Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1
Article first published online: 10 APR 2008
© 2008 Battelle Memorial Institute. Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd
Volume 10, Issue 7, pages 1861–1876, July 2008
How to Cite
McLean, J. S., Pinchuk, G. E., Geydebrekht, O. V., Bilskis, C. L., Zakrajsek, B. A., Hill, E. A., Saffarini, D. A., Romine, M. F., Gorby, Y. A., Fredrickson, J. K. and Beliaev, A. S. (2008), Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1. Environmental Microbiology, 10: 1861–1876. doi: 10.1111/j.1462-2920.2008.01608.x
- Issue published online: 10 APR 2008
- Article first published online: 10 APR 2008
- Received 6 November, 2007; accepted 19 February, 2008.
In aerobic chemostat cultures maintained at 50% dissolved O2 tension (3.5 mg l−1 dissolved O2), Shewanella oneidensis strain MR-1 rapidly aggregated upon addition of 0.68 mM CaCl2 and retained this multicellular phenotype at high dilution rates. Confocal microscopy analysis of the extracellular matrix material contributing to the stability of the aggregate structures revealed the presence of extracellular DNA, protein and glycoconjugates. Upon onset of O2-limited growth (dissolved O2 below detection) however, the Ca2+-supplemented chemostat cultures of strain MR-1 rapidly disaggregated and grew as motile dispersed cells. Global transcriptome analysis comparing aerobic aggregated to O2-limited unaggregated cells identified genes encoding cell-to-cell and cell-to-surface adhesion factors whose transcription increased upon exposure to increased O2 concentrations. The aerobic aggregated cells also revealed increased expression of putative anaerobic electron transfer and homologues of metal reduction genes, including mtrD (SO1782), mtrE (SO1781) and mtrF (SO1780). Our data indicate that mechanisms involved in autoaggregation of MR-1 are dependent on the function of pilD gene which encodes a putative prepilin peptidase. Mutants of S. oneidensis strain MR-1 deficient in PilD and associated pathways, including type IV and Msh pili biogenesis, displayed a moderate increase in sensitivity to H2O2. Taken together, our evidence indicates that aggregate formation in S. oneidensis MR-1 may serve as an alternative or an addition to biochemical detoxification to reduce the oxidative stress associated with production of reactive oxygen species during aerobic metabolism while facilitating the development of hypoxic conditions within the aggregate interior.