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.
Similar content being viewed by others
References
E Canale-Parola (1977) ArticleTitlePhysiology and evolution of spirochetes. Bact Rev 41 181–204 Occurrence Handle1:CAS:528:DyaE2sXktVajtLg%3D Occurrence Handle324466
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
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
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
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
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
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
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
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
JC Gottschal (1993) ArticleTitleGrowth kinetics and competition—some contemporary comments. Antonie van Leeuwenhoek 63 299–313 Occurrence Handle1:STN:280:ByuC3cnps1M%3D Occurrence Handle8279826
W Harder L Dijkhuizen (1983) ArticleTitlePhysiological response to nutrient limitation. Annu Rev Microbiol 37 1–23 Occurrence Handle1:CAS:528:DyaL2cXjtV2r Occurrence Handle6357049
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
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
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
S Jackowski CO Rock (1981) ArticleTitleRegulation of coenzyme A biosynthesis. J Bacteriol 148 926–932
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
HW Jannasch (1967) ArticleTitleEnrichments of aquatic bacteria in continuous culture. Arch Microbiol 59 165–173 Occurrence Handle1:STN:280:CCaD3s3mslM%3D
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
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
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
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
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
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
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
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
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
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
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
O Strunk W Ludwig (1997) ARB: Software for phylogenetic analysis. Technical University of Munich Munich, Germany
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
H Veldkamp (1977) ArticleTitleEcological studies with the chemostat. Adv Microb Ecol 1 59–94 Occurrence Handle1:CAS:528:DyaE1cXhvVKrug%3D%3D
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
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/PL00021035