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PreprintCited by 33Metal Extraction and BioleachingMicrobial Fuel Cells and BioremediationMicrobial metabolism and enzyme function

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

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Hoover, Rene L., Keffer, Jessica L., Polson, Shawn W., Chan, Clara S.·2023·mSystems
DOI 10.1101/2023.01.26.525709PMC PMC10734462

Preprint — published as 10.1128/msystems.00038-23 · Paper page

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Abstract

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 the range of 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 known iron oxidases (Cyc2, MtoA) and nitrite-oxidizing bacteria (NOB) Candidatus Nitrotoga with nitrite oxidase (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 Gallionellaceae FeOB. Within FeOB, we found genes that may represent adaptations for iron oxidation, including a variety of extracellular electron uptake (EEU) mechanisms. FeOB genomes encoded more predicted c -type cytochromes overall, 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 are known to efficiently conduct electrons across longer distances and function across a wide range of redox potentials that overlap with mineral redox potentials, which can help expand the range of usable iron substrates. Overall, the results of pangenome analyses suggest that the Gallionellaceae genera Gallionella , Sideroxydans , and Ferriphaselus are primarily iron oxidizers, capable of oxidizing dissolved Fe 2+ as well as a range of solid iron or other mineral substrates. 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 have both known 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 makes sense that they would 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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Metadata

Authors
Hoover, R. L., Keffer, J. L., Polson, S. W., & Chan, C. S.
Affiliations
University of Delaware (US)
Corresponding author
Chan, Clara S.
ORCID
Venue
mSystems
Publisher
openRxiv
Published
2023-01-26
Volume
8
Issue
6
Pages
e0003823-e0003823
ISSN
2379-5077 (ISSN-L)
DOI
10.1101/2023.01.26.525709
PMC
PMC10734462
OpenAlex
W4387949721
Cited by
33
References
1
Citations by year
2026: 17 · 2025: 7 · 2024: 7 · 2023: 2
FWCI
2.61
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • mSystems (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (1817651, P20 GM103446, 1833525)
  • U.S. Department of Defense
  • University of Delaware (P20-GM103446)
  • Delaware IDeA Network of Biomedical Research Excellence (P20‐GM103446)
  • Unidel Foundation
  • National Institutes of Health
  • Office of Naval Research (N00014-17-1-2640, N00014-17-1, N00014)
  • National Institute of General Medical Sciences (P20GM103446)
Topics
  • Physical Sciences › Materials Science › Metals and Alloys › Metal Extraction and Bioleaching
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords
Gallionellaceae, iron-oxidizing bacteria, nitrite-oxidizing bacteria, pan-genome, phylogeny, multiheme c-type cytochromes, extracellular electron transfer, reverse electron transfer, biomineralization, biogeochemical cycles, Gallionella, metabolic flexibility, denitrification

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