Skip to main content
SpringerLink
Log in

Network Relationships of Bacteria in a Stable Mixed Culture

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We investigated the network relationships of bacteria in a structurally stable mixed culture degrading cellulose. The mixed culture consists of four bacterial strains (a cellulose-degrading anaerobe [strain S], a saccharide-utilizing anaerobe [strain F], a peptide- and acetate-utilizing aerobe [strain 3] and a peptide-, glucose-, and ethanol-utilizing aerobe [strain 5]). Interspecies interactions were examined by analyzing the effects of culture filtrates on the growth of the other strains and by comprehensively analyzing population dynamics in the mixed-culture systems with all possible combinations of the four bacterial strains. The persistence of strain S depends on the effects of strain 5. However, strain 5 is a disadvantaged strain because strain 3 has bacteriocidal activity on strain 5. The extinction of strain 5 is indirectly prevented by strain F that suppresses the growth of strain 3. Although strain F directly has suppressive effects on the growth of strain S, strain F is essential for the persistence of strain S, considering the indirect effects (maintaining strain 5, which is essential for the survival of strain S, by inhibiting strain 3). These indirect relationships form a bacterial network in which all the relationships including suppressive effects were well balanced to maintain the structural stability. In addition to direct metabolite interactions, such kind of indirect relationships could have a great impact on microbial community structure in the natural environment.

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

Similar content being viewed by others

References

  1. Alexander M (1997) Microbial communities and interactions: a prelude. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. ASM, Washington, DC, pp 5–13

    Google Scholar 

  2. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245–1248

    Article  PubMed  CAS  Google Scholar 

  3. Bohannan BJM, Lenski RE (2000) The relative importance of competition and predation varies with productivity in a model community. Am Nat 156:329–340

    Article  Google Scholar 

  4. Briones A, Raskin L (2003) Diversity and dynamics of microbial communities in engineered environments and their implications for process stability. Curr Opin Biotechnol 14:270–276

    Article  PubMed  CAS  Google Scholar 

  5. Bruns A, Cypionka H, Overmann J (2002) Cyclic AMP and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. Appl Environ Microbiol 68:3978–3987

    Article  PubMed  CAS  Google Scholar 

  6. Bruns A, Nubel U, Cypionka H, Overmann J (2003) Effect of signal compounds and incubation conditions on the culturability of freshwater bacterioplankton. Appl Environ Microbiol 69:1980–1989

    Article  PubMed  CAS  Google Scholar 

  7. von Canstein HF, Li Y, Felske A, Wagner-Döbler I (2001) Long-term stability of mercury reducing microbial biofilm communities analyzed by 16S-23S rDNA interspacer region polymorphism. Microb Ecol 42:624–634

    Article  PubMed  Google Scholar 

  8. Cui ZJ, Li MD, Piao Z, Huang ZY, Ishii M, Igarashi Y (2002) Selection of a composite microbial system MC1 with efficient and stability cellulose degradation bacteria and its function. Environ Sci 23:36–39

    CAS  Google Scholar 

  9. Dollhopf SL, Pariseau ML, Hashsham SA, Tiedje JM (2003) Competitive and cooperative interactions affecting a fermentative spirochete in anaerobic chemostats. Microb Ecol 46:1–11

    Article  PubMed  CAS  Google Scholar 

  10. Fernández A, Huang S, Seston S, Xing J, Hickey R, Criddle C, Tiedje J (1999) How stable is stable? Function versus community composition. Appl Environ Microbiol 65:3697–3704

    PubMed  Google Scholar 

  11. Fernández AS, Hashsham SA, Dollhope SL, Raskin L, Glagoleva O, Dazzo FB, Hickey RF, Criddle CS, Tiedje JM (2000) Flexible community structure correlates with stable community function in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66:4058–4067

    Article  PubMed  Google Scholar 

  12. Graber JR, Breznak JA (2005) Folate cross-feeding supports symbiotic homoacetogenic spirochetes. Appl Environ Microbiol 71:1883–1889

    Article  PubMed  CAS  Google Scholar 

  13. Grenier D, Mayrand D (1986) Nutritional relationships between oral bacteria. Infect Immun 53:616–620

    PubMed  CAS  Google Scholar 

  14. Guan LL, Onuki H, Kamino K (2000) Bacterial growth stimulation with exogenous siderophore and synthetic N-acyl homoserine lactone autoinducers under iron-limited and low-nutrient conditions. Appl Environ Microbiol 66:2797–2803

    Article  PubMed  CAS  Google Scholar 

  15. Haruta S, Cui Z, Huang Z, Li M, Ishii M, Igarashi Y (2002) Construction of a stable microbial community with high cellulose-degradation ability. Appl Microbiol Biotechnol 59:529–534

    Article  PubMed  CAS  Google Scholar 

  16. Hashsham SA, Fernandez AS, Dollhopf SL, Dazzo FB, Hickey RF, Tiedje JM, Criddle CS (2000) Parallel processing of substrate correlates with greater functional stability in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66:4050–4057

    Article  PubMed  CAS  Google Scholar 

  17. Hobley L, King JR, Sockett RE (2006) Bdellovibrio predation in the presence of decoys: three-way bacterial interactions revealed by mathematical and experimental analyses. Appl Environ Microbiol 72:6757–6765

    Article  PubMed  CAS  Google Scholar 

  18. Holdeman LV, Cato EP, Moore WEC (1977) Anaerobe laboratory manual, 4th edn. Anaerobe Laboratory, Virginia Polytechnic Institute and State University, Blacksburg, VA

    Google Scholar 

  19. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62

    Article  PubMed  CAS  Google Scholar 

  20. Kato S, Haruta S, Cui ZJ, Ishii M, Igarashi Y (2004) Effective cellulose degradation by a mixed-culture system composed of a cellulolytic Clostridium and aerobic non-cellulolytic bacteria. FEMS Microbiol Ecol 51:133–142

    Article  PubMed  CAS  Google Scholar 

  21. Kato S, Haruta S, Cui ZJ, Ishii M, Yokota A, Igarashi Y (2004) Clostridium straminisolvens sp. nov., a moderately thermophilic, aerotolerant and cellulolytic bacterium isolated from a cellulose-degrading bacterial community. Int J Syst Evol Microbiol 54:2043–2047

    Article  PubMed  Google Scholar 

  22. Kato S, Haruta S, Cui ZJ, Ishii M, Igarashi Y (2005) Stable coexistence of five bacterial strains as a cellulose-degrading community. Appl Environ Microbiol 71:7099–7106

    Article  PubMed  CAS  Google Scholar 

  23. Kerr B, Riley MA, Feldman MW, Bohannan BJM (2002) Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418:171174

    Article  Google Scholar 

  24. Leibold MA, Chase JM, Shurin JB, Downing AL (1997) Species turnover and the regulation of trophic structure. Annu Rev Ecol Syst 28:467–494

    Article  Google Scholar 

  25. Maniatis T, Fritsch EF, Sambrook J (eds) (1982) In: Molecular cloning. 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

  26. McCann KS (2000) The diversity–stability debate. Nature 405:228–233

    Article  PubMed  CAS  Google Scholar 

  27. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74

    Article  Google Scholar 

  28. Saddler JN, Chan MKH (1982) Optimization of Clostridium thermocellum growth on cellulose and pretreated wood substrates. Appl Microbiol Biotechnol 16:99–104

    Article  CAS  Google Scholar 

  29. Saikaly PE, Oerther DB (2004) Bacterial competition in activated sludge: theoretical analysis of varying solid retention times on diversity. Microb Ecol 48:274–284

    Article  PubMed  Google Scholar 

  30. Slechta ES, Mulvey MA (2006) Contact-dependent inhibition: bacterial brakes and secret handshakes. Trends Microbiol 14:58–60

    Article  PubMed  CAS  Google Scholar 

  31. Smith NR, Yu Z, Mohn WW (2003) Stability of the bacterial community in a pulp mill effluent treatment system during normal operation and a system shutdown. Water Res 37:4873–4884

    Article  PubMed  CAS  Google Scholar 

  32. Sorensen SR, Ronen Z, Aamand J (2002) Growth in coculture stimulates metabolism of the phenylurea herbicide isoproturon by Sphingomonas sp. strain SRS2. Appl Environ Microbiol 68:3478–3485

    Article  PubMed  CAS  Google Scholar 

  33. Taillisz P, Girard H, Millet J, Beguin P (1989) Enhanced cellulose fermentation by an asporogenous and ethanol-tolerant mutant of Clostridium thermocellum. Appl Environ Microbiol 55:207–211

    Google Scholar 

  34. Tait K, Sutherland IW (2002) Antagonistic interactions amongst bacteriocin-producing enteric bacteria in dual species biofilms. J Appl Microbiol 93:345–352

    Article  PubMed  CAS  Google Scholar 

  35. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466

    Article  Google Scholar 

  36. Zhu H, Qu F, Zhu LH (1993) Isolation of genomic DNAs from plants, fungi and bacteria using benzyl chloride. Nucleic Acids Res 21:5278–5280

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Masanori Arita for valuable discussions and encouragement.

Author information

Author notes

  1. Souichiro Kato

    Present address: Laboratory of Applied Microbiology, Marine Biotechnology Institute, 3-75-1 Heita, Kamaishi, Iwate, 026-0001, Japan

  2. Shin Haruta

    Present address: Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, 1-1 Minami-Osawa, Hachioji, Tokyo, 192-0397, Japan

Authors and Affiliations

  1. Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo, 113-8657, Japan

    Souichiro Kato, Shin Haruta, Masaharu Ishii & Yasuo Igarashi

  2. College of Agronomy and Biotechnology, China Agricultural University, Yuanmingyuan Xilu, Haidian-Qu, Beijing, 100094, People’s Republic of China

    Zong Jun Cui

Authors
  1. Souichiro Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shin Haruta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zong Jun Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masaharu Ishii
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasuo Igarashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shin Haruta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kato, S., Haruta, S., Cui, Z.J. et al. Network Relationships of Bacteria in a Stable Mixed Culture. Microb Ecol 56, 403–411 (2008). https://doi.org/10.1007/s00248-007-9357-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-007-9357-4

Keywords

Search

Navigation