Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis
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-...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.723835/full |
| _version_ | 1818738706890096640 |
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| author | Kristen Bertling Areen Banerjee Daad Saffarini |
| author_facet | Kristen Bertling Areen Banerjee Daad Saffarini |
| author_sort | Kristen Bertling |
| collection | DOAJ |
| description | 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. |
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| format | Article |
| id | doaj.art-0ed3b955145a4b06821cca3097b16969 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-18T01:13:12Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-0ed3b955145a4b06821cca3097b169692022-12-21T21:26:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.723835723835Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensisKristen BertlingAreen BanerjeeDaad SaffariniShewanella 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.723835/fullaerobic respirationShewanella oneidensis MR1crpcAMP phosphodiesteraseanti-sigma factorcytochrome oxidase |
| spellingShingle | Kristen Bertling Areen Banerjee Daad Saffarini Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis Frontiers in Microbiology aerobic respiration Shewanella oneidensis MR1 crp cAMP phosphodiesterase anti-sigma factor cytochrome oxidase |
| title | Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis |
| title_full | Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis |
| title_fullStr | Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis |
| title_full_unstemmed | Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis |
| title_short | Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis |
| title_sort | aerobic respiration and its regulation in the metal reducer shewanella oneidensis |
| topic | aerobic respiration Shewanella oneidensis MR1 crp cAMP phosphodiesterase anti-sigma factor cytochrome oxidase |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.723835/full |
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