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Twisted stalks are morphologically unique bacterial extracellular organo-metallic structures containing Fe(III) oxyhydroxides that are produced by microaerophilic Fe(II)-oxidizers belonging to the Betaproteobacteria and Zetaproteobacteria. Understanding the underlying genetic and physiological mechanisms of stalk formation is of great interest based on their potential as novel biogenic nanomaterials and their relevance as putative biomarkers for microbial Fe(II) oxidation on ancient Earth. Despite the recognition of these special biominerals for over 150 years, the genetic foundation for the stalk phenotype has remained unresolved. Here we present a candidate gene cluster for the biosynthesis and secretion of the stalk organic matrix that we identified with a trait-based analyses of a pan-genome comprising 16 Zetaproteobacteria isolate genomes. The “ s talk  f ormation in  Z etaproteobacteria”  (sfz)  cluster comprises six genes ( sfz1-sfz6 ), of which  sfz1  and  sfz2  were predicted with functions in exopolysaccharide synthesis, regulation, and export,  sfz4  and  sfz6  with functions in cell wall synthesis manipulation and carbohydrate hydrolysis, and  sfz3  and  sfz5  with unknown functions. The stalk-forming Betaproteobacteria  Ferriphaselus  R-1 and OYT-1, as well as dread-forming Zetaproteobacteria  Mariprofundus aestuarium  CP-5 and  Mariprofundus ferrinatatus  CP-8 contain distant  sfz  gene homologs, whereas stalk-less Zetaproteobacteria and Betaproteobacteria lack the entire gene cluster. Our pan-genome analysis further revealed a significant enrichment of clusters of orthologous groups (COGs) across all Zetaproteobacteria isolate genomes that are associated with the regulation of a switch between sessile and motile growth controlled by the intracellular signaling molecule c-di-GMP. Potential interactions between stalk-former unique transcription factor genes,  sfz  genes, and c-di-GMP point toward a c-di-GMP regulated surface attachment function of stalks during sessile growth.

Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export