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Published March 2022 | Supplemental Material + Submitted + Published
Journal Article Open

Comparative Genomics on Cultivated and Uncultivated Freshwater and Marine "Candidatus Manganitrophaceae" Species Implies Their Worldwide Reach in Manganese Chemolithoautotrophy

Abstract

Chemolithoautotrophic manganese oxidation has long been theorized but only recently demonstrated in a bacterial coculture. The majority member of the coculture, "Candidatus Manganitrophus noduliformans," is a distinct but not yet isolated lineage in the phylum Nitrospirota (Nitrospirae). Here, we established two additional MnCO₃-oxidizing cultures using inocula from Santa Barbara (California) and Boetsap (South Africa). Both cultures were dominated by strains of a new species, designated "Candidatus Manganitrophus morganii." The next most abundant members differed in the available cultures, suggesting that while "Ca. Manganitrophus" species have not been isolated in pure culture, they may not require a specific syntrophic relationship with another species. Phylogeny of cultivated "Ca. Manganitrophus" and related metagenome-assembled genomes revealed a coherent taxonomic family, "Candidatus Manganitrophaceae," from both freshwater and marine environments and distributed globally. Comparative genomic analyses support this family being Mn(II)-oxidizing chemolithoautotrophs. Among the 895 shared genes were a subset of those hypothesized for Mn(II) oxidation (Cyc2 and PCC_1) and oxygen reduction (TO_1 and TO_2) that could facilitate Mn(II) lithotrophy. An unusual, plausibly reverse complex 1 containing 2 additional pumping subunits was also shared by the family, as were genes for the reverse tricarboxylic acid carbon fixation cycle, which could enable Mn(II) autotrophy. All members of the family lacked genes for nitrification found in Nitrospira species. The results suggest that "Ca. Manganitrophaceae" share a core set of candidate genes for the newly discovered manganese-dependent chemolithoautotrophic lifestyle and likely have a broad, global distribution.

Additional Information

© 2022 Yu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 12 November 2021; Accepted 24 February 2022; Published 14 March 2022. We thank Stephanie Connon for assistance with 16S rRNA gene amplicon sequencing and analysis. We thank the two anonymous reviewers for their constructive comments on the manuscript. This work was supported by NASA Astrobiology Institute Exobiology grant number 80NSSC19K0480 and by Caltech's Center for Environmental Microbial Interactions and Division of Geological and Planetary Sciences. Fieldwork in South Africa by U.F.L. was supported by Woodward Fischer (Caltech) under grants from the NSF (IOS-1833247) and the Packard Foundation. Data availability: The partial 16S rRNA gene amplicon sequences of enrichment cultures and metagenome-assembled genomes of "Candidatus Manganitrophus morganii" strains SA1 and SB1 have been deposited with the National Center for Biotechnology Information (NCBI) under BioProject no. PRJNA776098. The authors declare no conflict of interest.

Attached Files

Published - mbio.03421-21.pdf

Submitted - 2021.11.15.468770v1.full.pdf

Supplemental Material - mbio.03421-21-s0001.docx

Supplemental Material - mbio.03421-21-sf001.jpg

Supplemental Material - mbio.03421-21-sf002.jpg

Supplemental Material - mbio.03421-21-st001.xlsx

Supplemental Material - mbio.03421-21-st002.docx

Supplemental Material - mbio.03421-21-st003.docx

Supplemental Material - mbio.03421-21-st004.docx

Supplemental Material - mbio.03421-21-st005.docx

Supplemental Material - mbio.03421-21-st006.xlsx

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Additional details

Created:
August 20, 2023
Modified:
October 23, 2023