Iron oxidation by a fused cytochrome-porin common to diverse iron-oxidizing bacteria

Abstract

SummaryFe oxidation is one of Earth’s major biogeochemical processes, key to weathering, soil formation, water quality, and corrosion. However, our ability to track the contributions of Fe-oxidizing microbes is limited by our relatively incomplete knowledge of microbial Fe oxidation mechanisms, particularly in neutrophilic Fe-oxidizers. The genomes of many Fe-oxidizers encode homologs to an outer-membrane cytochrome (Cyc2) that has been shown to oxidize Fe in two acidophiles. Here, we demonstrate the Fe oxidase function of a heterologously expressed Cyc2 homolog derived from a neutrophilic Fe oxidizer. Phylogenetic analyses show that Cyc2 from neutrophiles cluster together, suggesting a common function. Sequence analysis and modeling reveal the entire Cyc2 family is defined by a unique structure, a fused cytochromeporin, consistent with Fe oxidation on the outer membrane, preventing internal Fe oxide encrustation. Metatranscriptomes from Fe-oxidizing environments show exceptionally high expression of cyc2, supporting its environmental role in Fe oxidation. Together, these results provide evidence that cyc2 encodes Fe oxidases in diverse Fe-oxidizers and therefore can be used to recognize microbial Fe oxidation. The presence of cyc2 in 897 genomes suggests that microbial Fe oxidation may be a widespread metabolism.

Marine Fe-oxidizingZetaproteobacteria: Historical, ecological, and genomic perspectives

“…Based on this, the Fe oxidation pathway model for the Zetaproteobacteria was revised (Figure 8). Cyc2 homologs have been found in other Zetaproteobacteria and other neutrophilic FeOB, strengthening the proposed pathway (97, 98). In fact, every single ZOTU that has a genomic representative, including ZOTUs without isolates, has a homolog of this putative Fe oxidation gene, consistent with the notion that all Zetaproteobacteria are Fe-oxidizers (43, 95).…”

Intra-genus metabolic diversity facilitates co-occurrence of multiple Ferrovum species at an acid mine drainage site

“…Each genome contains high molecular weight, Cyc2-like proteins found in other Ferrovum taxa [16]. Cyc2-like proteins are found in many acidophilic and neutrophilic Fe(II) oxidizers and are highly expressed in their metatranscriptomes [31]. Therefore, this protein likely plays a role in Fe(II) oxidation.…”

Metabolic diversity and co-occurrence of multiple Ferrovum species at an acid mine drainage site

“…Cyc2 is an Fe oxidase [32,33]. Cyc2-like proteins are also highly expressed in neutrophilic Fe(II) oxidizers [34]. Therefore, this protein likely plays a role in Fe(II) oxidation in Ferrovum.…”