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

被引:298
作者
Chan, Clara S. [1 ,2 ,3 ]
Fakra, Sirine C. [4 ]
Emerson, David [5 ]
Fleming, Emily J. [5 ]
Edwards, Katrina J. [2 ,3 ]
机构
[1] Woods Hole Oceanog Inst, Dept Marine Chem & Geochem, Woods Hole, MA 02543 USA
[2] Univ So Calif, Dept Biol Sci, Los Angeles, CA 90089 USA
[3] Univ So Calif, Dept Earth Sci, Los Angeles, CA 90089 USA
[4] Univ Calif Berkeley, Lawrence Berkeley Lab, Berkeley, CA 94720 USA
[5] Bigelow Lab Ocean Sci, W Boothbay Harbor, ME USA
基金
美国能源部; 美国国家科学基金会;
关键词
biomineralization; Gallionella; Mariprofundus ferrooxydans; spectromicroscopy; Zetaproteobacteria; X-RAY MICROSCOPY; HYDROTHERMAL VENTS; FE(II)-OXIDIZING BACTERIA; GALLIONELLA-FERRUGINEA; CONSPICUOUS VEILS; SPECTROSCOPY; OXYGEN; OXIDATION; OXIDE; BIOMINERALIZATION;
D O I
10.1038/ismej.2010.173
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
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 mu m 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 (similar to 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. The ISME Journal (2011) 5, 717-727; doi:10.1038/ismej.2010.173; published online 25 November 2010
引用
收藏
页码:717 / 727
页数:11
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