Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes

Background: Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals releases phosphate and lanthanides to the biosphere. Currently, the microorganisms involved in phosphate mineral dissolu...

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Published in:BMC Biology
Main Authors: Voutsinos, Marcos Y., West-Roberts, Jacob A., Sachdeva, Rohan, Moreau, John W., Banfield, Jillian F.
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central 2024
Subjects:
Online Access:https://eprints.gla.ac.uk/320514/
https://eprints.gla.ac.uk/320514/2/320514.pdf
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spelling ftuglasgow:oai:eprints.gla.ac.uk:320514 2024-05-19T07:38:54+00:00 Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes Voutsinos, Marcos Y. West-Roberts, Jacob A. Sachdeva, Rohan Moreau, John W. Banfield, Jillian F. 2024-02-19 text https://eprints.gla.ac.uk/320514/ https://eprints.gla.ac.uk/320514/2/320514.pdf en eng BioMed Central https://eprints.gla.ac.uk/320514/2/320514.pdf Voutsinos, M. Y., West-Roberts, J. A., Sachdeva, R., Moreau, J. W. <http://eprints.gla.ac.uk/view/author/51704.html> and Banfield, J. F. (2024) Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes. BMC Biology <https://eprints.gla.ac.uk/view/journal_volume/BMC_Biology.html>, 22(1), 41. (doi:10.1186/s12915-024-01841-0 <https://doi.org/10.1186/s12915-024-01841-0>) (PMID:38369453) (PMCID:PMC10875860) cc_by_4 Articles PeerReviewed 2024 ftuglasgow https://doi.org/10.1186/s12915-024-01841-0 2024-05-01T14:04:01Z Background: Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals releases phosphate and lanthanides to the biosphere. Currently, the microorganisms involved in phosphate mineral dissolution and the role of lanthanides in microbial metabolism are poorly understood. Results: Although there have been many studies of soil microbiology, very little research has investigated microbiomes of weathered rock. Here, we sampled weathered granite and associated soil to identify the zones of lanthanide phosphate mineral solubilisation and genomically define the organisms implicated in lanthanide utilisation. We reconstructed 136 genomes from 11 bacterial phyla and found that gene clusters implicated in lanthanide-based metabolism of methanol (primarily xoxF3 and xoxF5) are surprisingly common in microbial communities in moderately weathered granite. Notably, xoxF3 systems were found in Verrucomicrobia for the first time, and in Acidobacteria, Gemmatimonadetes and Alphaproteobacteria. The xoxF-containing gene clusters are shared by diverse Acidobacteria and Gemmatimonadetes, and include conserved hypothetical proteins and transporters not associated with the few well studied xoxF systems. Given that siderophore-like molecules that strongly bind lanthanides may be required to solubilise lanthanide phosphates, it is notable that candidate metallophore biosynthesis systems were most prevalent in bacteria in moderately weathered rock, especially in Acidobacteria with lanthanide-based systems. Conclusions: Phosphate mineral dissolution, putative metallophore production and lanthanide utilisation by enzymes involved in methanol oxidation linked to carbonic acid production co-occur in the zone of moderate granite weathering. In combination, these microbial processes likely accelerate the conversion of granitic rock to soil. Article in Journal/Newspaper Carbonic acid University of Glasgow: Enlighten - Publications BMC Biology 22 1
institution Open Polar
collection University of Glasgow: Enlighten - Publications
op_collection_id ftuglasgow
language English
description Background: Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals releases phosphate and lanthanides to the biosphere. Currently, the microorganisms involved in phosphate mineral dissolution and the role of lanthanides in microbial metabolism are poorly understood. Results: Although there have been many studies of soil microbiology, very little research has investigated microbiomes of weathered rock. Here, we sampled weathered granite and associated soil to identify the zones of lanthanide phosphate mineral solubilisation and genomically define the organisms implicated in lanthanide utilisation. We reconstructed 136 genomes from 11 bacterial phyla and found that gene clusters implicated in lanthanide-based metabolism of methanol (primarily xoxF3 and xoxF5) are surprisingly common in microbial communities in moderately weathered granite. Notably, xoxF3 systems were found in Verrucomicrobia for the first time, and in Acidobacteria, Gemmatimonadetes and Alphaproteobacteria. The xoxF-containing gene clusters are shared by diverse Acidobacteria and Gemmatimonadetes, and include conserved hypothetical proteins and transporters not associated with the few well studied xoxF systems. Given that siderophore-like molecules that strongly bind lanthanides may be required to solubilise lanthanide phosphates, it is notable that candidate metallophore biosynthesis systems were most prevalent in bacteria in moderately weathered rock, especially in Acidobacteria with lanthanide-based systems. Conclusions: Phosphate mineral dissolution, putative metallophore production and lanthanide utilisation by enzymes involved in methanol oxidation linked to carbonic acid production co-occur in the zone of moderate granite weathering. In combination, these microbial processes likely accelerate the conversion of granitic rock to soil.
format Article in Journal/Newspaper
author Voutsinos, Marcos Y.
West-Roberts, Jacob A.
Sachdeva, Rohan
Moreau, John W.
Banfield, Jillian F.
spellingShingle Voutsinos, Marcos Y.
West-Roberts, Jacob A.
Sachdeva, Rohan
Moreau, John W.
Banfield, Jillian F.
Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
author_facet Voutsinos, Marcos Y.
West-Roberts, Jacob A.
Sachdeva, Rohan
Moreau, John W.
Banfield, Jillian F.
author_sort Voutsinos, Marcos Y.
title Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
title_short Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
title_full Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
title_fullStr Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
title_full_unstemmed Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
title_sort weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes
publisher BioMed Central
publishDate 2024
url https://eprints.gla.ac.uk/320514/
https://eprints.gla.ac.uk/320514/2/320514.pdf
genre Carbonic acid
genre_facet Carbonic acid
op_relation https://eprints.gla.ac.uk/320514/2/320514.pdf
Voutsinos, M. Y., West-Roberts, J. A., Sachdeva, R., Moreau, J. W. <http://eprints.gla.ac.uk/view/author/51704.html> and Banfield, J. F. (2024) Weathered granites and soils harbour microbes with lanthanide-dependent methylotrophic enzymes. BMC Biology <https://eprints.gla.ac.uk/view/journal_volume/BMC_Biology.html>, 22(1), 41. (doi:10.1186/s12915-024-01841-0 <https://doi.org/10.1186/s12915-024-01841-0>) (PMID:38369453) (PMCID:PMC10875860)
op_rights cc_by_4
op_doi https://doi.org/10.1186/s12915-024-01841-0
container_title BMC Biology
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