Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation

Abstract

Neutrophilic Fe-oxidizing bacteria (FeOB) are often identified by their distinctive morphologies, such as the extracellular twisted ribbon-like stalks formed by Gallionella ferruginea or Mariprofundus ferrooxydans. Similar filaments preserved in silica are often identified as FeOB fossils in rocks. Although it is assumed that twisted iron stalks are indicative of FeOB, the stalk's metabolic role has not been established. To this end, we studied the marine FeOB M. ferrooxydans by light, X-ray and electron microscopy. Using time-lapse light microscopy, we observed cells excreting stalks during growth (averaging 2.2 lm h À1 ). Scanning transmission X-ray microscopy and near-edge X-ray absorption fine structure (NEXAFS) spectroscopy show that stalks are Fe(III)-rich, whereas cells are low in Fe. Transmission electron microscopy reveals that stalks are composed of several fibrils, which contain few-nanometer-sized iron oxyhydroxide crystals. Lepidocrocite crystals that nucleated on the fibril surface are much larger (B100 nm), suggesting that mineral growth within fibrils is retarded, relative to sites surrounding fibrils. C and N 1s NEXAFS spectroscopy and fluorescence probing show that stalks primarily contain carboxyl-rich polysaccharides. On the basis of these results, we suggest a physiological model for Fe oxidation in which cells excrete oxidized Fe bound to organic polymers. These organic molecules retard mineral growth, preventing cell encrustation. This model describes an essential role for stalk formation in FeOB growth. We suggest that stalk-like morphologies observed in modern and ancient samples may be correlated confidently with the Fe-oxidizing metabolism as a robust biosignature.

Ferriphaselus amnicola gen. nov., sp. nov., a neutrophilic, stalk-forming, iron-oxidizing bacterium isolated from an iron-rich groundwater seep

“…All stalks represented a left-handed (S-type) helical structure. As with stalks produced by strain R-1 (Krepski et al, 2012) and M. ferrooxydans (Chan et al, 2011), stalks of strain OYT1 T contained polysaccharides (Fig. S2), as determined by lectin-staining with concanavalin A, as described previously (Chan et al, 2011).…”

<i>Acidithiobacillus ferrooxidans</i> as a Bioelectrocatalyst for Conversion of Atmospheric CO₂ into Extracellular Pyruvic Acid

“…We speculate that organic acids, such as pyruvic acid, diffuse into the cytoplasm of cells, where they subsequently dissociate and acidify the cytoplasm, resulting in loss of the PMF, 9 11 which is responsible for the uphill ET of approximately 1 eV (see Fig. 1 12 which has the remarkable ability to synthesize biopolymers at a rate of 2.6 µm h ¹1 , 13 are needed to confirm the potential of Fe 2+ -oxidizing chemoautotrophs as bioelectrocatalysts for CO 2 fixation and the production of valuable chemicals in extracellular environments. …”

Genomic insights into the uncultivated marine Zetaproteobacteria at Loihi Seamount

“…The Zetaproteobacteria create distinct extracellular structures, such as helical stalks (Singer et al, 2011) and tubular sheaths (Fleming et al, 2013), that are composed primarily of iron oxyhydroxides and organic polymers (Chan et al, 2011). These structures are a by-product of their metabolism and are capable of creating a structured habitat, both physically and chemically, within the environment.…”