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.
| Original language | English (US) |
|---|---|
| Article number | e2025188118 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 118 |
| Issue number | 25 |
| DOIs | |
| State | Published - Jun 22 2021 |
Funding
ACKNOWLEDGMENTS. 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, Aps\u00E1alooke, 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.\u2019s interest in rock varnish research. ACKNOWLEDGMENTS. 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, Aps\u00E1alooke, 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, Nano-SIMS, 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.\u2019s interest in rock varnish research.
Keywords
- Rock varnish | desert varnish | Cyanobacteria manganese oxidative stress
ASJC Scopus subject areas
- General