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Regulation of gene expression in Shewanella oneidensis MR-1 during electron acceptor limitation and bacterial nanowire formation
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Barchinger, Sarah E., Pirbadian, Sahand, Sambles, Christine, Baker, Carol S., Leung, Kar Man, Burroughs, Nigel John, El-Naggar, Mohamed Y., Golbeck, John H. and Spormann, A. M. (2016) Regulation of gene expression in Shewanella oneidensis MR-1 during electron acceptor limitation and bacterial nanowire formation. Applied and Environmental Microbiology, 82 (17). pp. 5428-5443. doi:10.1128/AEM.01615-16
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Official URL: http://dx.doi.org/10.1128/AEM.01615-16
Abstract
In limiting oxygen as an electron acceptor, the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 rapidly forms nanowires, extensions of its outer membrane containing the cytochromes MtrC and OmcA needed for extracellular electron transfer. RNA-Seq analysis was employed to determine differential gene expression over time from triplicate chemostat cultures that were limited for oxygen. We identified 465 genes with decreased expression and 677 genes with increased expression. The coordinated increased expression of heme biosynthesis, cytochrome maturation, and transport pathways indicates that S. oneidensis MR-1 increases cytochrome production, including transcription of genes encoding MtrA, MtrC and OmcA, and transports these decaheme cytochromes across the cytoplasmic membrane during electron acceptor limitation and nanowire formation. In contrast, the expression of the mtrA and mtrC homologs mtrF and mtrD either remain unaffected or decrease under these conditions. The ompW gene, encoding a small outer membrane porin, has 40-fold higher expression during oxygen limitation, and it is proposed that OmpW plays a role in cation transport to maintain electrical neutrality during electron transfer. The genes encoding the anaerobic respiration regulator CRP and the extracytoplasmic function sigma factor RpoE are among transcription factor genes with increased expression. RpoE could function by signaling the initial response to oxygen limitation. Our results show that RpoE activates transcription from promoters upstream of mtrC and omcA. The transcriptome and mutant analysis of S. oneidensis MR-1 nanowire production are consistent with independent regulatory mechanisms for extending the outer membrane into tubular structures and for ensuring the electron transfer function of the nanowires.
| Item Type: | Journal Article | ||||||
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| Divisions: | Faculty of Science > Mathematics Faculty of Science > Centre for Systems Biology |
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| Journal or Publication Title: | Applied and Environmental Microbiology | ||||||
| Publisher: | American Society for Microbiology | ||||||
| ISSN: | 0099-2240 | ||||||
| Official Date: | 24 June 2016 | ||||||
| Dates: |
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| Volume: | 82 | ||||||
| Number: | 17 | ||||||
| Page Range: | pp. 5428-5443 | ||||||
| DOI: | 10.1128/AEM.01615-16 | ||||||
| Status: | Peer Reviewed | ||||||
| Publication Status: | Published | ||||||
| Access rights to Published version: | Restricted or Subscription Access |
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