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Bacterial chemolithoautotrophy via manganese oxidation

Yu, Hang and Leadbetter, Jared R. (2020) Bacterial chemolithoautotrophy via manganese oxidation. Nature, 583 (7816). pp. 453-458. ISSN 0028-0836. https://resolver.caltech.edu/CaltechAUTHORS:20200408-160710037

[img] Image (JPEG) (Extended Data Fig. 1: Effect of temperature, anti-bacterials and Mn(II)Cl₂ on biological Mn(II)CO₃ oxidation) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 2: Mn(II) oxidation and growth by the co-culture) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 3: Properties of the refined co-culture) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 4: Microscopy of Mn oxide nodules formed by the co-culture) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 5: Phylogenetic analyses on species A) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 6: Phylogenetic analyses and aerobic heterotrophic growth of isolated species B) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 7: Phylogenetic analyses of cytochrome bd oxidase subunit I and cytochrome bd-like oxidases) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 8: Sequence alignment of cytochrome bd and bd-like oxidases) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 9: Stable isotope probing of Mn(II)-oxidizing co-culture measured using nanoSIMS) - Supplemental Material
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[img] MS Excel (Supplementary Table 1 - contains community profiles of Mn-oxidising enrichments by iTag sequencing of 16S rRNA genes) - Supplemental Material
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[img] MS Excel (Supplementary Table 3 - contains transcriptomics analyses of multiple biological replicates of the co-culture after oxidising different amounts of Mn(II)) - Supplemental Material
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Abstract

Manganese is one of the most abundant elements on Earth. The oxidation of manganese has long been theorized—yet has not been demonstrated—to fuel the growth of chemolithoautotrophic microorganisms. Here we refine an enrichment culture that exhibits exponential growth dependent on Mn(II) oxidation to a co-culture of two microbial species. Oxidation required viable bacteria at permissive temperatures, which resulted in the generation of small nodules of manganese oxide with which the cells associated. The majority member of the culture—which we designate ‘Candidatus Manganitrophus noduliformans’—is affiliated to the phylum Nitrospirae (also known as Nitrospirota), but is distantly related to known species of Nitrospira and Leptospirillum. We isolated the minority member, a betaproteobacterium that does not oxidize Mn(II) alone, and designate it Ramlibacter lithotrophicus. Stable-isotope probing revealed ¹³CO₂ fixation into cellular biomass that was dependent upon Mn(II) oxidation. Transcriptomic analysis revealed candidate pathways for coupling extracellular manganese oxidation to aerobic energy conservation and autotrophic CO₂ fixation. These findings expand the known diversity of inorganic metabolisms that support life, and complete a biogeochemical energy cycle for manganese that may interface with other major global elemental cycles.


Item Type:Article
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https://www.nature.com/articles/s41586-020-2468-5DOIArticle
https://rdcu.be/b5DrmPublisherFree ReadCube access
https://pubs.acs.org/doi/10.1021/cen-09828-scicon4Featured InC&EN -- Science Concentrates
ORCID:
AuthorORCID
Yu, Hang0000-0002-7600-1582
Leadbetter, Jared R.0000-0002-7033-0844
Alternate Title:Cultivation of manganese oxidising chemolithoautotrophic bacteria
Additional Information:© 2020 Springer Nature Limited. Received 26 September 2019; Accepted 05 May 2020; Published 15 July 2020. This work was supported by NASA Astrobiology Institute Exobiology grant #80NSSC19K0480; and by Caltech’s Center for Environmental Microbial Interactions and Division of Geological and Planetary Sciences. We thank S. Connon for assistance with iTag sequencing preparations; G. Rossman and U. Lingappa for spectroscopic analyses and minerology insights; G. Chadwick for discussions on physiology and bioenergetics; I. Antoshechkin and V. Kumar for assistance with nucleic acid library preparation and sequencing at the Millard and Muriel Jacobs Genetics and Genomics Laboratory; N. Dalleska for assistance with ICP–MS analyses at the Environmental Analysis Center; F. Gao for inputs on RNA data analysis using kallisto software at the Bioinformatics Resource Center in the Beckman Institute; C. Ma for assistance with SEM analyses at the GPS Analytical Facility; Y. Guan for assistance with nanoSIMS analyses at the GPS Microanalysis Center; and multiple colleagues for feedback before publication. Data availability: All sequencing data has been deposited at the NCBI under BioProject PRJNA562312. The cloned 16S rRNA gene sequences of ‘Candidatus Manganitrophus noduliformans’ (species A) and R. lithotrophicus (species B) from the co-culture have been deposited at GenBank under accession numbers MN381734 and MN381735, respectively. The iTAG sequences from the different enrichments have been deposited at the Sequence Read Archive (SRA) under accession numbers SRR10031198, SRR10031199 and SRR10031200. Genome sequences of the co-culture, from which the genome of ‘Candidatus Manganitrophus noduliformans’ was reconstructed, have been deposited under BioSample SAMN12638105 with raw sequences deposited at SRA under accession number SRR10032644; the reconstructed genome of ‘Candidatus Manganitrophus noduliformans’ has been deposited at DDBJ/ENA/GenBank under accession number VTOW00000000. Genome sequences of R. lithotrophicus strain RBP-1 have been deposited under BioSample SAMN12638106, with raw sequences deposited at SRA under accession number SRR10031379; the reconstructed genome of R. lithotrophicus strain RBP-1 has been deposited at DDBJ/ENA/GenBank under accession number VTOX00000000. Additionally, reconstructed genomes have been deposited in Joint Genome Institute (JGI) Genomes Online Database Study ID Gs0134339, with Integrated Microbial Genome ID 2784132095 for ‘Candidatus Manganitrophus noduliformans’ and ID 2778260901 for R. lithotrophicus strain RBP-1. Transcriptome sequence data for the seven biological replicates have been deposited at SRA under accession numbers SRR10060009, SRR10060010, SRR10060011, SRR10060012, SRR10060013, SRR10060017 and SRR10060018. Unique biological materials are available from the corresponding author upon reasonable request. Source data are provided with this paper. Author Contributions: H.Y. and J.R.L. together applied for funding, designed and conducted the experiments, performed data analyses, prepared the figures and wrote the manuscript. The authors declare no competing interests. Peer review information: Nature thanks Edward F. DeLong, Philip Hugenholtz, Bradley M. Tebo, Michael Wagner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Group:Caltech Center for Environmental Microbial Interactions (CEMI), Millard and Muriel Jacobs Genetics and Genomics Laboratory
Funders:
Funding AgencyGrant Number
NASA80NSSC19K0480
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Caltech Division of Geological and Planetary SciencesUNSPECIFIED
Issue or Number:7816
Record Number:CaltechAUTHORS:20200408-160710037
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200408-160710037
Official Citation:Yu, H., Leadbetter, J.R. Bacterial chemolithoautotrophy via manganese oxidation. Nature 583, 453–458 (2020). https://doi.org/10.1038/s41586-020-2468-5
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:102416
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:13 Jul 2020 20:31
Last Modified:20 Jul 2020 16:32

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