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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.

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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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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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