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Abstract

Neutrophilic Fe(II) oxidizing bacteria play an important role in biogeochemical processes and have also received attention for multiple technological applications. These micro-organisms are thought to couple their metabolism with extracellular electron transfer (EET) while oxidizing Fe(II) as electron donor outside the cell. ES-1 is a freshwater chemolithoautotrophic Fe(II) oxidizing bacterium that is challenging to culture and not yet genetically tractable. Analysis of the ES-1 genome predicts multiple EET pathways, which are proposed to be involved in Fe(II) oxidation, but not yet validated. Here we expressed components of two of the proposed EET pathways, including the Mto and Slit_0867–0870 PCC3 pathways from ES-1 into , an established model EET organism. We demonstrate that combinations of putative inner membrane and periplasmic components from the Mto and Slit_0867–0870 PCC3 pathways partially complemented EET activity in mutants lacking native components. Our results provide evidence for electron transfer functionality and interactions of inner membrane and periplasmic components from the Mto and Slit_0867–0870 PCC3 pathways. Based on these findings, we suggest that EET in ES-1 could be more complicated than previously considered and raises questions regarding directionality of these electron transfer pathways.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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/content/journal/micro/10.1099/mic.0.001240
2022-09-16
2024-03-29
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References

  1. Coursolle D, Gralnick JA. Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 2010; 77:995–1008 [View Article] [PubMed]
    [Google Scholar]
  2. Conley BE, Intile PJ, Bond DR, Gralnick JA. Divergent Nrf family proteins and MtrCAB homologs facilitate extracellular electron transfer in Aeromonas hydrophila. Appl Environ Microbiol 2018; 84:e02134-18 [View Article]
    [Google Scholar]
  3. Conley BE, Weinstock MT, Bond DR, Gralnick JA. A hybrid extracellular electron transfer pathway enhances the survival of Vibrio natriegens. Appl Environ Microbiol 2020; 86:e01253-20 [View Article]
    [Google Scholar]
  4. Jiménez Otero F, Chan CH, Bond DR. Identification of different putative outer membrane electron conduits necessary for Fe (III) citrate, Fe (III) oxide, Mn (IV) oxide, or electrode reduction by Geobacter sulfurreducens. J Bacteriol 2018; 200:e00347-18 [View Article]
    [Google Scholar]
  5. Summers ZM, Gralnick JA, Bond DR. Cultivation of an obligate Fe(II)-oxidizing lithoautotrophic bacterium using electrodes. mBio 2013; 4:e00420–12 [View Article] [PubMed]
    [Google Scholar]
  6. Kato S. Biotechnological aspects of microbial extracellular electron transfer. Microbes Environ 2015; 30:133–139 [View Article]
    [Google Scholar]
  7. Light SH, Su L, Rivera-Lugo R, Cornejo JA, Louie A et al. A flavin-based extracellular electron transfer mechanism in diverse gram-positive bacteria. Nature 2018; 562:140–144 [View Article] [PubMed]
    [Google Scholar]
  8. Jain A, Gralnick JA. Engineering lithoheterotrophy in an obligate chemolithoautotrophic Fe(II) oxidizing bacterium. Sci Rep 2021; 11:1–6 [View Article] [PubMed]
    [Google Scholar]
  9. He S, Barco RA, Emerson D, Roden EE. Comparative genomic analysis of neutrophilic iron(II) oxidizer genomes for candidate genes in extracellular electron transfer. Front Microbiol 2017; 8:1–17 [View Article]
    [Google Scholar]
  10. Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C et al. Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(ll)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol 2012; 3:1–11 [View Article]
    [Google Scholar]
  11. Jain A, Gralnick JA. Evidence for auxiliary anaerobic metabolism in obligately aerobic Zetaproteobacteria. ISME J 2020; 14:1057–1062 [View Article] [PubMed]
    [Google Scholar]
  12. Edwards MJ, White GF, Butt JN, Richardson DJ, Clarke TA. The crystal structure of a biological insulated transmembrane molecular wire. Cell 2020; 181:665–673 [View Article]
    [Google Scholar]
  13. Emerson D, Moyer C. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 1997; 63:4784–4792 [View Article] [PubMed]
    [Google Scholar]
  14. Sturm G, Richter K, Doetsch A, Heide H, Louro RO et al. A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime. ISME J 2015; 9:1802–1811 [View Article] [PubMed]
    [Google Scholar]
  15. Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front Microbiol 2015; 6:332 [View Article] [PubMed]
    [Google Scholar]
  16. Jain A, Coelho A, Madjarov J, Paquete CM, Gralnick JA. Evidence for quinol oxidation activity of ImoA, a novel NapC/NirT family protein from the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. mBio (in press) 2022
    [Google Scholar]
  17. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA et al. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 1995; 166:175–176 [View Article] [PubMed]
    [Google Scholar]
  18. Saltikov CW, Newman DK. Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci 2003; 100:10983–10988 [View Article]
    [Google Scholar]
  19. Stookey LL. Ferrozine---a new spectrophotometric reagent for iron. Anal Chem 1970; 42:779–781 [View Article]
    [Google Scholar]
  20. Bücking C, Piepenbrock A, Kappler A, Gescher J. Outer-membrane cytochrome-independent reduction of extracellular electron acceptors in Shewanella oneidensis. Microbiology 2012; 158:2144–2157 [View Article]
    [Google Scholar]
  21. Jiao Y, Newman DK. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J Bacteriol 2007; 189:1765–1773 [View Article] [PubMed]
    [Google Scholar]
  22. Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L et al. Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol 2013; 4:254 [View Article] [PubMed]
    [Google Scholar]
  23. Levar CE, Hoffman CL, Dunshee AJ, Toner BM, Bond DR. Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens. ISME J 2017; 11:741–752 [View Article] [PubMed]
    [Google Scholar]
  24. Keffer JL, McAllister SM, Garber AI, Hallahan BJ, Sutherland MC et al. Iron oxidation by a fused cytochrome-porin common to diverse iron-oxidizing bacteria. mBio 2021; 12:e0107421 [View Article]
    [Google Scholar]
  25. Zhou N, Keffer JL, Polson SW, Chan CS. Unraveling fe(II)-oxidizing mechanisms in a facultative fe(II) oxidizier, Sideroxydans lithotrophicus strain ES-1, via culturing, transcriptomics and reverse transcription-quantative PCR. Appl Environ Microbiol 2022; 86:e01595–21 [View Article]
    [Google Scholar]
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