Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis

Bertling, Kristen; Banerjee, Areen; Saffarini, Daad

doi:10.3389/fmicb.2021.723835

Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis

Journal Article · Thu Sep 09 00:00:00 EDT 2021 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2021.723835· OSTI ID:1849828

Bertling, Kristen ^[1]; Banerjee, Areen ^[2]; Saffarini, Daad ^[2]

Univ. of Wisconsin-Milwaukee, WI (United States). Dept. of Biological Sciences; Univ. of Wisconsin-Milwaukee, Milwaukee, WI (United States)
Univ. of Wisconsin-Milwaukee, WI (United States). Dept. of Biological Sciences

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 ΔcpdA mutant was more deficient in aerobic respiration with several carbon sources tested compared to Δcrp, which was moderately deficient only in the presence of lactate. To identify the reason for ΔcpdA 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.

View Accepted Manuscript (DOE)

Research Organization:: University of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-07ER64382

OSTI ID:: 1849828

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 12; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (33)

A kinetic model describingShewanella oneidensis MR-1 growth, substrate consumption, and product secretion Tang, Yinjie J.; Meadows, Adam L.; Keasling, Jay D. Biotechnology and Bioengineering, Vol. 96, Issue 1 https://doi.org/10.1002/bit.21101	journal	January 2006
Comparative Microbial Fuel Cell Evaluations of Shewanella spp. Bretschger, Orianna; Cheung, Andrea C. M.; Mansfeld, Florian Electroanalysis, Vol. 22, Issue 7-8 https://doi.org/10.1002/elan.200800016	journal	March 2010
The Role of Shewanella oneidensis MR-1 Outer Surface Structures in Extracellular Electron Transfer Bouhenni, Rachida A.; Vora, Gary J.; Biffinger, Justin C. Electroanalysis, Vol. 22, Issue 7-8 https://doi.org/10.1002/elan.200880006	journal	March 2010
The bacterial cytochrome cbb3 oxidases Pitcher, Robert S.; Watmough, Nicholas J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1655 https://doi.org/10.1016/j.bbabio.2003.09.017	journal	April 2004
The cytochrome bd respiratory oxygen reductases Borisov, Vitaliy B.; Gennis, Robert B.; Hemp, James Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11 https://doi.org/10.1016/j.bbabio.2011.06.016	journal	November 2011
The superfamily of heme–copper oxygen reductases: Types and evolutionary considerations Sousa, Filipa L.; Alves, Renato J.; Ribeiro, Miguel A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 4 https://doi.org/10.1016/j.bbabio.2011.09.020	journal	April 2012
Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA Gao, Haichun; Yang, Zamin K.; Barua, Soumitra The ISME Journal, Vol. 3, Issue 8 https://doi.org/10.1038/ismej.2009.40	journal	April 2009
Combined effect of loss of the caa3 oxidase and Crp regulation drives Shewanella to thrive in redox-stratified environments Zhou, Guangqi; Yin, Jianhua; Chen, Haijiang The ISME Journal, Vol. 7, Issue 9 https://doi.org/10.1038/ismej.2013.62	journal	April 2013
Towards environmental systems biology of Shewanella Fredrickson, James K.; Romine, Margaret F.; Beliaev, Alexander S. Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1947	journal	July 2008
Regulation and Maturation of the Shewanella oneidensis Sulfite Reductase SirA Brockman, Kenneth L.; Shirodkar, Sheetal; Croft, Trevor J. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57587-6	journal	January 2020
Expression of terminal oxidases under nutrient-starved conditions in Shewanella oneidensis: detection of the A-type cytochrome c oxidase Le Laz, Sébastien; kpebe, Arlette; Bauzan, Marielle Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19726	journal	January 2016
Reduced expression of cytochrome oxidases largely explains cAMP inhibition of aerobic growth in Shewanella oneidensis Yin, Jianhua; Meng, Qiu; Fu, Huihui Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24449	journal	April 2016
MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1 Beliaev, Alex S.; Saffarini, Daad A.; McLaughlin, Jennifer L. Molecular Microbiology, Vol. 39, Issue 3 https://doi.org/10.1046/j.1365-2958.2001.02257.x	journal	February 2001
CpdA is involved in amino acid metabolism in Shewanella oneidensis MR-1 Kasai, Takuya; Kouzuma, Atsushi; Watanabe, Kazuya Bioscience, Biotechnology, and Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1080/09168451.2017.1413326	journal	January 2018
Gene and Protein Expression Profiles of Shewanella oneidensis during Anaerobic Growth with Different Electron Acceptors Beliaev, Alex S.; Thompson, Dorothea K.; Khare, Tripti OMICS: A Journal of Integrative Biology, Vol. 6, Issue 1 https://doi.org/10.1089/15362310252780834	journal	January 2002
Revisiting bacterial cyclic nucleotide phosphodiesterases: cyclic AMP hydrolysis and beyond Matange, Nishad FEMS Microbiology Letters, Vol. 362, Issue 22 https://doi.org/10.1093/femsle/fnv183	journal	September 2015
Oxygen-regulated gene expression in Escherichia coli: (Delivered at the 122nd Ordinary Meeting of the Society for General Microbiology, 25 March 1992) Guest, J. R. Journal of General Microbiology, Vol. 138, Issue 11 https://doi.org/10.1099/00221287-138-11-2253	journal	November 1992
Anaerobic regulation by an atypical Arc system in Shewanella oneidensis: An atypical Arc system in S. oneidensis Gralnick, Jeffrey A.; Brown, C. Titus; Newman, Dianne K. Molecular Microbiology, Vol. 56, Issue 5 https://doi.org/10.1111/j.1365-2958.2005.04628.x	journal	March 2005
Differential expression of multiple terminal oxidases for aerobic respiration in Pseudomonas aeruginosa Kawakami, Takuro; Kuroki, Miho; Ishii, Masaharu Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2009.02109.x	journal	December 2009
The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1 : Dissimilatory sulfite reduction by the octahaem SirA Shirodkar, Sheetal; Reed, Samantha; Romine, Margie Environmental Microbiology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1462-2920.2010.02313.x	journal	August 2010
Cytochrome c oxidase in prokaryotes Ludwig, Bernd FEMS Microbiology Letters, Vol. 46, Issue 1 https://doi.org/10.1111/j.1574-6968.1987.tb02451.x	journal	March 1987
Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration: c-type cytochromes of S. oneidensis Gao, Haichun; Barua, Soumitra; Liang, Yili Microbial Biotechnology, Vol. 3, Issue 4 https://doi.org/10.1111/j.1751-7915.2010.00181.x	journal	June 2010
The Structure of cbb3 Cytochrome Oxidase Provides Insights into Proton Pumping Buschmann, S.; Warkentin, E.; Xie, H. Science, Vol. 329, Issue 5989 https://doi.org/10.1126/science.1187303	journal	June 2010
Identification of Genes Involved in Cytochrome c Biogenesis in Shewanella oneidensis, Using a Modified mariner Transposon Bouhenni, R.; Gehrke, A.; Saffarini, D. Applied and Environmental Microbiology, Vol. 71, Issue 8 https://doi.org/10.1128/AEM.71.8.4935-4937.2005	journal	August 2005
ArcB1, a Homolog of Escherichia coli ArcB, Regulates Dimethyl Sulfoxide Reduction in Shewanella oneidensis MR-1 Shroff, Namita P.; Charania, Moiz A.; Saffarini, Daad A. Journal of Bacteriology, Vol. 192, Issue 12 https://doi.org/10.1128/JB.01695-09	journal	April 2010
Involvement of a Membrane-Bound Class III Adenylate Cyclase in Regulation of Anaerobic Respiration in Shewanella oneidensis MR-1 Charania, M. A.; Brockman, K. L.; Zhang, Y. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01829-08	journal	April 2009
Involvement of Cyclic AMP (cAMP) and cAMP Receptor Protein in Anaerobic Respiration of Shewanella oneidensis Saffarini, D. A.; Schultz, R.; Beliaev, A. Journal of Bacteriology, Vol. 185, Issue 12 https://doi.org/10.1128/JB.185.12.3668-3671.2003	journal	June 2003
The superfamily of heme-copper respiratory oxidases. García-Horsman, J. A.; Barquera, B.; Rumbley, J. Journal of Bacteriology, Vol. 176, Issue 18 https://doi.org/10.1128/jb.176.18.5587-5600.1994	journal	September 1994
Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. Dehio, C.; Meyer, M. Journal of Bacteriology, Vol. 179, Issue 2 https://doi.org/10.1128/jb.179.2.538-540.1997	journal	January 1997
Influences of Aerobic Respiration on Current Generation by Shewanella oneidensis MR-1 in Single-Chamber Microbial Fuel Cells Kouzuma, Atsushi; Hashimoto, Kazuhito; Watanabe, Kazuya Bioscience, Biotechnology, and Biochemistry, Vol. 76, Issue 2 https://doi.org/10.1271/bbb.110633	journal	February 2012
A Biochemical Approach to Study the Role of the Terminal Oxidases in Aerobic Respiration in Shewanella oneidensis MR-1 Le Laz, Sébastien; Kpebe, Arlette; Bauzan, Marielle PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0086343	journal	January 2014
Specific expression and function of the A-type cytochrome c oxidase under starvation conditions in Pseudomonas aeruginosa Osamura, Tatsuya; Kawakami, Takuro; Kido, Reiko PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0177957	journal	May 2017
CRP Regulates D-Lactate Oxidation in Shewanella oneidensis MR-1 Kasai, Takuya; Kouzuma, Atsushi; Watanabe, Kazuya Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00869	journal	May 2017

Similar Records

Physiological roles of ArcA, Crp, and EtrA and their interactive control on aerobic and anaerobic respiration in Shewanella oneidensis

Journal Article · Thu Dec 31 23:00:00 EST 2009 · PLoS ONE · OSTI ID:1025416

Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses

Journal Article · Mon Dec 31 23:00:00 EST 2007 · BMC Genomics · OSTI ID:963672

Impact of ArcA loss in Shewanella oneidensis revealed by comparative proteomics under aerobic and anaerobic conditions

Journal Article · Fri Jun 01 00:00:00 EDT 2012 · Proteomics · OSTI ID:1050802

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Shewanella oneidensis MR1
aerobic respiration
anti-sigma factor
cAMP phosphodiesterase
crp
cytochrome oxidase
microbiology

Aerobic Respiration and Its Regulation in the Metal Reducer Shewanella oneidensis

Citation Formats

References (33)

Similar Records

Related Subjects