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An ecophysiological explanation for manganese enrichment in rock varnish.

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.

SUBMITTER: Lingappa UF

PROVIDER: S-EPMC8237629 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:We investigated rock varnish, a thin, manganese- and iron-rich, dark surface crust, on basaltic lava flows and petroglyphs in the Owens and Rose Valleys (California) by portable X-ray fluorescence (pXRF) and femtosecond laser-ablation inductively-coupled-plasma mass spectrometry (fs-LA-ICPMS). The major element composition of the varnish was consistent with a mixture of Mn-Fe oxyhydroxides and clay minerals. As expected, it contained elevated concentrations of elements that are typically enriched in rock varnish, e.g., Mn, Pb, Ba, Ce, and Co, but also showed unusually high enrichments in U, Cu, and Th. The rare earth and yttrium (REY) enrichment pattern revealed a very strong positive cerium (Ce) anomaly and distinct negative europium (Eu) and Y anomalies. The light rare earth elements (REE) were much more strongly enriched than the heavy REY. These enrichment patterns are consistent with a formation mechanism by leaching of Mn and trace elements from aeolian dust, reprecipitation of Mn and Fe as oxyhydroxides, and scavenging of trace elements by these oxyhydroxides. We inferred accumulation rates of Mn and Fe in the varnish from their areal densities measured by pXRF and the known ages of some of the lava flow surfaces. The areal densities of Mn and Fe, as well as their accumulation rates, were comparable to our previous results from the desert of Saudi Arabia. There was a moderate dependence of the Mn areal density on the inclination of the rock surfaces, but no relationship to its cardinal orientation. We attempted to use the degree of varnish regrowth on the rock art surfaces as an estimate of their age. While an absolute dating of the petroglyphs was not possible because of the lack of suitable calibration surfaces and a considerable amount of variability, the measured degree of varnish regrowth on the various petroglyphs was consistent with chronologies based on archeological and other archaeometric techniques. In particular, our results suggest that rock art creation in the study area continued over an extended period of time, possibly starting around the Pleistocene/Holocene transition and extending into the last few centuries.

Project description:Rock varnish is a thin coating enriched with manganese (Mn) and iron (Fe) oxides. The mineral composition and formation of rock varnish elicit considerable attention from geologists and microbiologists. However, limited research has been devoted to the semiconducting properties of these Fe/Mn oxides in varnish and relatively little attention is paid to the mineral-microbe interaction under sunlight. In this study, the mineral composition and the bacterial communities on varnish from the Gobi Desert in Xinjiang, China were analyzed. Results of principal components analysis and t-test indicated that more electroactive genera such as Acinetobacter, Staphylococcus, Dietzia, and Pseudomonas gathered on varnish bacterial communities than on substrate rock and surrounding soils. We then explored the culture of varnish, substrate and soil samples in media and the extracellular electron transfer (EET) between bacterial communities and mineral electrodes under light/dark conditions for the first time. Orthogonal electrochemical experiments demonstrated that the most remarkable photocurrent density of 6.1 ± 0.4 μA/cm2 was observed between varnish electrode and varnish microflora. Finally, based on Raman and 16S rRNA gene-sequencing results, coculture system of birnessite and Pseudomonas (the major Mn oxide and a common electroactive bacterium in varnish) was established to study underlying mechanism. A steadily growing photocurrent (205 μA at 100 h) under light was observed with a stable birnessite after 110 h. However, only 47 μA was generated in the dark control and birnessite was reduced to Mn2+ in 13 h, suggesting that birnessite helped deliver electrons instead of serving as an electron acceptor under light. Our study demonstrated that electroactive bacterial communities were positively correlated with Fe/Mn semiconducting minerals in varnish, and diversified EET process occurred on varnish under sunlight. Overall, these phenomena may influence bacterial-community structure in natural environments over time.

Project description:Manganese-oxidizing bacteria in the aquatic environment have been comprehensively investigated. However, little information is available about the distribution and biogeochemical significance of these bacteria in terrestrial soil environments. In this study, stratified soils were initially examined to investigate the community structure and diversity of manganese-oxidizing bacteria. Total 344 culturable bacterial isolates from all substrata exhibited Mn(II)-oxidizing activities at the range of 1 µM to 240 µM of the equivalent MnO2. The high Mn(II)-oxidizing isolates (>50 mM MnO2) were identified as the species of phyla Actinobacteria, Firmicutes and Proteobacteria. Seven novel Mn(II)-oxidizing bacterial genera (species), namely, Escherichia, Agromyces, Cellulomonas, Cupriavidus, Microbacterium, Ralstonia, and Variovorax, were revealed via comparative phylogenetic analysis. Moreover, an increase in the diversity of soil bacterial community was observed after the combined enrichment of Mn(II) and carbon-rich complex. The phylogenetic classification of the enriched bacteria represented by predominant denaturing gradient gel electrophoresis bands, was apparently similar to culturable Mn(II)-oxidizing bacteria. The experiments were further undertaken to investigate the properties of the Mn oxide aggregates formed by the bacterial isolates with high Mn(II)-oxidizing activity. Results showed that these bacteria were closely encrusted with their Mn oxides and formed regular microspherical aggregates under prolonged Mn(II) and carbon-rich medium enrichment for three weeks. The biotic oxidation of Mn(II) to Mn(III/IV) by these isolates was confirmed by kinetic examinations. X-ray diffraction assays showed the characteristic peaks of several Mn oxides and rhodochrosite from these aggregates. Leucoberbelin blue tests also verified the Mn(II)-oxidizing activity of these aggregates. These results demonstrated that Mn oxides were formed at certain amounts under the enrichment conditions, along with the formation of rhodochrosite in such aggregates. Therefore, this study provides insights into the structure and diversity of soil-borne bacterial communities in Mn(II)-oxidizing habitats and supports the contribution of soil-borne Mn(II)-oxidizing bacteria to Mn oxide mineralization in soils.

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An ecophysiological explanation for manganese enrichment in rock varnish.

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