SREL Reprint #3788

Leptothrix ochracea genomes reveal potential for mixotrophic growth on Fe(II) and organic carbon

Gracee K. Tothero1,2,3, Rene L. Hoover1,2,3, Ibrahim F. Farag4, Daniel I. Kaplan5, Pamela Weisenhorn6,
David Emerson7, and Clara S. Chan1,2,3,4

1Microbiology Graduate Program, University of Delaware, Newark, Delaware, USA
2Delaware Biotechnology Institute, Newark, Delaware, USA
3Department of Earth Sciences, University of Delaware, Newark, Delaware, USA
4School of Marine Science and Policy, University of Delaware, Newark, Delaware, USA
5Savannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina, USA
6Argonne National Laboratory, Lemont, Illinois, USA
7Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine, USA

Abstract: Leptothrix ochracea creates distinctive iron-mineralized mats that carpet streams and wetlands. Easily recognized by its iron-mineralized sheaths, L. ochracea was one of the first microorganisms described in the 1800s. Yet it has never been isolated and does not have a complete genome sequence available, so key questions about its physiology remain unresolved. It is debated whether iron oxidation can be used for energy or growth and if L. ochracea is an autotroph, heterotroph, or mixotroph. To address these issues, we sampled L. ochracea-rich mats from three of its typical environments (a stream, wetlands, and a drainage channel) and reconstructed nine high-quality genomes of L. ochracea from metagenomes. These genomes contain iron oxidase genes cyc2 and mtoA, showing that L. ochracea has the potential to conserve energy from iron oxidation. Sox genes confer potential to oxidize sulfur for energy. There are genes for both carbon fixation (RuBisCO) and utilization of sugars and organic acids (acetate, lactate, and formate). In silico stoichiometric metabolic models further demonstrated the potential for growth using sugars and organic acids. Metatranscriptomes showed a high expression of genes for iron oxidation; aerobic respiration; and utilization of lactate, acetate, and sugars, as well as RuBisCO, supporting mixotrophic growth in the environment. In summary, our results suggest that L. ochracea has substantial metabolic flexibility. It is adapted to iron-rich, organic carbon-containing wetland niches, where it can thrive as a mixotrophic iron oxidizer by utilizing both iron oxidation and organics for energy generation and both inorganic and organic carbon for cell and sheath production.

Keywords: Leptothrix ochracea, chemolithotrophy, mixotrophy, iron-oxidizing bacteria, iron microbial mats

SREL Reprint #3788

Tothero, G. K., R. L. Hoover, I. F. Farag, D. I. Kaplan, P. Weisenhorn, D. Emerson, and C. S. Chan. 2024. Leptothrix ochracea genomes reveal potential for mixotrophic growth on Fe(II) and organic carbon. Applied and Environmental Microbiology 90(9).

This information was provided by the University of Georgia's Savannah River Ecology Laboratory (srel.uga.edu).