Evidence for Horizontal and Vertical Transmission of Mtr-Mediated Extracellular Electron Transfer among the
            <i>Bacteria</i>

Baker, Isabel R; Conley, Bridget; Gralnick, Jeffrey A.; Girguis, Peter R.

doi:10.1128/mbio.02904-21

Cited by 31 publications

(32 citation statements)

References 146 publications

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“…Multiheme cytochrome electron transfer proteins have evolved to support the exchange of electrons between cells and the extracellular environment. , By binding a series of adjacent cofactors that span tertiary structures, these proteins enable electron transport across the insulating membrane and across micrometer-scale distances by insulating the heme prosthetic groups from the solvent. − This high-efficiency electron transport enables diverse microorganisms to respire on extracellular metals, minerals, and materials. ,− The Gram-negative bacterium Shewanella oneidensis has evolved a cytochrome-based pathway, designated the metal-reducing pathway (Mtr), to support extracellular electron transfer (EET). , This pathway allows microbes to respire on Fe(III), Mn(III), and Mn(IV). , Additionally, the Mtr pathway can reduce extracellular minerals, like hematite or ferrihydrite, as well as synthetic nanoparticles and electrodes. ,− …”

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confidence: 99%

Determinants of Multiheme Cytochrome Extracellular Electron Transfer Uncovered by Systematic Peptide Insertion

et al. 2022

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The multiheme cytochrome MtrA enables microbial respiration by transferring electrons across the outer membrane to extracellular electron acceptors. While structural studies have identified residues that mediate the binding of MtrA to hemes and to other cytochromes that facilitate extracellular electron transfer (EET), the relative importance of these interactions for EET is not known. To better understand EET, we evaluated how insertion of an octapeptide across all MtrA backbone locations affects Shewanella oneidensis MR-1 respiration on Fe(III). The EET efficiency was found to be inversely correlated with the proximity of the insertion to the heme prosthetic groups. Mutants with decreased EET efficiencies also arose from insertions in a subset of the regions that make residue–residue contacts with the porin MtrB, while all sites contacting the extracellular cytochrome MtrC presented high peptide insertion tolerance. MtrA variants having peptide insertions within the CXXCH motifs that coordinate heme cofactors retained some ability to support respiration on Fe(III), although these variants presented significantly decreased EET efficiencies. Furthermore, the fitness of cells expressing different MtrA variants under Fe(III) respiration conditions correlated with anode reduction. The peptide insertion profile, which represents the first comprehensive sequence–structure–function map for a multiheme cytochrome, implicates MtrA as a strategic protein engineering target for the regulation of EET.

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confidence: 99%

Determinants of Multiheme Cytochrome Extracellular Electron Transfer Uncovered by Systematic Peptide Insertion

et al. 2022

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“…Likewise, HGT of MHC has been extensively reported in the literature, including for NrfA ( Welsh et al 2014 ), HAO ( Bergmann et al 2005 ), and several MHCs involved in extracellular electron transfer, such as MtrCAB and OmcA from Shewanella spp. ( Zhong et al 2018 ; Baker et al 2022 ).…”

Section: Discussionmentioning

confidence: 99%

A New Paradigm of Multiheme Cytochrome Evolution by Grafting and Pruning Protein Modules

Soares

Costa

Paquete

et al. 2022

Molecular Biology and Evolution

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Multiheme cytochromes play key roles in diverse biogeochemical cycles, but understanding the origin and evolution of these proteins is a challenge due to their ancient origin and complex structure. Up until now, the evolution of multiheme cytochromes composed by multiple redox modules in a single polypeptide chain was proposed to occur by gene fusion events. In this context, the pentaheme nitrite reductase NrfA and the tetraheme cytochrome c554 were previously proposed to be at the origin of the extant octa- and nonaheme cytochromes c involved in metabolic pathways that contribute to the nitrogen, sulfur and iron biogeochemical cycles by a gene fusion event. Here, we combine structural and character-based phylogenetic analysis with an unbiased root placement method to refine the evolutionary relationships between these multiheme cytochromes. The evidence show that NrfA and cytochrome c554 belong to different clades, which suggests that these two multiheme cytochromes are products of truncation of ancestral octaheme cytochromes related to extant ONR and MccA, respectively. From our phylogenetic analysis, the last common ancestor is predicted to be an octaheme cytochrome with nitrite reduction ability. Evolution from this octaheme framework led to the great diversity of extant multiheme cytochromes analyzed here by pruning and grafting of protein modules and hemes. By shedding light into the evolution of multiheme cytochromes that intervene in different biogeochemical cycles, this work contributes to our understanding about the interplay between biology and geochemistry across large time scales in the history of Earth.

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“…Likewise, HGT of MHC has been extensively reported in the literature, including for NrfA (Welsh et al 2014), HAO (Bergmann et al 2005) and several MHC involved in extracellular electron transfer, such as MtrCAB and OmcA from Shewanella spp. (Zhong et al 2018; Baker et al 2022).…”

Section: Discussionmentioning

confidence: 99%

“…2014), HAO(Bergmann et al 2005) and several MHC involved in extracellular electron transfer, such as MtrCAB and OmcA from Shewanella spp. (Zhong et al 2018;Baker et al 2022). …”

mentioning

confidence: 99%

A new paradigm of multiheme cytochrome evolution by grafting and pruning protein modules

Soares

Paquete

Costa

et al. 2022

Preprint

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Multiheme cytochromes play key roles in diverse biogeochemical cycles, but understanding the origin and evolution of these proteins is a challenge due to their ancient origin and complex structure. Up until now, the evolution of multiheme cytochromes composed by multiple redox modules in a single polypeptide chain was proposed to occur by gene fusion events. In this context, the pentaheme nitrite reductase NrfA and the tetraheme cytochrome c554 were previously proposed to be at the origin of the extant octa- and nonaheme cytochromes c involved in metabolic pathways that contribute to the nitrogen, sulfur and iron biogeochemical cycles by a gene fusion event. Here, we combine structural and character-based phylogenetic analysis with an unbiased root placement method to refine the evolutionary relationships between these multiheme cytochromes. The evidence show that NrfA and cytochrome c554 belong to different clades, which suggests that these two multiheme cytochromes are products of truncation of ancestral octaheme cytochromes related to extant ONR and MccA, respectively. From our phylogenetic analysis, the last common ancestor is predicted to be an octaheme cytochrome with nitrite reduction ability. Evolution from this octaheme framework led to the great diversity of extant multiheme cytochromes analised here by pruning and grafting of protein modules and hemes. By shedding light into the evolution of multiheme cytochromes that intervene in different biogeochemical cycles, this work contributes to our understanding about the interplay between biology and geochemistry across large time scales in the history of Earth.

show abstract

Evidence for Horizontal and Vertical Transmission of Mtr-Mediated Extracellular Electron Transfer among the Bacteria

Cited by 31 publications

References 146 publications

Determinants of Multiheme Cytochrome Extracellular Electron Transfer Uncovered by Systematic Peptide Insertion

Determinants of Multiheme Cytochrome Extracellular Electron Transfer Uncovered by Systematic Peptide Insertion

A New Paradigm of Multiheme Cytochrome Evolution by Grafting and Pruning Protein Modules

A new paradigm of multiheme cytochrome evolution by grafting and pruning protein modules

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