Skip to main content

Advertisement

SpringerLink
Log in

Marine Heterotrophic Bacteria in Continuous Culture, the Bacterial Carbon Growth Efficiency, and Mineralization at Excess Substrate and Different Temperatures

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

To model the physiological potential of marine heterotrophic bacteria, their role in the food web, and in the biogeochemical carbon cycle, we need to know their growth efficiency response within a matrix of different temperatures and degrees of organic substrate limitation. In this work, we present one part of this matrix, the carbon growth efficiencies of marine bacteria under different temperatures and nonlimiting organic and inorganic substrate supply. We ran aerobic turbidostats with glucose enriched seawater, inoculated with natural populations of heterotrophic marine bacteria at 10, 14, 18, 22, and 26°C. The average cell-specific growth rates increased with temperature from 1.17 to 2.6 h−1. At steady-state total CO2 production, biomass production [particulate organic carbon (POC) and nitrogen (PON)], and viruslike particle abundance was measured. CO2 production and specific growth rate increased with increasing temperature. Bacterial carbon growth efficiency (BCGE), the particulate carbon produced per dissolved carbon utilized, varied between 0.12 and 0.70. Maximum BCGE values and decreased specific respiration rates occurred at higher temperatures (22 and 26°C) and growth rates. This trend was largely attributable to an increase in POC per cell abundance; when the BCGE was recalculated, parameterizing the biomass as the product of cell concentration and a constant cellular carbon content, the opposite trend was observed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Azam, F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280: 694–696

    Article  CAS  Google Scholar 

  2. Barillier, A, Garnier, J (1993) Influence of temperature and substrate concentration on bacterial growth yield in Seine River Water batch culture. Appl Environ Microbiol 59: 1678–1682

    PubMed  CAS  Google Scholar 

  3. Biddanda, B, 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 

  4. Bjørnsen, P (1986) Bacterioplankton growth yield in continuous seawater cultures. Mar Ecol Prog Ser 30: 191–196

    Google Scholar 

  5. Brophy, JE, Carlson, DJ (1989) Production of biologically refractory dissolved organic carbon by natural seawater microbial populations. Deep-Sea Res 36: 497–507

    Article  CAS  Google Scholar 

  6. Cajal-Medrano, R, Maske, H (1999). Growth efficiency, growth rate and the remineralization of organic substrate by bacterioplankton—revisiting the Pirt model. Aquat Microb Ecol 19: 119–128

    Google Scholar 

  7. Cajal-Medrano, R, Maske, H (2005) Growth efficiency and respiration at different growth rates in glucose-limited chemostats with natural marine bacteria populations. Aquat Microb Ecol 38: 125–133

    Google Scholar 

  8. Christian, RR, Wiebe, WJ (1974) The effects of temperature upon the reproduction and respiration of a marine obligate psychrophile. Can J Microbiol 20: 1341–1345

    Article  Google Scholar 

  9. Daneri, G, Riemann, B, Williams, PJB (1994) In situ bacterial production and growth yield measured by thymidine, leucine and fractionated dark oxygen uptake. J Plankton Res 16: 105–113

    Article  CAS  Google Scholar 

  10. del Giorgio, PA, Duarte, CM (2002) Respiration in the open ocean. Nature 420: 379–384

    Article  PubMed  CAS  Google Scholar 

  11. del Giorgio, PA, Cole, JJ (2000) Bacterial energetics and growth efficiency. In: Kirchman, DL (Ed.) Microbial Ecology of the Oceans, Wiley-Liss, New York, pp 289–325

    Google Scholar 

  12. del Giorgio, PA, Cole, JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29: 503–541

    Article  Google Scholar 

  13. Fakuda, R, Ogama, H, Nagata, T, Koike, I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64: 3352–3358

    Google Scholar 

  14. Fuhrman, JA (1999) Marine viruses and their geochemical and ecological effects. Nature 399: 541–548

    Article  PubMed  CAS  Google Scholar 

  15. Kirchman, DL (1993) Statistical analysis of direct counts of microbial abundance. In: Kemp, PF, Sherr, BF, Sherr, EB, Cole, J (Eds.) Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, pp 117–120

    Google Scholar 

  16. Herbert, RA, Bel, CR (1977) Growth characteristics of an obligately psychrophilic Vibrio sp. Arch Microbiol 113: 220–251

    Article  Google Scholar 

  17. Hernández-Ayón, M, Belli, SL, Zirino, A (1999) pH, alkalinity and total CO2 in costal seawater by potentiometer titration with a difference derivative readout. Anal Chim Acta 394: 101–108

    Article  Google Scholar 

  18. Heissenberger, A, Herndl, GJ (1994) Formation of high molecular weight material by free-living marine bacteria. Mar Ecol Prog Ser 111: 129–135

    Article  CAS  Google Scholar 

  19. Ingraham, J, Maaloe, J, Neidhardt, J (1983) Growth of the Bacterial Cell. Sinauer Associates, Sunderland, MA, p 435

  20. Ingraham, J, Marr, AG (1996) Effect of temperature, pressure, pH, and osmotic stress on growth. In: Neidhardt, FC, Curtiss, R III, Ingraham, JL, Lin, ECC, Brooks Low, K, Magasanik, B, Reznikoff, WS, Riley, M, Schaechter, M, Umbarger, HE (Eds.) Escherichia coli and Salmonella Cellular and Molecular Biology, 2nd ed. American Society for Microbiology, Washington, DC, pp 1570–1578

    Google Scholar 

  21. Karl, DM, Hebel, D, Bjorkman, K, Letelier, RM (1998) The role of dissolved organic matter release in the productivity of the oligotrophic North Pacific. Ocean. Limnol Oceanogr 43: 1270–1286

    Article  CAS  Google Scholar 

  22. Kroer, N (1994) Relationships between biovolume and carbon and nitrogen content of bacterioplankton. FEMS Microbiol Ecol 13: 217–224

    Article  Google Scholar 

  23. Kroer, N (1993) Bacterial growth efficiency on natural dissolved organic matter. Limnol Oceanogr 38: 1282–1290

    Article  CAS  Google Scholar 

  24. Lee, S, Fuhrman, JA (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53: 1298–1303

    PubMed  CAS  Google Scholar 

  25. Maske, H, Garcia-Mendoza, E (1994) Adsorption of dissolved organic matter to the inorganic filter substrate and its implications for 14C uptake measurements. Appl Environ Microbiol 60: 3887–3890

    PubMed  CAS  Google Scholar 

  26. Middelboe, M, Jorgensen, NOG, Kroer, N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfect marine bacterioplankton. Appl Environ Microbiol 62: 1991–1997

    PubMed  CAS  Google Scholar 

  27. Moran, XAG, Gasol, J, Arin, L, Estrada, M (1999) A comparison between glass fiber and membrane filters for the estimation of phytoplankton POC and DOC production. Mar Ecol Progr Ser 187: 31–41

    CAS  Google Scholar 

  28. Nayar, S, Chou, LM (2003) Relative efficiencies of different filters in retaining phytoplankton for pigment and productivity studies. Estuar Coast Shelf Sci 58: 241–248

    Article  CAS  Google Scholar 

  29. Nedwell, DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbial Ecol 30: 101–111

    Article  CAS  Google Scholar 

  30. Neijessel, OM, Teixera de Mattos, JM, Tempest, DW (1996) Growth yield and energy distribution. In: Neidhardth F, Curtiss, R III, Ingraham, JL, Lin, ECC, Brooks Low, K, Magasanik, B, Reznikoff, WS, Riley, M, Schaechter, M, Umbarger, HE (Eds.) Escherichia coli and Salmonella Cellular and Molecular Biology, 2nd edn. ASM Press, Washington DC, pp 1683–1691

    Google Scholar 

  31. Noble, RT, Fuhrman, JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113–118

    Google Scholar 

  32. Pomeroy, L, Wiebe, WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23: 187–204

    Google Scholar 

  33. 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 

  34. Sherr, EB, Sherr, BF (1996) Temporal offset in oceanic production and respiration processes implied by seasonal changes in atmospheric oxygen: the role of heterotrophic microbes. Aquat Microb Ecol 11: 91–100

    Google Scholar 

  35. Shia, FK, Ducklow, HW (1994) Temperature regulation of heterotrophic bacterioplancton abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39: 1243–1250

    Article  Google Scholar 

  36. Strom, SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman, DL (Ed.) Microbial Ecology of the Oceans. Wiley-Liss, New York, pp 351–386

    Google Scholar 

  37. Turley, CM, Hughes, D (1992) Effects of storage on direct estimates of bacterial numbers of preserved seawater samples. Deep-Sea Res 39: 375–394

    Article  Google Scholar 

  38. Vrede, K, Heldal, M, Norland, S, Bratbak, G (2002) Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol 68: 2965–2971

    Article  PubMed  CAS  Google Scholar 

  39. Williams, PJB (2000) Heterotrophic bacteria and dynamics of dissolved organic material. In: Kirchman, DL (Ed.) Microbial Ecology of the Oceans. Wiley-Liss, New York, pp 153–200

    Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. R. Mouriño-Pérez for taking the confocal microscope images. A. Jiménez-Mercado would like to acknowledge a student fellowship from CONACYT. This work was partially financed by UABC 0267 and UABC-CICESE 0247.

Author information

Authors and Affiliations

  1. Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, P.O. Box 453, Ensenada, Baja California, México CP 22880

    Alejandrina Jiménez-Mercado & Ramón Cajal-Medrano

  2. Centro de Investigación Científica y Educación Superior de Ensenada, Ensenada, Mexico

    Helmut Maske

Authors
  1. Alejandrina Jiménez-Mercado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramón Cajal-Medrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helmut Maske
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ramón Cajal-Medrano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiménez-Mercado, A., Cajal-Medrano, R. & Maske, H. Marine Heterotrophic Bacteria in Continuous Culture, the Bacterial Carbon Growth Efficiency, and Mineralization at Excess Substrate and Different Temperatures. Microb Ecol 54, 56–64 (2007). https://doi.org/10.1007/s00248-006-9171-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9171-4

Keywords

Search

Navigation