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Competitive and Cooperative Interactions Affecting a Fermentative Spirochete in Anaerobic Chemostats

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Abstract

Terminal restriction fragment length polymorphism and fluorescent in situ hybridization revealed that spirochete-related populations dominated two glucose-fed methanogenic bioreactor communities at dilution rates of 0.06, 0.13, and 0.17 day−1. At dilution rates of 0.25 and 0.50 day−1, spirochete-related populations decreased while Clostridium-related populations increased. Isolates representing both dominant populations were obtained (Treponema R8 and Clostridium S9) and competed against each other in continuous culture. Treponema R8 outcompeted Clostridium S9 at all dilution rates applied (0.17 to 1.0 day−1) when sufficient pantothenate was supplied in the medium. Without sufficient pantothenate, the population size of Treponema R8 was limited to 40% of the total cells. Coculture of Treponema R8 with Methanobacterium bryantii increased the cell yield of Treponema R8 and relieved the pantothenate requirement. Triculture of Treponema R8, Clostridium S9, and M. bryantii in pantothenate-deficient medium allowed Treponema R8 to outcompete Clostridium S9 in continuous culture up to a dilution rate of 0.50 day−1. These experiments demonstrate that cofactor and vitamin requirements can affect the competitive success of a microbial species.

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References

  1. E Canale-Parola (1977) ArticleTitlePhysiology and evolution of spirochetes. Bact Rev 41 181–204 Occurrence Handle1:CAS:528:DyaE2sXktVajtLg%3D Occurrence Handle324466

    CAS  PubMed  Google Scholar 

  2. E Canale-Parola (1992) Free-living sacchrolytic spirochetes: The genus Spirochaeta. A Balows HG Truper M Dworkin K Schleifer (Eds) The Prokaryotes, A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, vol 2 Springer-Verlag New York 3524–3536

    Google Scholar 

  3. C Delbes R Moletta J Godon (2001) ArticleTitleBacterial and archaeal 16S rDNA and 16S rRNA dynamics during an acetate crisis in an anaerobic digester ecosystem. FEMS Microbiol Ecol 35 19–26 Occurrence Handle1:CAS:528:DC%2BD3MXhvVagsrg%3D Occurrence Handle11248386

    CAS  PubMed  Google Scholar 

  4. HJ Doddema GD Vogels (1978) ArticleTitleImproved identification of methanogenic bacteria by fluorescence microscopy. Appl Environ Microbiol 36 752–754 Occurrence Handle1:STN:280:CSaD1c7jvFI%3D Occurrence Handle103504

    CAS  PubMed  Google Scholar 

  5. SL Dollhopf SA Hashsham FB Dazzo RF Hickey CS Criddle JM Tiedje (2001) ArticleTitleThe impact of fermentative organisms on carbon flow in methanogenic systems under constant low substrate conditions. Appl Microbiol Biotechnol 56 531–538 Occurrence Handle1:CAS:528:DC%2BD3MXmsFKgs78%3D Occurrence Handle11549033

    CAS  PubMed  Google Scholar 

  6. SL Dollhopf SA Hashsham JM Tiedje (2002) ArticleTitleInterpreting 16S rDNA T-RFLP data: Application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microb Ecol 42 495–505

    Google Scholar 

  7. A Fernandez S Hashsham SL Dollhopf L Raskin O Glagoleva FB Dazzo RF Hickey C Criddle JM Tiedje (2000) ArticleTitleFlexible community structure correlates with stable community function in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66 4058–4067 Occurrence Handle1:CAS:528:DC%2BD3cXmsVajsb0%3D Occurrence Handle10966429

    CAS  PubMed  Google Scholar 

  8. A Fernandez S Huang S Seston J Xing RF Hickey C Criddle JM Tiedje (1999) ArticleTitleHow stable is stable? Function vs community stability. Appl Environ Microbiol 65 3697–3704 Occurrence Handle1:CAS:528:DyaK1MXltVOltL8%3D Occurrence Handle10427068

    CAS  PubMed  Google Scholar 

  9. BM Fuchs FO Glockner J Wulf R Amann (2000) ArticleTitleUnlabeled helper oligonucleotides increase the in situ accessibility to 16S rRNA of fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 66 2603–3607

    Google Scholar 

  10. JC Gottschal (1993) ArticleTitleGrowth kinetics and competition—some contemporary comments. Antonie van Leeuwenhoek 63 299–313 Occurrence Handle1:STN:280:ByuC3cnps1M%3D Occurrence Handle8279826

    CAS  PubMed  Google Scholar 

  11. W Harder L Dijkhuizen (1983) ArticleTitlePhysiological response to nutrient limitation. Annu Rev Microbiol 37 1–23 Occurrence Handle1:CAS:528:DyaL2cXjtV2r Occurrence Handle6357049

    CAS  PubMed  Google Scholar 

  12. S Hashsham A Fernandez SL Dollhopf FB Dazzo RF Hickey JM Tiedje C Criddle (2000) ArticleTitleParallel processing of substrate correlates with greater functional stability in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66 4050–4057 Occurrence Handle10.1128/AEM.66.9.4050-4057.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVajsbw%3D Occurrence Handle10966428

    Article  CAS  PubMed  Google Scholar 

  13. RB Hespell E Canale-Parola (1973) ArticleTitleGlucose and pyruvate metabolism of Spirochaeta litoralis, an anaerobic marine spirochete. J Bacteriol 116 931–937 Occurrence Handle1:CAS:528:DyaE2cXht1eisg%3D%3D Occurrence Handle4745435

    CAS  PubMed  Google Scholar 

  14. JE Hobbie RJ Daley S Jasper (1977) ArticleTitleUse of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33 1225–1228 Occurrence Handle1:STN:280:CSiB38%2FjvVE%3D Occurrence Handle327932

    CAS  PubMed  Google Scholar 

  15. S Jackowski CO Rock (1981) ArticleTitleRegulation of coenzyme A biosynthesis. J Bacteriol 148 926–932

    Google Scholar 

  16. S Jackowski CO Rock (1986) ArticleTitleConsequences of reduced intracellular coenzyme A content in Escherichia coll. J Bacteriol 166 866–871 Occurrence Handle1:CAS:528:DyaL28Xktl2js7o%3D Occurrence Handle3519582

    CAS  PubMed  Google Scholar 

  17. HW Jannasch (1967) ArticleTitleEnrichments of aquatic bacteria in continuous culture. Arch Microbiol 59 165–173 Occurrence Handle1:STN:280:CCaD3s3mslM%3D

    CAS  Google Scholar 

  18. JR Leadbetter TM Schmidt JR Graber JA Breznak (1999) ArticleTitleAcetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 283 686–689 Occurrence Handle10.1126/science.283.5402.686 Occurrence Handle1:CAS:528:DyaK1MXot1yhtw%3D%3D Occurrence Handle9924028

    Article  CAS  PubMed  Google Scholar 

  19. FE Loeffler KM Ritalahti JM Tiedje (1997) ArticleTitleDechlorination of chloroethenes is inhibited by 2-bromoethanesulfonate in the absence of methanogens. Appl Environ Microbiol 63 4982–4985

    Google Scholar 

  20. A Matin H Veldkamp (1978) ArticleTitlePhysiological basis of the selective advantage of a Spirillum sp. in a carbon-limited environment. J Gen Microbiol 105 187–197 Occurrence Handle1:CAS:528:DyaE1cXksFKgsbw%3D Occurrence Handle641523

    CAS  PubMed  Google Scholar 

  21. FH Mikx (1997) ArticleTitleEnvironmental effects on the growth and proteolysis of Treponema denticola ATCC 33520. Oral Microbiol Immunol 12 249–253 Occurrence Handle1:CAS:528:DyaK2sXls1Wks7k%3D Occurrence Handle9467395

    CAS  PubMed  Google Scholar 

  22. FH Mikx F Jacobs C Satumalay (1992) ArticleTitleCell-bound peptidase activities of Treponema denticola ATCC 33520 in continuous culture. J Gen Microbiol 138 1837–1842 Occurrence Handle1:CAS:528:DyaK3sXjsFKjsw%3D%3D Occurrence Handle1402787

    CAS  PubMed  Google Scholar 

  23. N Pfennig S Wagener (1986) ArticleTitleAn improved method of perparing wet mounts for photomicrographs of microorganisms. J Microbiol Methods 4 303–306 Occurrence Handle10.1016/0167-7012(86)90043-6

    Article  Google Scholar 

  24. M Pohlschroeder SB Leschine E Canale-Parola (1994) ArticleTitle Spirochaeta caldaria sp. nov., a thermophilic bacterium that enhances cellulose degradation by Clostridium thermocellum. Arch Microbiol 161 17–24 Occurrence Handle1:CAS:528:DyaK2cXltVShtg%3D%3D

    CAS  Google Scholar 

  25. H Sahm L Eggeling (1999) ArticleTitle d-Pantothenate synthesis in Corynebacterium glutamicum and use of panBC and genes encoding l-valine synthesis for d-pantothenate overproduction. Appl Environ Microbiol 65 1973–1979 Occurrence Handle1:CAS:528:DyaK1MXjtVams70%3D Occurrence Handle10223988

    CAS  PubMed  Google Scholar 

  26. B Schink (1997) ArticleTitleEnergetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61 262–280 Occurrence Handle1:CAS:528:DyaK2sXktFGqtb8%3D Occurrence Handle9184013

    CAS  PubMed  Google Scholar 

  27. DR Shelton JM Tiedje (1984) ArticleTitleIsolation and partial characterization of bacteria in an anaerobic consortium that mineralizes 3-chlorobenzoic acid. Appl Environ Microbiol 48 840–848 Occurrence Handle1:CAS:528:DyaL2cXmtFKjtbc%3D

    CAS  Google Scholar 

  28. J Snaidr R Amann I Huber W Ludwig KH Schleifer (1997) ArticleTitlePhylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63 2884–2896 Occurrence Handle1:CAS:528:DyaK2sXktlekt7Y%3D Occurrence Handle9212435

    CAS  PubMed  Google Scholar 

  29. O Strunk W Ludwig (1997) ARB: Software for phylogenetic analysis. Technical University of Munich Munich, Germany

    Google Scholar 

  30. JS Terracciano E Canale Parola (1984) ArticleTitleEnhancement of chemotaxis in Spirochaeta aurantia grown under conditions of nutrient limitation. J Bacteriol 159 173–178 Occurrence Handle1:CAS:528:DyaL2cXks12isLk%3D Occurrence Handle6735977

    CAS  PubMed  Google Scholar 

  31. H Veldkamp (1977) ArticleTitleEcological studies with the chemostat. Adv Microb Ecol 1 59–94 Occurrence Handle1:CAS:528:DyaE1cXhvVKrug%3D%3D

    CAS  Google Scholar 

  32. J Xing C Criddle R Hickey (1997) ArticleTitleLong-term adaptive shifts in anaerobic community structure in response to a sustained cyclic substrate perturbation. Microb Ecol 33 50–58 Occurrence Handle9039765

    PubMed  Google Scholar 

Download references

Acknowledgements

SLD was supported by the Michigan State University Distinguished Fellowship Program and the Center for Microbial Ecology. Thanks to Terry Marsh, John Breznak, Tom Schmidt, and Kay Gross and their laboratory members for assistance with molecular techniques, physiology and coculture experiments, access to microscopy equipment, and helpful input on this manuscript.

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Correspondence to J. M. Tiedje.

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Dollhopf, S., Pariseau, M., Hashsham, S. et al. Competitive and Cooperative Interactions Affecting a Fermentative Spirochete in Anaerobic Chemostats . Microb Ecol 46, 1–11 (2003). https://doi.org/10.1007/PL00021035

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