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.

Analysis of Rock Varnish from the Mojave Desert by Handheld Laser-Induced Breakdown Spectroscopy

“…The repetitive spikes in spectral intensity observed for all elements except Si and H along the depth profile in Figure 10 f–h are suggestive of a repetitive compositional variation through the varnish layer that could be interpreted to reflect multiple depositional cycles. The coherent behavior of Si and H suggests that silica plays an important and independent role in the development of rock varnish through the slow dissolution of silica in the presence of moisture from surficial material accumulations and then its subsequent gelling, condensation, and case hardening to form the indurated varnish layer [ 23 , 41 ] that incorporates the Mn-rich domains generated by cyanobacterial concentration [ 16 ].…”

“…Biological mediation by chemolithotrophic bacteria that precipitate Mn from a solution by oxidizing Mn 2+ and Mn 3+ to Mn 4+ may play a role in Mn fixation and concentration [ 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 ], but some have argued that Mn enrichment in rock varnish is largely an abiotic inorganic process involving leaching, mobilization and photochemical oxidation [ 8 , 12 , 14 , 15 , 35 ] and that silicic acid acts as a mechanism for elemental mobilization, complexation and cementation [ 41 ]. Recently, Lingappa et al [ 16 ] described a unifying ecophysical model for rock varnish formation. Their model explains rock varnish as an aerobic microbial ecosystem governed by sunlight, water and manganese redox cycling operating in the moist environment of microdepressions on rock surfaces where dust accumulates, and photosynthetic cyanobacteria sequester high concentrations of Mn in their cells and exploit the unique redox chemistry of manganese complexes as a catalytic antioxidant system.…”

“…Varying in color from shades of orange, mahogany, brown and black, rock varnish characteristically comprises a tens to hundreds of micrometers thick cyclic accretionary sequence of discontinuous dark and light micron-thick layers of variable morphology, mineralogy and chemistry [ 1 , 2 , 3 , 4 , 5 , 6 , 7 ]. Understanding the origin of rock varnish has recently become a subject of particular research interest [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 ] because of its potential as a paleoclimate proxy [ 17 , 18 , 19 , 20 ] and as a terrestrial analog to rock surface coatings on Mars [ 21 , 22 , 23 , 24 ]. Although a variety of microanalytical techniques have been used to examine rock varnish in the laboratory, in situ examination of rock varnish is challenging.…”

A Multi-Analytical Approach to Infer Mineral–Microbial Interactions Applied to Petroglyph Sites in the Negev Desert of Israel

“…Examination of the black varnish in the petrographic thin sections revealed a clear micron-size laminated pattern (Figure 7a) with a curved shape and oriented parallel to the surface. This micro texture is defined as a stromatolite structure and is typical of desert varnish [17,19,27]. Mappings of the elemental composition of the black crust revealed that Mn and Fe are not homogeneously distributed, but their content varies in the different layers of the coating.…”

“…Despite the fact that geochemical aspects of rock varnish have been thoroughly investigated [19][20][21][22][23][24] and it is believed that its primary source of material is airborne dust, there is an ongoing debate about the exact process of formation and specifically whether or not microorganisms are involved in this process [5,25,26]. In a recent study, Lingappa et al [27] proposed a new hypothesis for varnish formation. They state that Cyanobacteria accumulate manganese as a nonenzymatic antioxidant system and that, consequently to the cells death, the manganese-rich residue left behind is oxidized to generate the manganese oxides present in the varnish.…”