Reconstructing electron transfer components from an Fe(II) oxidizing bacterium

Jain, Abhiney; Kalb, Madison J; Gralnick, Jeffrey A.

doi:10.1099/mic.0.001240

Cited by 6 publications

(2 citation statements)

References 28 publications

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“…5 ). There is some evidence that the direction of electron flow through Mto/Mtr can be reversible ( 33 , 69 , 70 ). So, it may be that the functions of MtoA and MtrA are interchangeable, and in fact, they may be indistinguishable proteins that can conduct electrons across the outer membrane in either direction.…”

Section: Resultsmentioning

confidence: 99%

Gallionellaceae pangenomic analysis reveals insight into phylogeny, metabolic flexibility, and iron oxidation mechanisms

Hoover,

Keffer,

Polson

et al. 2023

mSystems

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The iron-oxidizing Gallionellaceae drive a wide variety of biogeochemical cycles through their metabolisms and biominerals. To better understand the environmental impacts of Gallionellaceae, we need to improve our knowledge of their diversity and metabolisms, especially any novel iron oxidation mechanisms. Here, we used a pangenomic analysis of 103 genomes to resolve Gallionellaceae phylogeny and explore their genomic potential. Using a concatenated ribosomal protein tree and key gene patterns, we determined Gallionellaceae has four genera, divided into two groups: iron-oxidizing bacteria (FeOB) Gallionella , Sideroxydans , and Ferriphaselus with iron oxidation genes ( cyc2 , mtoA ) and nitrite-oxidizing bacteria (NOB) Candidatus Nitrotoga with the nitrite oxidase gene nxr . The FeOB and NOB have similar electron transport chains, including genes for reverse electron transport and carbon fixation. Auxiliary energy metabolisms, including S oxidation, denitrification, and organotrophy, were scattered throughout the FeOB. Within FeOB, we found genes that may represent adaptations for iron oxidation, including a variety of extracellular electron uptake mechanisms. FeOB genomes encoded more predicted c -type cytochromes than NOB genomes, notably more multiheme c -type cytochromes (MHCs) with >10 CXXCH motifs. These include homologs of several predicted outer membrane porin-MHC complexes, including MtoAB and Uet. MHCs efficiently conduct electrons across longer distances and function across a wide range of redox potentials that overlap with mineral redox potentials, which can expand the range of usable iron substrates. Overall, the results of pangenome analyses suggest that the Gallionellaceae genera Gallionella , Sideroxydans , and Ferriphaselus have acquired a range of adaptations to succeed in various environments but are primarily iron oxidizers. IMPORTANCE Neutrophilic iron-oxidizing bacteria (FeOB) produce copious iron (oxyhydr)oxides that can profoundly influence biogeochemical cycles, notably the fate of carbon and many metals. To fully understand environmental microbial iron oxidation, we need a thorough accounting of iron oxidation mechanisms. In this study, we show the Gallionellaceae FeOB genomes encode both characterized iron oxidases as well as uncharacterized multiheme cytochromes (MHCs). MHCs are predicted to transfer electrons from extracellular substrates and likely confer metabolic capabilities that help Gallionellaceae occupy a range of different iron- and mineral-rich niches. Gallionellaceae appear to specialize in iron oxidation, so it would be advantageous for them to have multiple mechanisms to oxidize various forms of iron, given the many iron minerals on Earth, as well as the physiological and kinetic challenges faced by FeOB. The multiple iron/mineral oxidation mechanisms may help drive the widespread ecological success of Gallionellaceae.

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Section: Resultsmentioning

confidence: 99%

Gallionellaceae pangenomic analysis reveals insight into phylogeny, metabolic flexibility, and iron oxidation mechanisms

Hoover,

Keffer,

Polson

et al. 2023

mSystems

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“…Therefore, we assumed that it was capable of motility. The genera we found as potential flockers have members which have been verified as EET-performers: Sideroxydans, Azonexus, Rhodoferax (Jain et al 2022; Jangir et al, 2016; Finneran et al, 2003).…”

Section: Discussionmentioning

confidence: 66%

Extracellular electron transfer genes expressed by candidate flocking bacteria in cable bacteria sediment

Lustermans,

Sereika,

Burdorf

et al. 2024

Preprint

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Cable bacteria, filamentous sulfide oxidizers that live in sediments, are at times associated with large flocks of swimming bacteria. It has been proposed that these flocks of bacteria transport electrons extracellularly to cable bacteria via an electron shuttle intermediate, but the identity and activity of these bacteria in freshwater sediment remains mostly uninvestigated. We coupled metagenomics and metatranscriptomics to 16S rRNA amplicon-based correlations with cable bacteria from two time series experiments up to 155 days. We identified bacteria expressing genes for extracellular electron transfer and motility, including synthesis genes for potential extracellular electron shuttles: phenazines and flavins. Of the 85 high quality MAGs (Metagenome Assembled Genomes >90% complete and <5% contaminated), 56 had genes encoding flagellar proteins, and of these 22 had genes encoding extracellular electron transport proteins. The candidate flockers constituted 21.4% of all MAGs and 42.1% of the proposed flocking bacteria expressed extracellular electron transfer genes. The proposed flockers belonged to a large variety of taxonomic groups: 18 genera spread across 9 phyla. Our data suggest that electric relationships in freshwater sediments between cable bacteria and other microbes likely help to generate and/or sustain cryptic element cycling and ‘deep oxygen breathing’, affecting more element cycles than sulfur, like metal– and in particular iron– and carbon cycles.

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