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The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen

Abstract

Strict anaerobes cannot grow in the presence of greater than 5 µM dissolved oxygen1. Despite this growth inhibition, many strict anaerobes of the Bacteroides class of eubacteria can survive in oxygenated environments until the partial pressure of O2 ( p O 2 ) is sufficiently reduced. For example, the periodontal pathogens Porphyromonas gingivalis and Tannerella forsythensis colonize subgingival plaques of mammals, whereas several other Bacteroides species colonize the gastrointestinal tract of animals. It has been suggested that pre-colonization of these sites by facultative anaerobes is essential for reduction of the p O 2 and subsequent colonization by strict anaerobes2. However, this model is inconsistent with the observation that Bacteroides fragilis can colonize the colon in the absence of facultative anaerobes3. Thus, this strict anaerobe may have a role in reduction of the environmental p O 2 . Although some strictly anaerobic bacteria can consume oxygen through an integral membrane electron transport system4, the physiological role of this system has not been established in these organisms. Here we demonstrate that B. fragilis encodes a cytochrome bd oxidase that is essential for O2 consumption and is required, under some conditions, for the stimulation of growth in the presence of nanomolar concentrations of O2. Furthermore, our data suggest that this property is conserved in many other organisms that have been described as strict anaerobes.

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Figure 1: O2-dependent growth stimulation of B. fragilis requires cytochrome bd oxidase.
Figure 2: The B. fragilis cydAB genes are required for consumption of O2.
Figure 3: The cydAB region of B. fragilis.
Figure 4: Phylogram of CydA amino acid sequences.

References

  1. Engelkirk, P. G., Duben-Engelkirk, J. & Dowell, V. R. Principles and Practice of Clinical Anaerobic Bacteriology (Star Publishing Company, Belmont, California, 1992)

    Google Scholar 

  2. Levitt, M. D. Oxygen tension in the gut. N. Engl. J. Med. 282, 1039–1040 (1970)

    CAS  Article  PubMed  Google Scholar 

  3. Bornside, G. H., Donovan, W. E. & Myers, M. B. Intracolonic tensions of oxygen and carbon dioxide in germfree, conventional, and gnotobiotic rats. Proc. Soc. Exp. Biol. Med. 151, 437–441 (1976)

    CAS  Article  PubMed  Google Scholar 

  4. Lemos, R. S. et al. The ‘strict’ anaerobe Desulfovibrio gigas contains a membrane-bound oxygen-reducing respiratory chain. FEBS Lett. 496, 40–43 (2001)

    CAS  Article  PubMed  Google Scholar 

  5. Duwat, P. et al. Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J. Bacteriol. 183, 4509–4516 (2001)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Poole, R. K. & Cook, G. M. Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv. Microb. Physiol. 43, 165–224 (2000)

    CAS  Article  PubMed  Google Scholar 

  7. Macy, J., Probst, I. & Gottschalk, G. Evidence for cytochrome involvement in fumarate reduction and adenosine 5′-triphosphate synthesis by Bacteroides fragilis grown in the presence of hemin. J. Bacteriol. 123, 436–442 (1975)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Baughn, A. D. & Malamy, M. H. The essential role of fumarate reductase in haem-dependent growth stimulation of Bacteroides fragilis. Microbiology 149, 1503–1511 (2003)

    Article  Google Scholar 

  9. Kushnareva, Y., Murphy, A. N. & Andreyev, A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation–reduction state. Biochem. J. 368, 545–553 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Cypionka, H. Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54, 827–848 (2000)

    CAS  Article  PubMed  Google Scholar 

  11. Weisburg, W. G., Oyaizu, Y., Oyaizu, H. & Woese, C. R. Natural relationship between Bacteroides and Flavobacteria.. J. Bacteriol. 164, 230–236 (1985)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Bocchetta, M., Gribaldo, S., Sanangelantoni, A. & Cammarano, P. Phylogenetic depth of the bacterial genra Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J. Mol. Evol. 50, 366–380 (2000)

    ADS  CAS  Article  PubMed  Google Scholar 

  13. Di Giulio, M. The universal ancestor was a thermophile or a hyperthermophile: Tests and further evidence. J. Theor. Biol. 221, 425–436 (2003)

    MathSciNet  Article  PubMed  Google Scholar 

  14. Castresana, J. & Saraste, M. Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biol. Sci. 20, 443–448 (1995)

    CAS  Article  Google Scholar 

  15. Catling, D. C., Zahnle, K. J. & McKay, C. P. Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293, 839–843 (2001)

    ADS  CAS  Article  PubMed  Google Scholar 

  16. Towe, K. M. The problematic rise of archean oxygen. Science 295, 1419 (2002)

    Article  PubMed  Google Scholar 

  17. Baughn, A. D. & Malamy, M. H. A mitochondrial-like aconitase in the bacterium Bacteroides fragilis: Implications for the evolution of the mitochondrial Krebs cycle. Proc. Natl Acad. Sci. USA 99, 4662–4667 (2002)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Tally, F. P., Snydman, D. R., Shimell, M. J. & Malamy, M. H. Characterization of pBFTM10, a clindamycin–erythromycin resistance transfer factor from Bacteroides fragilis. J. Bacteriol. 151, 686–691 (1982)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Swofford, D. L. Phylogenetic Analysis Using Parsimony and Other Methods (Sinauer, Sunderland, 2002)

    Google Scholar 

  20. Claros, M. G. & von Heijne, G. TopPred II: An improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685–686 (1994)

    CAS  PubMed  Google Scholar 

  21. Schmalfuβ, H. & Werner, H. Ein empfindlicher qualitativer Sauerstoff-Nachweis mit Pyrogallol und Kalilauge. Berichte Deutsch. Chem. Gesellschaft 52, 71–73 (1925)

    Article  Google Scholar 

  22. Page, R. D. Treeview: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357–358 (1996)

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank A. L. Sonenshein for critical review of the manuscript, and D. W. Lazinski and A. Camilli for comments on the manuscript. This study was supported by a US Public Health Service Grant.

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Correspondence to Michael H. Malamy.

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Supplementary information

41586_2004_BFnature02285_MOESM1_ESM.pdf

Supplementary Figure 1: Phylogram of CydA amino acid sequences. Sequences were aligned by the CLUSTALW method. The tree was calculated by using the parsimony method with PAUP 4.0b10 and visualized by using TREEVIEWPPC 1.6.5. The scale represents 0.1 substitutions per residue. Numbers at the nodes represent bootstrap values from 100 repetitions. (PDF 9 kb)

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Baughn, A., Malamy, M. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427, 441–444 (2004). https://doi.org/10.1038/nature02285

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