Acad. Sci. U. S. A. 96:4023-4027.
27. Zinser ER, Kolter R. 2000. Prolonged stationary-phase incubation selects for lrp mutations in Escherichia coli K-12. J. Bacteriol. 182:4361-4365.
28. Zinser ER, Kolter R. 2004. Escherichia coli evolution during stationary phase. Res. Microbiol. 155:328-336.
29. Farrell MJ, Finkel SE. 2003. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J. Bacteriol. 185:7044-7052.
30. Zinser ER, Schneider D, Blot M, Kolter R. 2003. Bacterial evolution through the selective loss of beneficial genes. Trade-offs in expression involving two loci. Genetics 164:1271-1277.
31. Finkel SE. 2006. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4:113-120.
32. Connell N, Han Z, Moreno F, Kolter R. 1987. An E. coli promoter induced by the cessation of growth. Mol. Microbiol. 1:195-201.
33. Myers CR, Nealson KH. 1988. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240: 1319-1321.
34. Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, Eisen JA, Seshadri R, Ward N, Methe B, Clayton RA, Meyer T, Tsapin A, Scott J, Beanan M, Brinkac L, Daugherty S, DeBoy RT, Dodson RJ, Durkin AS, Haft DH, Kolonay JF, Madupu R, Peterson JD, Umayam LA, White O, Wolf AM, Vamathevan J, Weidman J, Impraim M, Lee K, Berry K, Lee C, Mueller J, Khouri H, Gill J, Utterback TR, McDonald LA, Feldblyum TV, Smith HO, Venter JC, Nealson KH, Fraser CM. 2002. Genome sequence of the dissimilatory metal ionreducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20:1118-1123.
35. Huu NB, Denner EB, Ha DT, Wanner G, Stan-Lotter H. 1999. Marinobacter aquaeolei sp. nov., a halophilic bacterium isolated from a Vietnamese oil-producing well. Int. J. Syst. Bacteriol. 49(Pt 2):367-375.
36. Kleiber M. 1932. Body size and metabolism. Hilgardia 6:315-353.
37. Unisense. 2012. Oxygen sensor user manual. Unisense, Aarhus, Denmark.
38. Herigstad B, Hamilton M, Heersink J. 2001. How to optimize the drop plate method for enumerating bacteria. J. Microbiol. Methods 44:121-129.
39. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675.
40. Ridler TW, Calvard ES. 1978. Picture thresholding using an iterative selection method. IEEE Trans. Syst. Man Cybern. 8:630-632.
41. Gray DR, Yue S, Chueng C, Godfrey W. 2005. Bacterial vitality detected by a novel fluorogenic redox dye using flow cytometry, abstr I-111, p 331. Abstr. 105th Gen. Meet. Am. Soc. Microbiol., Atlanta, GA.
42. Barnett V, Lewis T. 1994. Outliers in statistical data, 3rd ed. Wiley, Chichester, United Kingdom.
43. Kolter R, Siegele DA, Tormo A. 1993. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47:855-874.
44. Sezonov G, Joseleau-Petit D, D'Ari R. 2007. Escherichia coli physiology in Luria-Bertani broth. J. Bacteriol. 189:8746-8749.
45. Kjelleberg S. 1993. Starvation in bacteria. Plenum Press, New York, NY.
46. Janda S, Kotyk A. 1985. Effects of suspension density on microbial metabolic processes. Folia Microbiol. (Praha) 30:465-473.
47. Santruckova H, Straskraba M. 1991. On the relationship between specific respiration activity and microbial biomass in soils. Soil Biol. Biochem. 23:525-532.
48. Aertsen A, Michiels CW. 2004. Stress and how bacteria cope with death and survival. Crit. Rev. Microbiol. 30:263-273.
49. López-Amorós R, Castel S, Comas-Riu J, Vives-Rego J. 1997. Assessment of E. coli and Salmonella viability and starvation by confocal laser microscopy and flow cytometry using rhodamine 123, DiBAC4(3), propidium iodide, and CTC. Cytometry 29:298-305.
50. Petit M, George I, Servais P. 2000. Survival of Escherichia coli in freshwater: beta-D-glucuronidase activity measurements and characterization of cellular states. Can. J. Microbiol. 46:679-684.
51. Oliver JD. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43:93-100.
52. Morita RY. 1997. Bacteria in oligotrophic environments: starvationsurvival lifestyle. Chapman & Hall, New York, NY.
53. Roussel EG, Bonavita MAC, Querellou J, Cragg BA, Webster G, Prieur D, Parkes RJ. 2008. Extending the sub-sea-floor biosphere. Science 320: 1046.
54. D'Hondt S, Jorgensen BB, Miller DJ, Batzke A, Blake R, Cragg BA, Cypionka H, Dickens GR, Ferdelman T, Hinrichs KU, Holm NG, Mitterer R, Spivack A, Wang G, Bekins B, Engelen B, Ford K, Gettemy G, Rutherford SD, Sass H, Skilbeck CG, Aiello IW, Guerin G, House CH, Inagaki F, Meister P, Naehr T, Niitsuma S, Parkes RJ, Schippers A, Smith DC, Teske A, Wiegel J, Padilla CN, Acosta JL. 2004. Distributions of microbial activities in deep subseafloor sediments. Science 306:2216-2221.
55. D'Hondt S, Rutherford S, Spivack AJ. 2002. Metabolic activity of subsurface life in deep-sea sediments. Science 295:2067-2070.
56. D'Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP, Kallmeyer J, Abrams LJ, Smith DC, Graham D, Hasiuk F, Schrum H, Stancin AM. 2009. Subseafloor sedimentary life in the South Pacific Gyre. Proc. Natl. Acad. Sci. U. S. A. 106:11651-11656.
57. Parkes RJ, Cragg BA, Bale SJ, Getlifff JM, Goodman K, Rochelle PA, Fry JC, Weightman AJ, Harvey SM. 1994. Deep bacterial biosphere in Pacific Ocean sediments. Nature 371:410-413.
58. Reimers CE. 1987. An in situ microprofiling instrument for measuring interfacial pore water gradients: methods and oxygen profiles from the North Pacific Ocean. Deep Sea Res. A 34:2019-2035.
59. Berner RA. 1980. Early diagenesis: a theoretical approach. Princeton University Press. Princeton, NJ.
60. Hemmingsen AM. 1960. Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep. Steno Mem. Hosp. Nordisk Insulin Lab. 9:6-110.
61. Agutter PS, Wheatley DN. 2004. Metabolic scaling: consensus or controversy? Theor. Biol. Med. Model. 1:13.
62. Enquist BJ, Allen AP, Brown JH, Gillooly JF, KerkhoffAJ, Niklas KJ, Price CA, West GB. 2007. Biological scaling: does the exception prove the rule? Nature 445:E9-E10; discussion E10-E11.
63. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293:2248-2251.
64. Hochachka PW, Somero GN. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York, NY.
65. Makarieva AM, Gorshkov VG, Li BL. 2005. Energetics of the smallest: do bacteria breathe at the same rate as whales? Proc. Biol. Sci. 272:2219-2224.
66. Makarieva AM, Gorshkov VG, Li BL, Chown SL, Reich PB, Gavrilov VM. 2008. Mean mass-specific metabolic rates are strikingly similar across life's major domains: evidence for life's metabolic optimum. Proc. Natl. Acad. Sci. U. S. A. 105:16994-16999.
67. Prothero J. 1986. Scaling of energy metabolism in unicellular organisms: a reanalysis. Comp. Biochem. Physiol. A Comp. Physiol. 83:243-248.
68. Reich PB, Tjoelker MG, Machado JL, Oleksyn J. 2006. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439:457-461.
69. West GB, Brown JH, Enquist BJ. 1999. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677-1679.
70. Loferer-Krössbacher M, Klima J, Psenner R. 1998. Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl. Environ. Microbiol. 64:688-694.
71. West GB, Brown JH, Enquist BJ. 2000. The origin of universal scaling laws in biology, p 87-112. In Brown JH, West GB (ed), Scaling in biology. Oxford University Press, New York, NY.