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An ecophysiological explanation for manganese enrichment in rock varnish

Lingappa, Usha F. and Yeager, Chris M. and Sharma, Ajay and Lanza, Nina L. and Morales, Demosthenes P. and Xie, Gary and Atencio, Ashley D. and Chadwick, Grayson L. and Monteverde, Danielle R. and Magyar, John S. and Webb, Samuel M. and Valentine, Joan Selverstone and Hoffman, Brian M. and Fischer, Woodward W. (2021) An ecophysiological explanation for manganese enrichment in rock varnish. Proceedings of the National Academy of Sciences, 118 (25). Art. No. e2025188118. ISSN 0027-8424. PMCID PMC8237629. doi:10.1073/pnas.2025188118. https://resolver.caltech.edu/CaltechAUTHORS:20210622-144020892

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Abstract

Desert varnish is a dark rock coating that forms in arid environments worldwide. It is highly and selectively enriched in manganese, the mechanism for which has been a long-standing geological mystery. We collected varnish samples from diverse sites across the western United States, examined them in petrographic thin section using microscale chemical imaging techniques, and investigated the associated microbial communities using 16S amplicon and shotgun metagenomic DNA sequencing. Our analyses described a material governed by sunlight, water, and manganese redox cycling that hosts an unusually aerobic microbial ecosystem characterized by a remarkable abundance of photosynthetic Cyanobacteria in the genus Chroococcidiopsis as the major autotrophic constituent. We then showed that diverse Cyanobacteria, including the relevant Chroococcidiopsis taxon, accumulate extraordinary amounts of intracellular manganese—over two orders of magnitude higher manganese content than other cells. The speciation of this manganese determined by advanced paramagnetic resonance techniques suggested that the Cyanobacteria use it as a catalytic antioxidant—a valuable adaptation for coping with the substantial oxidative stress present in this environment. Taken together, these results indicated that the manganese enrichment in varnish is related to its specific uptake and use by likely founding members of varnish microbial communities.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2025188118DOIArticle
https://www.pnas.org/content/suppl/2021/06/09/2025188118.DCSupplementalPublisherSupporting Information
https://dx.doi.org/10.22002/D1.1960DOIData
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8237629PubMed CentralArticle
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA630476Related ItemData
ORCID:
AuthorORCID
Lingappa, Usha F.0000-0001-5691-6788
Yeager, Chris M.0000-0001-9662-5811
Sharma, Ajay0000-0002-0829-6753
Lanza, Nina L.0000-0003-4445-7996
Morales, Demosthenes P.0000-0002-4521-3478
Chadwick, Grayson L.0000-0003-0700-9350
Monteverde, Danielle R.0000-0002-0198-8220
Magyar, John S.0000-0002-3586-8286
Webb, Samuel M.0000-0003-1188-0464
Valentine, Joan Selverstone0000-0002-7174-925X
Hoffman, Brian M.0000-0002-3100-0746
Fischer, Woodward W.0000-0002-8836-3054
Additional Information:© 2021 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Contributed by Joan Selverstone Valentine, May 3, 2021 (sent for review December 7, 2020; reviewed by Valeria Cizewski Culotta and Kenneth H. Nealson). This research was supported by NSF Grant IOS-1833247 (U.F.L. and W.W.F.), NSF Graduate Research Fellowship Program (U.F.L.), NIH Grant GM111097 (B.M.H.), National Aeronautics and Space Administration Exobiology Grant 18-EXO18-0040 (W.W.F. and N.L.L.), and Los Alamos National Laboratory Laboratory-Directed Research and Development Project 20170414ER (C.M.Y. and N.L.L.). Use of the Stanford Synchrotron Radiation Lightsource (SSRL), SLAC National Accelerator Laboratory, was supported by the Department of Energy (DOE) Office of Basic Energy Sciences under Contract DE-AC02-76SF00515 and the SSRL Structural Molecular Biology Program supported by the DOE Office of Biological and Environmental Research and the NIH/National Institute of General Medical Sciences (Grant P41GM103393). This project benefited from the use of instrumentation made available by the Caltech Environmental Analysis Center, Caltech Microanalysis Center, and Caltech Geological and Planetary Sciences Division Analytical Facility. Fieldwork for this project was conducted on ancestral lands of the Hopi, Pueblo, Ute, Apsáalooke, and Serrano peoples. We thank George Rossman, Hope Johnson, Jared Leadbetter, and Yonaton Goldsmith for helpful discussions and insight; Chi Ma, Yunbin Guan, and Nathan Dalleska for help with SEM, NanoSIMS, and ICP-MS analyses; Nick Edwards and Sharon Bone for support at SSRL; Babbitt Ranches for allowing us to sample; Shoichiro Suda for supplying the Ryu 1-3 strain; and Jason Tor and the environmental microbiology class at Hampshire College for sparking U.F.L.’s interest in rock varnish research. Data Availability: Sequence data have been deposited as FASTQ files on the Sequence Read Archive (SRA) (BioProject ID PRJNA630476) (98). Binned genomes from samples 24 and 41 are available at CaltechDATA, https://dx.doi.org/10.22002/D1.1960 (99). Author contributions: U.F.L., C.M.Y., N.L.L., J.S.V., and W.W.F. designed research; U.F.L., C.M.Y., A.S., N.L.L., D.P.M., A.D.A., D.R.M., J.S.M., S.M.W., B.M.H., and W.W.F. performed research; U.F.L., C.M.Y., A.S., G.X., G.L.C., and B.M.H. analyzed data; and U.F.L., J.S.V., and W.W.F. wrote the paper. Reviewers: V.C.C., Johns Hopkins University; and K.H.N., University of Southern California. The authors declare no competing interest. See online for related content such as Commentaries. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2025188118/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NSFIOS-1833247
NSF Graduate Research FellowshipUNSPECIFIED
NIHGM111097
NASA18-EXO18-0040
Los Alamos National Laboratory20170414ER
Department of Energy (DOE)DE-AC02-76SF00515
NIHP41GM103393
Subject Keywords:rock varnish; desert varnish; Cyanobacteria; manganese ; oxidative stress
Issue or Number:25
PubMed Central ID:PMC8237629
DOI:10.1073/pnas.2025188118
Record Number:CaltechAUTHORS:20210622-144020892
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210622-144020892
Official Citation:An ecophysiological explanation for manganese enrichment in rock varnish. Usha F. Lingappa, Chris M. Yeager, Ajay Sharma, Nina L. Lanza, Demosthenes P. Morales, Gary Xie, Ashley D. Atencio, Grayson L. Chadwick, Danielle R. Monteverde, John S. Magyar, Samuel M. Webb, Joan Selverstone Valentine, Brian M. Hoffman, Woodward W. Fischer. Proceedings of the National Academy of Sciences Jun 2021, 118 (25) e2025188118; DOI: 10.1073/pnas.2025188118
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109523
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Jun 2021 19:15
Last Modified:27 Aug 2021 16:19

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