Leptothrix ochracea Genomes Reveal Potential for Mixotrophic Growth by Oxidation of Iron and Organic Carbon


Gracee K. Tothero1* (gtothero@udel.edu), Ibrahim F. Farag1, Daniel I. Kaplan2, Pamela Weisenhorn3, Clara S. Chan1 (cschan@udel.edu)


1University of Delaware, Newark, DE; 2University of Georgia, Athens, GA; 3Argonne National Laboratory, Lemont, IL


Iron oxyhydroxides are extremely reactive components of environmental systems, exerting a strong influence on biogeochemical cycles, so the project aims to understand the controls on iron oxidation, particularly by microorganisms. At the Savannah River Site (SRS) in South Carolina, extensive iron-oxidizing microbial mats carpet streams and wetlands, sorbing uranium and other metals, and thus mediate the transport and availability of toxins. To understand the drivers of these processes, researchers need to determine the niche and physiology of iron-oxidizing bacteria (FeOB). Neutrophilic FeOB are typically considered chemolithoautotrophs, using the energy of iron oxidation to fix carbon, but this potentially limits FeOB impacts given the low energetic yield of iron oxidation and the high costs of autotrophy. Therefore, the team posited that wetland FeOB may in fact utilize organic carbon, making organic carbon availability an important factor in iron oxidation and metal sequestration.

The iron microbial mats in Tims Branch stream and wetlands at the SRS are comprised of iron-mineralized sheaths typical of Leptothrix ochracea, an organism first described in 1888 by Winogradsky, who hypothesized that it grows a chemolithoautotrophic iron oxidizer. However, it has never been isolated and does not have a complete genome sequence available, so its physiological roles in iron and carbon cycling are very limited. These iron microbial mats were analyzed using 16S rRNA molecular surveys and by SILVA classification. Leptothrix was poorly detected (up to 0.004%) despite the obvious presence of sheaths. This is consistent with the rarity of L. ochracea in similar molecular surveys. Researchers performed whole-genome sequencing on nine iron microbial mats from stream and wetland sites from the SRS; eight high-quality genomes of L. ochracea were reconstructed from these mats. A full 16S rRNA sequence was recovered from one L. ochracea genome, which can be used as a reference for detecting L. ochracea. On reexamination of the 16S data, L. ochracea was present up to 8.2% relative abundance. All eight genomes contained genes for iron oxidation, carbon fixation, and utilization of organic acids and polysaccharides, demonstrating the potential for L. ochracea to grow as a mixotroph, i.e., using both iron(II) and organic carbon. To further investigate this potential, researchers computed stoichiometric metabolic models, which demonstrated the potential for growth using lactate. In sum, results suggest that organic carbon availability is an important driver of microbial iron oxidation and associated toxic metal bioremediation in these wetland environments.