Leptothrix ochracea genomes reveal potential for mixotrophic growth on Fe(II) and organic carbon
| Author(s) | Tothero, Gracee K. | |
| Author(s) | Hoover, Rene L. | |
| Author(s) | Farag, Ibrahim F. | |
| Author(s) | Kaplan, Daniel I. | |
| Author(s) | Weisenhorn, Pamela | |
| Author(s) | Emerson, David | |
| Author(s) | Chan, Clara S. | |
| Date Accessioned | 2024-08-21T14:44:29Z | |
| Date Available | 2024-08-21T14:44:29Z | |
| Publication Date | 2024-08-12 | |
| Description | This article was originally published in Applied and Environmental Microbiology. The version of record is available at: https://doi.org/10.1128/aem.00599-24. © 2024 Tothero et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/). | |
| 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. IMPORTANCE Winogradsky's observations of L. ochracea led him to propose autotrophic iron oxidation as a new microbial metabolism, following his work on autotrophic sulfur-oxidizers. While much culture-based research has ensued, isolation proved elusive, so most work on L. ochracea has been based in the environment and in microcosms. Meanwhile, the autotrophic Gallionella became the model for freshwater microbial iron oxidation, while heterotrophic and mixotrophic iron oxidation is not well-studied. Ecological studies have shown that Leptothrix overtakes Gallionella when dissolved organic carbon content increases, demonstrating distinct niches. This study presents the first near-complete genomes of L. ochracea, which share some features with autotrophic iron oxidizers, while also incorporating heterotrophic metabolisms. These genome, metabolic modeling, and transcriptome results give us a detailed metabolic picture of how the organism may combine lithoautotrophy with organoheterotrophy to promote Fe oxidation and C cycling and drive many biogeochemical processes resulting from microbial growth and iron oxyhydroxide formation in wetlands. | |
| Sponsor | We thank John Seaman of the Savannah River Ecology laboratory for hosting us in his lab during our SRS field work. We acknowledge Bruce Kingham and Mark Shaw at the University of Delaware DNA Sequencing and Genotyping Center for performing the SRS 16S rRNA amplicon and metagenome sequencing, Andre Comeau at the Integrated Microbial Resource sequencing center for assistance with Spruce Point metagenome sequencing, Tijana Galvina del Rio and Natasha Brown from the Joint Genome Institute for assistance with the metatranscriptome sequencing, Deborah Powell at the University of Delaware Bioimaging Center for performing SEM sample preparation and imaging, and Austin Chambers and Christopher Blanda for writing a custom Python script for detecting MCO motifs. We are grateful to Cara Santelli and Crystal Ng for the use of their diffusion sampler equipment at the Savannah River Site. We thank Chris Henry, Jose Faria, Filipe Liu, and Andrew Freiburger for access to and assistance with KBase metabolic modeling tools. We thank Jarrod Scott for performing DNA isolation and organizing metagenome sequencing for the Spruce Point sample and Emily Fleming for discussions and feedback. This work was supported by a DOE ESS Grant DE-SC0021010 to C.S.C., NSF EAR- 2243577 and EAR-18833525 to C.S.C., DOE ESS Contract DE-AC02-06CH11357 to P.B.W. and D.I.K., and NSF grant OIA-1826734 to D.E. G.K.T. was also supported by a fellowship from the University of Delaware Microbiology Graduate Program and Unidel Foundation. Support from the University of Delaware Center for Bioinformatics and Computational Biology Core Facility, including the use of the BIOMIX computer cluster, was made possible through funding from Delaware INBRE (NIH P20GM103446), the State of Delaware, and the Delaware Biotechnology Institute. Support was also received from DOE-EM through the Cooperative Agreement DE-EM0005228 to SREL/UGA. | |
| Citation | Tothero GK, Hoover RL, Farag IF, Kaplan DI, Weisenhorn P, Emerson D, Chan CS.0.Leptothrix ochracea genomes reveal potential for mixotrophic growth on Fe(II) and organic carbon. Appl Environ Microbiol0:e00599-24.https://doi.org/10.1128/aem.00599-24 | |
| ISSN | 1098-5336 | |
| URL | https://udspace.udel.edu/handle/19716/34791 | |
| Language | en_US | |
| Publisher | Applied and Environmental Microbiology | |
| dc.rights | Attribution 4.0 International | en |
| dc.rights.uri | http://creativecommons.org/licenses/by/4.0/ | |
| Keywords | Leptothrix ochracea | |
| Keywords | chemolithotrophy | |
| Keywords | mixotrophy | |
| Keywords | iron-oxidizing bacteria | |
| Keywords | iron microbial mats | |
| Title | Leptothrix ochracea genomes reveal potential for mixotrophic growth on Fe(II) and organic carbon | |
| Type | Article |
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