Abstract
Shewanella oneidensis MR-1 is a facultative anaerobe known for its ability to reduce metal oxides. Anaerobic respiration, especially metal reduction, has been the subject of extensive research. In contrast, S. oneidensis aerobic respiration has received less attention. S. oneidensis expresses cbb3- and aa3-type cytochrome c oxidases and a bd-type quinol oxidase. The aa3-type oxidase, which in other bacteria is the major oxygen reductase under oxygen replete conditions, does not appear to contribute to aerobic respiration and growth in S. oneidensis. Our results indicated that although the aa3-type oxidase does not play a role in aerobic growth on lactate, the preferred carbon source for S. oneidensis, it is involved in growth on pyruvate or acetate. These results highlight the importance of testing multiple carbon and energy sources when attempting to identify enzyme activities and mutant phenotypes. Several regulatory proteins contribute to the regulation of aerobic growth in S. oneidensis including CRP and ArcA. The 3',5'-cAMP phosphodiesterase (CpdA) appears to play a more significant role in aerobic growth than either CRP or ArcA, yet the deficiency does not appear to be the result of reduced oxidase genes expression. Interestingly, the ∆cpdA mutant was more deficient in aerobic respiration with several carbon sources tested compared to ∆crp, which was moderately deficient only in the presence of lactate. To identify the reason for ∆cpdA aerobic growth deficiency, we isolated a suppressor mutant with transposon insertion in SO_3550. Inactivation of this gene, which encodes an anti-sigma factor, restored aerobic growth in the cpdA mutant to wild-type levels. Inactivation of SO_3550 in wild-type cells, however, did not affect aerobic growth. The S. oneidensis genome encodes two additional CRP-like proteins that we designated CrpB and CrpC. Mutants that lack crpB and crpC were deficient in aerobic growth, but this deficiency was not due to the loss of oxidase gene expression.
Highlights
Shewanella oneidensis MR-1 is a Gram-negative facultative anaerobe found mostly at the oxic/anoxic interface in freshwater environments
The work presented in this paper suggests that the aa3-type and cbb3-type cytochrome oxidases are involved in aerobic respiration when pyruvate and acetate are used as carbon sources
Our results suggest that the aerobic growth deficiency observed in ∆cpdA is not due to the loss of cytochrome c oxidases, and this deficiency can be suppressed by a mutation in a putative anti-sigma factor
Summary
Shewanella oneidensis MR-1 is a Gram-negative facultative anaerobe found mostly at the oxic/anoxic interface in freshwater environments. The ability of S. oneidensis to thrive in such environments is attributed to its extreme respiratory versatility with regard to electron acceptors, which include oxygen, radionuclides, elemental sulfur, and metal oxides. The ability to use metals as terminal electron acceptors has spurred research into electricity generation by S. oneidensis. The location of c-type cytochromes, such as MtrC, on the outer cell surface (Beliaev et al, 2001) and the ability to reduce metal oxides made S. oneidensis and other metal reducing bacteria attractive candidates to study electricity production in microbial fuel cells (Bouhenni et al, 2010; Bretschger et al, 2010). In addition to the anaerobic reductases, S. oneidensis expresses three terminal aerobic oxidases. These are encoded by the cco operon (SO_2364–2357), the cox genes (SO_4606–4609), and cydABX (SO_3286–3284). The cco and cox operons encode the cbb3- and aa3-type enzymes that belong to the heme-copper oxidase (HCO) family, while cydAB encodes a bd-type quinol oxidase (Borisov et al, 2011; Sousa et al, 2012; Le Laz et al, 2014)
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