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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Aiyar, SE, Gaal, T, Gourse, RL (2002) rRNA promoter activity in the fast-growing bacterium Vibrio natriegens. J Bacteriol 184: 1349–1358
APHA (1992) Standard Methods for the Examination of Water And Wastewater, APHA, Washington, DC
Bakermans, C, Nealson, KH (2004) Relationship of critical temperature to macromolecular synthesis and growth yield in Psychrobacter cryopegella. J Bacteriol 186: 2340–2345
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
Cotner, JB, Ammerman, JA, Peele, ER, Bentzen, E (1997) Phosphorus limited bacterioplankton growth in the Sargasso Sea. Aquat Microb Ecol 13: 141–149
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
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
Dobberfuhl, DR, Elser, JJ (2000) Elemental stoichiometry of lower food web components in arctic and temperate lakes. J Plankton Res 22: 1341–1354
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
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
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
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
Farewell, A, Neidhardt, FC (1998) Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J Bacteriol 180: 4704–4710
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
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
Gillooly, JF, Brown, JH, West, GB, Savage, VM, Charnov, EL (2001) Effects of size and temperature on metabolic rate. Science 293: 2248–2251
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
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
Hanegraaf, PPF, Muller, EB (2001) The dynamics of the macromolecular composition of biomass. J Theor Biol 212: 237–251
Hobbie, JE, Daley, RJ, Jasper, S (1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33: 1225–1228
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
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
Klausmeier, CA, Litchman, E, Daufresne, T, Levin, SA (2004) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 171–174
Koch, AL (1971) The adaptive responses of Escherichia coli to a feast and famine existence. Adv Microbial Physiol 6: 147–217
Koch, AL (1996) What size should a bacterium be? A question of scale. Annu Rev Microbiol 50: 317–348
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
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
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
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
Marr, AG (1991) Growth rate of Escherichia coli. Microbiol Rev 55: 316–333
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
Neidhardt, FC, Ingraham, JL, Schaechter, M (1990) Physiology of the Bacterial Cell: A Molecular Approach. Sinauer, Sunderland, pp 506
Phillips, LE, Humphrey, TJ, Lappin-Scott, HM (1998) Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J Appl Microbiol 84: 820–826
Reich, PB, Oleksyn, J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS 101: 11001–11006
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
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
Rivkin, RB, Legendre, L (2001) Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291: 2398–2400
Ryals, J, Little, R, Bremer, H (1982) Temperature dependence of RNA synthesis parameters in Escherichia coli. J Bacteriol 151(2): 879–887
Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213
Sterner, RW, Elser, JJ (2002) Ecological Stoichiometry. The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton
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
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
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
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
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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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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