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Temperature Affects Stoichiometry and Biochemical Composition of Escherichia coli

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Abstract

Temperature is a master variable controlling biochemical processes in organisms, and its effects are manifested on many organizational levels in organisms and ecosystems. We examined the effects of temperature on the biochemical composition and stoichiometry of a model heterotrophic bacterium, Escherichia coli K-12, held at constant growth rate in chemostats. Increasing temperature led to increased cellular organic carbon (C) and organic nitrogen (N) with decreased phosphorus (P) content, leading to increased C/P and N/P biomass ratios. P content was related to cellular RNA, which is P-rich (9–10% by weight) and nonnucleic acid P (presumably composed of mostly phospholipids, intracellular phosphate, and polyphosphate). These results indicate that E. coli allocates an increased proportion of its P cell quota toward assembly (ribosomes) at low temperatures and an increasing proportion toward resource acquisition machinery (membranes) at higher temperatures. If these results are relevant to the behavior of prokaryotic heterotrophs in natural settings (the gut, soils, lakes, oceans, etc.), it suggests greater nutrient regeneration and less microbial nutrient retention as temperatures increase.

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References

  1. Aiyar, SE, Gaal, T, Gourse, RL (2002) rRNA promoter activity in the fast-growing bacterium Vibrio natriegens. J Bacteriol 184: 1349–1358

    Article  PubMed  CAS  Google Scholar 

  2. APHA (1992) Standard Methods for the Examination of Water And Wastewater, APHA, Washington, DC

    Google Scholar 

  3. Bakermans, C, Nealson, KH (2004) Relationship of critical temperature to macromolecular synthesis and growth yield in Psychrobacter cryopegella. J Bacteriol 186: 2340–2345

    Article  PubMed  CAS  Google Scholar 

  4. Biddanda, BA, Cotner, JB (2002) Love handles in aquatic ecosystems: the role of dissolved organic carbon drawdown, resuspended sediments, and terrigenous inputs in the carbon balance of Lake Michigan. Ecosystems 5: 431–445

    Article  CAS  Google Scholar 

  5. Cotner, JB, Ammerman, JA, Peele, ER, Bentzen, E (1997) Phosphorus limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13: 141–149

    Article  Google Scholar 

  6. Cotner, JB, Biddanda, BA (2002) Small players, large role: microbial influence on auto-heterotrophic coupling and biogeochemical processes in aquatic ecosystems. Ecosystems 5: 105–121

    Article  CAS  Google Scholar 

  7. Dicks, JW, Tempest, DW (1966) The influence of temperature and growth rate on the quantitative relationship between potassium, magnesium, phosphorus and ribonucleic acid of Aerobacter aerogenes growing in a chemostat. J Gen Microbiol 45

  8. Dobberfuhl, DR, Elser, JJ (2000) Elemental stoichiometry of lower food web components in arctic and temperate lakes. J Plankton Res 22: 1341–1354

    Article  CAS  Google Scholar 

  9. Elser, JJ, Dobberfuhl, DR, MacKay, NA, Schampel, JH (1996) Organism size, life history, and N:P stoichiometry: toward a unified view of cellular and ecosystem processes. Bioscience 46: 674–684

    Article  Google Scholar 

  10. Elser, JJ, Sterner, RW, Gorokhova, E, Fagan, WF, Markow, TA, Cotner, JB, Harrison, JF, Hobbie, SE, Odell, GM, Weider, LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550

    Article  Google Scholar 

  11. Elser, JJ, Acharya, K, Kyle, M, Cotner, J, Makino, W, Markow, TA, Watts, T, Hobbie, S, Fagan, WF, Schade, J, Sterner, RW (2003) General conditions for coupling of growth–RNA–phosphorus stoichiometry in diverse biota. Ecol Lett 6: 936–943

    Article  Google Scholar 

  12. Evans, CGT (1976) The concept of relative growth rate. In: Dean, ACR, Ellwood, DC, Evans, CGT, Melling, J (Eds.) Continuous Culture 6: Applications and New Fields, Wiley, London, pp 346–348

    Google Scholar 

  13. Farewell, A, Neidhardt, FC (1998) Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J Bacteriol 180: 4704–4710

    PubMed  CAS  Google Scholar 

  14. Fujioka, R, Sian-Denton, C, Borja, M, Castro, J, Morphew, K (1999) Soil: the environmental source of Escherichia coli and enterococci in Guam's streams. J Appl Microbiol 85: 83s–89s

    Google Scholar 

  15. Gausing, K (1977) Regulation of ribosome production in Escherichia coli: synthesis and stability of ribosomal RNA and of ribosomal protein messenger RNA at different growth rates. J Mol Biol 115: 335–354

    Article  PubMed  CAS  Google Scholar 

  16. Gillooly, JF, Brown, JH, West, GB, Savage, VM, Charnov, EL (2001) Effects of size and temperature on metabolic rate. Science 293: 2248–2251

    Article  PubMed  CAS  Google Scholar 

  17. Gorokhova, E, Kyle, M (2002) Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA–DNA content. J Plankton Res 24: 511–522

    Article  CAS  Google Scholar 

  18. Grover, JP (2000) Resource competition and community structure in aquatic microorganisms: experimental studies of algae and bacteria along a gradient of organic carbon to inorganic phosphorus supply. J Plankton Res 22: 1591–1610

    Article  CAS  Google Scholar 

  19. Hanegraaf, PPF, Muller, EB (2001) The dynamics of the macromolecular composition of biomass. J Theor Biol 212: 237–251

    Article  PubMed  CAS  Google Scholar 

  20. Hobbie, JE, Daley, RJ, Jasper, S (1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33: 1225–1228

    PubMed  CAS  Google Scholar 

  21. Ingraham, JL, Marr, AG (1996) Effect of temperature, pressure, pH and osmotic stress on growth. In: Neidhardt, FC (Ed.) Escherichia coli and Salmonella: Cellular and Molecular Biology, ASM Press, Washington, DC, pp 1570–1578

    Google Scholar 

  22. Katterer, T, Andren, O (2001) The ICBM family of analytically solved models of soil carbon, nitrogen and microbial biomass dynamics descriptions and application examples. Ecol Model 136: 191–207

    Article  CAS  Google Scholar 

  23. Klausmeier, CA, Litchman, E, Daufresne, T, Levin, SA (2004) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 171–174

    Article  PubMed  CAS  Google Scholar 

  24. Koch, AL (1971) The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microbial Physiol 6: 147–217

    Article  CAS  Google Scholar 

  25. Koch, AL (1996) What size should a bacterium be? A question of scale. Annu Rev Microbiol 50: 317–348

    Article  PubMed  CAS  Google Scholar 

  26. Lee, SH, Kemp, PF (1994) Single-cell RNA content of natural marine planktonic bacteria measured by hybridization with multiple 16S rRNA-targeted fluorescent probes. Limnol Oceanogr 39: 869–879

    Article  CAS  Google Scholar 

  27. Maaløe, O, Kjeldgaard, NO (1966) Control of Macromolecular Synthesis: A Study of DNA, RNA, and Protein Synthesis in Bacteria. W.A. Benjamin, New York, pp 284

    Google Scholar 

  28. Makino, W, Cotner, JB, Sterner, RW, Elser, J (2003) Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C:N:P stoichiometry. Funct Ecol 17: 121–130

    Article  Google Scholar 

  29. Makino, W, Cotner, JB (2004) Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth- and resource-dependent variations. Aquat Microb Ecol 34: 33–41

    Article  Google Scholar 

  30. Marr, AG (1991) Growth rate of Escherichia coli. Microbiol Rev 55: 316–333

    PubMed  CAS  Google Scholar 

  31. Martinez, MB, Flickinger, MC, Nelsestuen, GL (1999) Steady-state enzyme kinetics in the Escherichia coli periplasm: a model of a whole cell biocatalyst. J Biotechnol 71: 59–66

    Article  PubMed  CAS  Google Scholar 

  32. Neidhardt, FC, Ingraham, JL, Schaechter, M (1990) Physiology of the Bacterial Cell: A Molecular Approach. Sinauer, Sunderland, pp 506

    Google Scholar 

  33. Phillips, LE, Humphrey, TJ, Lappin-Scott, HM (1998) Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J Appl Microbiol 84: 820–826

    Article  PubMed  CAS  Google Scholar 

  34. Reich, PB, Oleksyn, J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS 101: 11001–11006

    Article  PubMed  CAS  Google Scholar 

  35. Rhee, G, Gotham, I (1981) The effect of environmental factors on phytoplankton growth: temperature and the interactions of temperature with nutrient limitation. Limnol Oceanogr 26: 635–648

    Article  CAS  Google Scholar 

  36. Rhee, G, Gotham, IJ (1981) The effect of environmental factors on phytoplankton growth: light and the interactions of light with nitrate limitation. Limnol Oceanogr 26: 649–659

    CAS  Google Scholar 

  37. Rivkin, RB, Legendre, L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291: 2398–2400

    Article  PubMed  CAS  Google Scholar 

  38. Ryals, J, Little, R, Bremer, H (1982) Temperature dependence of RNA synthesis parameters in Escherichia coli. J Bacteriol 151(2): 879–887

    PubMed  CAS  Google Scholar 

  39. Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213

    Article  CAS  Google Scholar 

  40. Sterner, RW, Elser, JJ (2002) Ecological Stoichiometry. The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton

    Google Scholar 

  41. Volfova, O, Zizka, Z, Anderova, M (1993) Effect of temperature on the physiology and cytology of the methylotrophic yeast Candida boidinii growing in methanol-limited chemostat. Folia Microbiol 38: 288–294

    Article  CAS  Google Scholar 

  42. Wagner, MM, Campbell, RG, Boudreau, CA, Durbin, EG (2001) Nucleic acids and growth of Calanus finmarchicus in the laboratory under different food and temperature conditions. Mar Ecol-Prog Ser 221: 185–197

    Article  CAS  Google Scholar 

  43. Woods, HA, Makino, W, Cotner, JB, Hobbie, SE, Harrison, JF, Acharya, K, Elser, JJ (2003) Temperature and the chemical composition of poikilothermic organisms. Funct Ecol 17: 237–245

    Article  Google Scholar 

  44. Yun, HS, Hong, J, Lim, HC (1996) Regulation of ribosome synthesis in Escherichia coli: effects of temperature and dilution rate changes. Biotechnol Bioeng 52: 615–624

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the US-NSF (DEB-9977047 and OCE-9416614), and NOAA (46290000). Ed Hall and Ted Stets provided comments on a previous version of this manuscript.

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Correspondence to James B. Cotner.

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Cotner, J.B., Makino, W. & Biddanda, B.A. Temperature Affects Stoichiometry and Biochemical Composition of Escherichia coli . Microb Ecol 52, 26–33 (2006). https://doi.org/10.1007/s00248-006-9040-1

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  • DOI: https://doi.org/10.1007/s00248-006-9040-1

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