Proterozoic Acquisition of Archaeal Genes for Extracellular Electron Transfer: A Metabolic Adaptation of Aerobic Ammonia-Oxidizing Bacteria to Oxygen Limitation

Arda Gülay*, Greg Fournier, Barth F. Smets, Peter R. Girguis

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

Many aerobic microbes can utilize alternative electron acceptors under oxygen-limited conditions. In some cases, this is mediated by extracellular electron transfer (or EET), wherein electrons are transferred to extracellular oxidants such as iron oxide and manganese oxide minerals. Here, we show that an ammonia-oxidizer previously known to be strictly aerobic, Nitrosomonas communis, may have been able to utilize a poised electrode to maintain metabolic activity in anoxic conditions. The presence and activity of multi-heme cytochromes in N. communis further suggest a capacity for EET. Molecular clock analysis shows that the ancestors of β-proteobacterial ammonia oxidizers appeared after Earth's atmospheric oxygenation when the oxygen levels were >10-4  pO2 (PAL), consistent with aerobic origins. Equally important, phylogenetic reconciliations of gene and species trees show that the multi-heme c-type EET proteins in Nitrosomonas and Nitrosospira lineages were likely acquired by gene transfer from γ-proteobacteria when the oxygen levels were between 0.1 and 1 pO2 (PAL). These results suggest that β-proteobacterial EET evolved during the Proterozoic when oxygen limitation was widespread, but oxidized minerals were abundant.
Original languageEnglish
Article numbermsad161
JournalMolecular Biology and Evolution
Volume40
Issue number8
Number of pages13
ISSN0737-4038
DOIs
Publication statusPublished - 2023

Keywords

  • Extracellular electron transfer
  • Ammonia oxidizing bacteria
  • Multiheme cytochromes
  • Horizontal gene transfer
  • Hypoxic

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