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 μm h−1). 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 (∼100 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.
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Acknowledgements
TEM analyses were performed at the Berkeley National Center for Electron Microscopy, at the Marine Biological Laboratory and at the University of Delaware Bioimaging Facility. We thank Reena Zalpuri (Berkeley) for ultramicrotoming samples, Natalie Villa (University of Delaware) for performing lectin studies and Shawn French (University of Guelph) for providing LPS standard. We thank T Tyliszczak and ALD Kilcoyne for support at the Advanced Light Source BL11.0.2 and 5.3.2, respectively, and Jill Banfield for helpful discussions. Funding was provided by a NSF Ridge 2000 postdoctoral fellowship (CSC, KJE), by the NSF Microbial Observatories Program (KJE, DE) and by the NASA Astrobiology Institute (KJE, DE). ALS is supported by the Office of Science, Basic Energy Sciences, Division of Materials Science of the United States Department of Energy (DE-AC02-05CH11231).
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Chan, C., Fakra, S., Emerson, D. et al. Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5, 717–727 (2011). https://doi.org/10.1038/ismej.2010.173
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DOI: https://doi.org/10.1038/ismej.2010.173
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