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Fe(III) Mineral Encrustation Uncouples Respiration from Reproduction of the Nitrate-Reducing Fe(II)-Oxidizing bacterium Acidovorax sp. BoFeN1

ABSTRACT: Fe(II) can be oxidized by mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria to Fe(III), leading to mineral precipitation. However, the effects of this process on the metabolism and reproduction ability of the Fe(II)-oxidizing bacterial cells have not yet been quantified. In this study, we investigated the effects of Fe(II) on the mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria Acidovorax sp. BoFeN1 by performing cell plate counts, chemical analyses, and scanning electron microscopy (SEM) imaging. The result showed that nitrate-reducing Fe(II)-oxidizing bacteria Acidovorax sp. BoFeN1 undergoes a striking physiological state in which respiration persists while cell reproduction collapses after their oxidation of Fe(II). Across 0.1–10 mM Fe(II), colony-forming units dropped by up to 103-fold, yet acetate consumption remained largely unaffected and nitrate reduction was even slightly promoted. SEM-EDS reveals extensive Fe(III) encrustation on cells. Adding an Fe(III) chelator, citrate, restored reproductive capacity without notably changes in Fe(II) oxidation or nitrate reduction, indicating that it was the products of Fe(II) oxidation, the secondary Fe(III) minerals, that impaired cell reproduction. These findings uncover a mineral encrustation-driven uncoupling between respiration and reproduction, suggest how natural organic ligands may buffer NRFeOx bacterial communities in Fe-rich anoxic environments, and point to cellular-level levers for mitigating denitrification failures and N2O risks in engineered and natural systems.

ORGANISM(S): Acidovorax

SUBMITTER: Chao Peng

PROVIDER: PXD072688 | iProX | Thu Jan 01 00:00:00 GMT 2026

REPOSITORIES: iProX

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Project description:Haloalkaliphilic microorganisms are double extremophiles functioning optimally at high salinity and pH. Their typical habitats are soda lakes, representing geologically ancient ecosystems which are still widespread on Earth and supposedly harbor relict microbial communities. We compared metabolic features and their genomic determinants in two strains of a single natronophilic species Dethiobacter alkaliphilus, the only cultured representative of “Dethiobacteria” class within Bacillota phylum. The strains of D. alkaliphilus were previously isolated from geographically remote Mongolian and Kenyan soda lakes. The type strain AHT1T was described as a facultatively chemolithoautotrophic sulfidogen reducing or disproportionating sulfur or thiosulfate, while strain Z-1002 was isolated as a chemolithoautotrophic iron reducer. Here, we uncovered iron reducing ability of strain AHT1T, as well as the capability of strain Z-1002 for thiosulfate reduction and anaerobic Fe(II) oxidation. Key catabolic processes sustaining the growth of both strains appeared to fit the geochemical settings of two contrasting natural alkaline environments, sulfur-enriched soda lakes and iron-enriched serpentinites. This assumption was supported by meta-analysis of publicly available Dethiobacterial metagenomes, as well as by the enrichment of a novel phylotype from a deep subsurface non-serpentinizing slightly alkaline water after its amendment with an Fe(III) mineral. Genome analysis of D. alkaliphilus strains revealed that the most probable determinants of iron and sulfur redox transformations in the organism are multiheme c-type cytochromes. Their phylogeny reconstruction showed that sulfur and thiosulfate respiration is most probably provided by evolutionary early forms of unconventional octaheme tetrathionate and sulfite reductases sharing a root with structurally similar group of OmhA/OcwA Fe(III)-reductases. Large sets of other multihemes are likely to provide Fe(III) reduction in both strains. Also, several different, yet phylogenetically related, determinants of anaerobic Fe(II) oxidation were identified in Z-1002 genome, and the oxidation process was further experimentally proven. Considering these results and phylogenetic relatedness of D. alkaliphilus’s sulfur reductases with Fe(III) reducing cytochromes, but not with archetypal bacterial sulfur/thiosulfate reductases, we suggest that sustaining high variation of multiheme cytochromes is an effective adaptive strategy to occupy geochemically contrasting alkaline anaerobic environments. We further propose that sulfur-enriched soda lakes are secondary habitats for D. alkaliphilus comparing to Fe-rich serpentinites, and discuss the evolutionary traits which might occur in prokaryotes on a crucial junction of the biosphere’s history, when intensification of the sulfur cycle outweighed the global significance of the iron cycle.

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Fe(III) Mineral Encrustation Uncouples Respiration from Reproduction of the Nitrate-Reducing Fe(II)-Oxidizing bacterium Acidovorax sp. BoFeN1

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