Biomineralization by neutrophilic, lithotrophic iron-oxidizing bacteria
Date
2011
Authors
Journal Title
Journal ISSN
Volume Title
Publisher
University of Delaware
Abstract
Biogenic Fe oxides influence the cycling of nutrients and contaminants in the environment, and may hold clues to understanding environments on ancient Earth. In many freshwater and marine habitats, these minerals are produced by lithotrophic bacteria that inhabit low-oxygen zones of redox gradients and comprise a significant part of the microbial community. Extracellular Fe-organic bacteriogenic filaments, such as the widely-observed Gallionella-like stalks often dominate the structures of Fe mats. Scientific interest in neutrophilic, lithotrophic FeOB is due to their influence on modern biogeochemical cycles, as well as their possible activities throughout Earth history (for instance, deposition of the Precambrian banded iron formations). In spite of this interest, much remains unknown about the diversity and physiology of these organisms, and their formation of filamentous Fe mats. Fe-depositing microbes were first recognized in the first half of the 19th Century, however our understanding of microbial Fe oxidation and biomineralization is limited, in part, because few FeOB isolates exist. Furthermore, there are no available freshwater isolates that form filamentous mats. Therefore, the first objective of the research presented here was to isolate a novel Fe stalk-forming FeOB from a freshwater environment. We successfully isolated strain R-1 from an Fe seep in Newark, DE, and characterized its physiology and phylogeny. Our results show that strain R-1 is a novel Betaproteobacterium, specially adapted for Fe(II) oxidation in circumneutral, freshwater settings. To our knowledge, this is the first reported stalk-forming freshwater FeOB isolate distinct from Gallionella. Strain R-1 provides a new model system for microbial Fe(II) oxidation and biomineralization. The morphology and texture of filamentous Fe mats are promising biosignatures for FeOB, which, if identified in the fossil record, would provide a new line of evidence toward understanding the history of oxygen on Earth. Therefore, the second goal of this work was to link filamentous Fe mats to microbial physiology and oxygen conditions. We studied growth and biomineralization by strain R-1 and marine FeOB Mariprofundus ferrooxydans in flat glass microslide growth chambers with opposing oxygen and Fe(II) gradients. Cultures were incubated over a range of oxygen levels and growth and mineral formation were documented by light microscopy. Filament widths and directional orientations were also quantified, and we made observations of Fe filaments in a ~170 million-year-old silica-Fe hydrothermal deposit. We argue that FeOB are active and produce recognizably biogenic Fe oxides even at extremely low oxygen levels, and that these oxides could serve as redox proxies in the geologic record.