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The ISME Journal (2013) 7, 338350 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 http://www.nature.com/ismej
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ORIGINAL ARTICLE
Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth
Birgit Luef1,2, Sirine C Fakra1,3, Roseann Csencsits2, Kelly C Wrighton1, Kenneth H Williams4, Michael J Wilkins5, Kenneth H Downing2, Philip E Long4, Luis R Comolli2 and Jillian F Banfield1,6
1Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, CA, USA;
2Lawrence Berkeley National Laboratory, Life Sciences Division, Berkeley, CA, USA; 3Lawrence Berkeley National Laboratory, Advanced Light Source, Berkeley, CA, USA; 4Lawrence Berkeley National Laboratory, Earth Sciences Division, Berkeley, CA, USA; 5Pacific Northwest National Laboratory, Biological Sciences Division, Richland, WA, USA and 6Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA, USA
Iron-reducing bacteria (FeRB) play key roles in anaerobic metal and carbon cycling and carry out biogeochemical transformations that can be harnessed for environmental bioremediation. A subset of FeRB require direct contact with Fe(III)-bearing minerals for dissimilatory growth, yet these bacteria must move between mineral particles. Furthermore, they proliferate in planktonic consortia during biostimulation experiments. Thus, a key question is how such organisms can sustain growth under these conditions. Here we characterized planktonic microbial communities sampled from an aquifer in Rifle, Colorado, USA, close to the peak of iron reduction following in situ acetate amendment. Samples were cryo-plunged on site and subsequently examined using correlated twoand three-dimensional cryogenic transmission electron microscopy (cryo-TEM) and scanning transmission X-ray microscopy (STXM). The outer membranes of most cells were decorated with aggregates up to 150 nm in diameter composed of B3 nm wide amorphous, Fe-rich nanoparticles.
Fluorescent in situ hybridization of lineage-specific probes applied to rRNA of cells subsequently imaged via cryo-TEM identified Geobacter spp., a well-studied group of FeRB. STXM results at the Fe L2,3 absorption edges indicate that nanoparticle aggregates contain a variable mixture of Fe(II) Fe(III), and are generally enriched in Fe(III). Geobacter bemidjiensis cultivated anaerobically in the laboratory on acetate and hydrous ferric oxyhydroxides also accumulated mixed-valence nanoparticle aggregates. In field-collected samples, FeRB with a wide variety of morphologies were associated with nano-aggregates, indicating that cell surface Fe(III) accumulation may be a general mechanism by which FeRB can grow while in planktonic suspension.
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