Skip to main content

Advertisement

SpringerLink
Log in

Environmental Stress Determines the Quality of Bacterial Lysate and Its Utilization Efficiency in a Simple Microbial Loop

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Heterotrophic bacteria provide the critical link in the microbial loop by converting dissolved organic matter (DOM) into particulate form. In this study, DOM was prepared from recently isolated estuarine bacterial strain Vibrio sp. (DSM14379) grown at different salinities [0.2%, 0.5%, 3%, 5%, or 10% (w/v)], washed, concentrated, and lysed by autoclaving. The corresponding lysate-containing media were designated LM0.2, LM0.5, LM3, LM5, and LM10. Vibrio sp. cells grown at different salinities had similar C/N/P ratios, but different C/S ratios, different trace element composition, and different 2D gel electrophoresis protein profiles. Pseudoalteromonas sp. (DSM06238) isolated from a similar environment was able to grow on all lysates, and its biomass production was dependent on lysate type. The highest growth rate and biomass production of Pseudoalteromonas sp. at saturation lysate concentrations were observed in LM3. The biomass production at saturation lysate concentrations was about 3-fold higher as compared to LM0.2 and LM10. The initial respiration rate, intracellular adenosine triphosphate (ATP) levels, and 3H-Leu and 3H-TdR incorporation rates were lowest in LM3. On the other hand, in LM0.2 or LM10 lysates the situation was reversed, the growth rates and biomass production were lowest, whereas 3H-Leu and 3H-TdR incorporation, respiration rates, as well as ATP levels, were highest. These results imply uncoupling of catabolism from growth in either high- or low-salinity lysates. The results also suggest that differences in organic carbon quality generated during Vibrio sp. growth at different NaCl concentrations were propagated through the simple microbial loop, which may have important ecological implications for higher trophic levels that depend on microbial grazing.

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. Amon, RMW, Benner, R (1994) Rapid cycling of high-molecular-weight dissolved organic matter in the ocean. Nature 369: 549–552

    Article  CAS  Google Scholar 

  2. Amon, RMW, Benner, R (1996) Bacterial utilization of different size classes of dissolved organic matter. Limnol Oceanogr 41: 41–51

    Article  CAS  Google Scholar 

  3. Azam, F, Fenchel, T, Field, JG, Gray, JS, Meyer-Reil, L-A, Thingstad, F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257–263

    Google Scholar 

  4. Baumann, P, Schubert, RHW (1984) Vibrionaceae. In: Krieg, NR (Ed.) Bergey’s Manual of Systematic Bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 516–538

    Google Scholar 

  5. Becker, C, Boersma, M (2003) Resource quality effects on life histories of Daphnia. Limnol Oceanogr 48: 700–706

    Article  Google Scholar 

  6. Biddanda, B, Benner, R (1997) Major contribution from mesopelagic plankton to heterotrophic metabolism in the upper ocean. Deep-Sea Res I 44: 2069–2085

    Google Scholar 

  7. Botsford, JL (1990) Analysis of protein expression in response to osmotic stress in Escherichia coli. FEMS Microbiol Lett 72: 355–360

    Article  CAS  Google Scholar 

  8. Brett, MT, Muller-Navarra, DC, Park, S-K (2000) Empirical analysis of the effect of phosphorus limitation on algal food quality for freshwater zooplankton. Limnol Oceanogr 45: 1564–1575

    Article  CAS  Google Scholar 

  9. Burbanck, WD, Eisen, JD (1960) The inadequacy of monobacterially-fed Paramecium aurelia as food for Didinium nasutum. J Protozool 7: 201–206

    Google Scholar 

  10. Corchero, JL, Cubarsi, R, Vila, P, Aris, A, Villaverde, A (2001) Cell lysis in Escherichia coli cultures stimulates growth and biosynthesis of recombinant proteins in surviving cells. Microbiol Res 156: 13–18

    Article  PubMed  CAS  Google Scholar 

  11. Danevčič, T, Rilfors, L, Štrancar, J, Lindblom, G, Stopar, D (2005) Effects of lipid composition on the membrane activity and lipid phase behaviour of Vibrio sp. DSM14379 cells grown at various NaCl concentrations. Biochim Biophys Acta 1712: 1–8

    Article  PubMed  CAS  Google Scholar 

  12. Dawes, EA (1985) Starvation, survival and energy reserves. In: Fletcher, M, Floodgate, GD (Eds.) Bacteria in their Natural Environments. Academic Press, New York, pp 43–80

    Google Scholar 

  13. Duché, O, Trémoulet, F, Namane, A, Labadie, J, The European Listeria Genome Consortium (2002) A proteomic analysis of the salt stress response of Listeria monocytogenes. FEMS Microbiol Lett 215: 183–188

    Article  PubMed  Google Scholar 

  14. Fuhrman, JA, Noble, RT (2000) Causative agents of bacterial mortality and the consequences to marine food webs. In: Bell, CR, Brylinsky, M, Johnson-Green, P (Eds.) Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology, vol. 1. Atlantic Canada Society for Microbial Ecology, Halifax, Canada, pp 145–152

    Google Scholar 

  15. Gnezda-Meijer, K, Mahne, I, Poljšak-Prijatelj, M, Stopar, D (2006) Host physiological status determines phage-like particle distribution in the lysate. FEMS Microbiol Ecol 55: 136–145

    Article  PubMed  CAS  Google Scholar 

  16. Görg, A (1992) Two-dimensional electrophoresis. Nature 349: 545–546

    Article  Google Scholar 

  17. Jones, RH, Flynn, KJ, Anderson, TR (2002) Effect of food quality on carbon and nitrogen growth efficiency in the copepod Acartia tonsa. Mar Ecol Prog Ser 235: 147–156

    Google Scholar 

  18. Jones, RH, Flynn, KJ (2005) Nutritional status and diet composition affect the value of diatoms as copepod prey. Science 307: 1457–1459

    Article  PubMed  CAS  Google Scholar 

  19. Kaye, JZ, Baross, JA (2004) Synchronous effects of temperature, hydrostatic pressure, and salinity on growth, phospholipid profiles, and protein patterns of four Halomonas species isolated from deep-sea hydrothermal-vent and sea surface environments. Appl Environ Microbiol 70: 6220–6229

    Article  PubMed  CAS  Google Scholar 

  20. Klein Breteler, WCM, Koski, M, Rampen, S (2004) Role of essential lipids in copepod nutrition: no evidence for trophic upgrading of food quality by a marine ciliate. Mar Ecol Prog Ser 274: 199–208

    Google Scholar 

  21. Korstad, J, Olsen, Y, Vadstein, O (1989) Life history characteristics of Brachionus plicatilis (rotifera) fed different algae. Hydrobiologia 186–187: 43–50

    Article  Google Scholar 

  22. Koski, M, Breteler, WK, Schogt, N (1998) Effect of food quality on rate of growth and development of the pelagic copepod Pseudocalanus elongatus (Copepoda, Calanoida). Mar Ecol Prog Ser 170: 169–187

    Google Scholar 

  23. Lundin, A, Thore, A (1975) Analytical information obtainable by evaluation of the time course of firefly bioluminescence in the assay of ATP. Anal Biochem 66: 47–63

    Article  PubMed  CAS  Google Scholar 

  24. Mason, CA, Hamer, G (1987) Cryptic growth in Klebsiella pneumoniae. Appl Microbiol Biotechnol 25: 577–584

    CAS  Google Scholar 

  25. Morita, RY (Ed.) (1997) Bacteria in Oligotrophic Environments. Chapman & Hall, New York

  26. Nioh, I, Furusaka, C (1968) Growth of bacteria in the heat-killed suspensions of the same bacteria. J Gen Appl Microbiol 14: 373–385

    Google Scholar 

  27. O’Farrell, PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007–4020

    PubMed  CAS  Google Scholar 

  28. Raubenheimer, D, Zemke-White, WL, Phillips, RJ, Clements, KD (2005) Algal macronutrients and food selection by the omnivorous marine fish Girella tricuspidata. Ecology 86: 2601–2610

    Google Scholar 

  29. Reed, RH (1986) Halotolerant and halophilic microbes. In: Herbert, RA, Codd, GA (Eds.) Microbes in Extreme Environments. Academic Press, New York, pp 55–81

    Google Scholar 

  30. Riemann, B, Bell, R (1990) Advances in estimating bacterial biomass and growth in aquatic systems. Arch Hydrobiol 118: 385–402

    CAS  Google Scholar 

  31. Rodriguez-Valera, F, Ventosa, A, Quesada, E, Ruiz-Berraquero, F (1982) Some physiological features of a Halococcus sp. at low salt concentrations. FEMS Microbiol Lett 15: 249–252

    Article  Google Scholar 

  32. Russell, JB, Cook, GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59: 48–62

    PubMed  CAS  Google Scholar 

  33. Schmidt, K, Jónasdóttir, SH (1997) Nutritional quality of two cyanobacteria: how rich is ‘poor’ food? Mar Ecol Prog Ser 151: 1–10

    Google Scholar 

  34. Shiah, FK, Ducklow, HW (1997) Bacterioplankton growth responses to temperature and chlorophyll variations in estuaries measured by thymidine: leucine incorporation ratio. Aquat Microb Ecol 13: 151–159

    Google Scholar 

  35. Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD, Fujimoto, EK, Goeke, NM, Olson, BJ, Klenk, DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76–85

    Article  PubMed  CAS  Google Scholar 

  36. Smith, DC, Azam, F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microbial Food Webs 6: 107–114

    Google Scholar 

  37. Staley, JT, Konopka, A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39: 321–346

    Article  PubMed  CAS  Google Scholar 

  38. Stopar, D, Černe, A, Zcaronzigman, M, Poljšak-Prijatelj, M, Turk, V (2004) Viral abundance and a high proportion of lysogens suggest that viruses are important members of the microbial community in the Gulf of Trieste. Microb Ecol 47: 1–8

    Article  PubMed  CAS  Google Scholar 

  39. Storz, G, Hengee-Aronis, R (Eds.) (2000) Bacterial Stress Responses. ASM Press, Washington, DC.

  40. Stramer, SL, Starzyk, MJ (1978) Improved growth of Thermus aquaticus on cellular lysates. Microbios 23: 193–198

    PubMed  CAS  Google Scholar 

  41. Sundh, I (1992) Biochemical composition of dissolved organic carbon derived from phytoplankton and used by heterotrophic bacteria. Appl Environ Microbiol 58: 2938–2947

    PubMed  CAS  Google Scholar 

  42. Štupar, J, Dolinšek, F, Simčič, J, Bizjak, M, Budič, B (2005) Trace element analysis of the hair of Duke Mirko Petrovic-Njegos—a possible means of clarification of his death. Trace Elem Electrolytes 22: 118–126

    Google Scholar 

  43. Tempest, DW, Neijssel, OM (1978) Eco-physiological aspects of microbial growth in aerobic nutrient-limited environments. Adv Microb Ecol 2: 105–153

    Google Scholar 

  44. Tempest, DW, Neijssel, OM (1984) The status of Y ATP and maintenance energy as biologically interpretable phenomena. Annu Rev Microbiol 38: 459–486

    Article  PubMed  CAS  Google Scholar 

  45. Twombly, S, Burns, C (1996) Effects of food quality on individual growth and development in the freshwater copepod Boeckella triarticulata. J Plankton Res 18: 2179–2196

    Article  Google Scholar 

  46. Vrede, T, Persson, J, Aronsen, G (2002) The influence of food quality (P : C ratio) on RNA:DNA ratio and somatic growth rate of Daphnia. Limnol Oceanogr 47: 487–494

    Article  CAS  Google Scholar 

  47. Wacker, A, von Elert, E (2004) Food quality controls egg quality of the zebra mussel Dreissena polymorpha: the role of fatty acids. Limnol Oceanogr 49: 1794–1801

    Article  CAS  Google Scholar 

  48. Wacker, A, Becher, P, von Elert, E (2002) Food quality effects of unsaturated fatty acids on larvae of the zebra mussel Dreissena polymorpha. Limnol Oceanogr 47: 1242–1248

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Slovenian Ministry of Higher Education, Science and Technology. We thank Daniel Žlindra from the Slovenian Forestry Institute and Dr. Bojan Budič from the National Institute of Chemistry, Slovenia, for helping with the element analyses, as well as Dr. Polona Jamnik and Aleš Goznik for their help with 2D electrophoresis.

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, 1000, Ljubljana, Slovenia

    Duško Odić & David Stopar

  2. Marine Biology Station Piran, National Institute of Biology, Fornače 41, 6330, Piran, Slovenia

    Valentina Turk

Authors
  1. Duško Odić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valentina Turk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Stopar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Stopar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Odić, D., Turk, V. & Stopar, D. Environmental Stress Determines the Quality of Bacterial Lysate and Its Utilization Efficiency in a Simple Microbial Loop. Microb Ecol 53, 639–649 (2007). https://doi.org/10.1007/s00248-006-9143-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9143-8

Keywords

Search

Navigation