Life on the rocks

Biofilms are interface micro-habitats formed by microbes that differ markedly from those of the ambient environment. The term 'subaerial biofilm' (SAB) was coined for microbial communities that develop on solid mineral surfaces exposed to the atmosphere. Subaerial biofilms are ubiquitous, self-sufficient, miniature microbial ecosystems that are found on buildings, bare rocks in deserts, mountains, and at all latitudes where direct contact with the atmosphere and solar radiation occurs. Subaerial biofilms on exposed terrestrial surfaces are characterized by patchy growth that is dominated by associations of fungi, algae, cyanobacteria and heterotrophic bacteria. Inherent subaerial settlers include specialized actinobacteria (e.g. Geodermatophilus), cyanobacteria and microcolonial fungi. Individuals within SAB communities avoid sexual reproduction, but cooperate extensively with one another especially to avoid loss of energy and nutrients. Subaerial biofilm metabolic activity centres on retention of water, protecting the cells from fluctuating environmental conditions and solar radiation as well as prolonging their vegetative life. Atmospheric aerosols, gases and propagatory particles serve as sources of nutrients and inoculum for these open communities. Subaerial biofilms induce chemical and physical changes to rock materials, and they penetrate the mineral substrate contributing to rock and mineral decay, which manifests itself as bio-weathering of rock surfaces. Given their characteristic slow and sensitive growth, SAB may also serve as bioindicators of atmospheric and/or climate change.     

Modern and fossil traces in terrestrial lithic substrates

A number of biogenic processes leads to the formation of distinctive traces in terrestrial lithic substrates. These include: burrowing by vertebrates in moderately lithified rocks; scraping by mammals; smoothing and polishing of limestone surfaces by the locomotion of mammals; excavation by bees, wasps, and ants producing nesting and dwelling tunnels; dissolution of limestone surfaces by terrestrial snails; endolithic activity of fungi, algae, and lichens on subaerial rock surfaces; root corrosion; etc. Processes of biochemical weathering, biophysical erosion, and enlargement of cracks and fissures by the pressure of plant roots do not leave distinctive traces and therefore lie outside the ichnological realm. The fossil preservation of terrestrial bioerosional traces is expected to be uncommon. Nevertheless, various possible means of preservation must be considered, such as by rapid burial by volcanic material, by fluvial sediments, by travertine or tufa, by loess, “conservation”; in caves, case hardening of surfaces of porous rocks, and preservation of subsoil traces below fossil soils.     

The role of fungi in biogenic weathering in boreal forest soils

In this article we discuss the possible significance of biological processes, and of fungi in particular, in weathering of minerals. We consider biological activity to be a significant driver of mineral weathering in forest ecosystems. In these environments fungi play key roles in organic matter decomposition, uptake, transfer and cycling of organic and inorganic nutrients, biogenic mineral formation, as well as transformation and accumulation of metals. The ability of lichens, mutualistic symbioses between fungi and photobionts such as algae or cyanobacteria, to weather minerals is well documented. The role of mycorrhizal fungi forming symbioses with forest trees is less well understood, but the mineral horizons of boreal forests are intensively colonised by mycorrhizal mycelia which transfer protons and organic metabolites derived from plant photosynthates to mineral surfaces, resulting in mineral dissolution and mobilisation and redistribution of anionic nutrients and metal cations. The mycorrhizal mycelia, in turn provide efficient systems for the uptake and direct transport of mobilised essential nutrients to their host plants which are large sinks. Since almost all (99.99 %) non-suberised lateral plant roots involved in nutrient uptake are covered by ectomycorrhizal fungi, most of this exchange of metabolites must take place through the plant–fungus interface. This idea is still consistent with a linear relationship between soil mineral surface area and weathering rate since the mycelia that emanate from the tree roots will have a larger area of contact with minerals if the mineral surface area is higher. Although empirical models based on bulk soil solution chemistry may fit field data, we argue that biological processes make an important contribution to mineral weathering and that a more detailed mechanistic understanding of these must be developed in order to predict responses to environmental changes and anthropogenic impact.     

Diversity of Rock-Inhabiting Cyanobacterial Lichens: Studies on Granite Inselbergs along the Orinoco and in Guyana

Abstract: A survey was undertaken of specialized saxicolous cyanobacterial lichens growing on exposed granitic rock surfaces of inselbergs in Venezuela and additionally in Guyana and French Guyana. The study focused on taxonomy and species composition. Twenty-three cyanobacterial lichens were found, four of which are new to science: Peltula auriculata, Phylliscum vermiformis, Psorotichia polyspora and Pterygiopsis guyanensis. Besides the new species, almost all taxa are absent from the available lists of lichen-forming fungi from the Guyana region. Although free-living cyanobacteria are the dominant group in biological crusts covering the inselbergs, the number of cyanobacterial lichens is relatively high and their distribution is homogenous over long distances and macro-climatic gradients. As inselberg rock faces undergo relatively fast weathering under moist tropical climates, numerous micro-habitats are formed. Among these, xeric micro-habitats are favourable for colonization by cyanobacterial lichens, mainly of the Lichinaceae and Peltulaceae. It is concluded that granite inselbergs in the savannas of the Orinoco lowland and the Guyana region are local centres of diversity for saxicolous cyanobacterial lichens.     

Geomicrobiology of a Weathering Crust from an Impact Crater and a Hypothesis for its Formation

Understanding the role of microbe-mineral interactions in rock weathering is vital to an understanding of nutrient availability to the biosphere and, in so far as weathering influences carbon dioxide drawdown, climate control. We studied a weathering crust on a resurge tsunami deposit (Loftarstone) from the ～ 455 Ma old Lockne impact crater, central Sweden with an integrated approach using XRD, electron microprobe analysis, SEM-EDS and GCMS analysis of organics. The lichens and fungal hyphae network preferentially weather the chlorite in the Loftarstone compared to feldspars and quartz. We demonstrate, using a fungal isolate (identified by ITS sequencing), that biologically induced dissolution of the calcite component produces cavities which increase the surface area of interaction between the biota and the rock substrate. The weathering crust exfoliates from the rock surface in sheets, which we attribute to the dissolution of the calcite matrix. We present a hypothesis for the crust development. As well as providing insights into weathering on substrates derived from a diversity of high-energy geological disturbances, such as impact events and tsunamis, the weathering crust provides a model system to understand weathering processes in other common lithologies with mixed mineralogies at small spatial scales, including many sedimentary rocks. This work reveals how each different clast plays a unique part in the weathering process, leading to a well-defined weathering sequence.     

Solubilization of Magnesium-Bearing Silicate Minerals and the Subsequent Formation of Glushinskite by Aspergillus niger

Microbes may play a substantial role in the weathering and alteration of minerals. However, not enough concerns have been realized about the complexity of microbe-mineral interactions. The present work reports the interactions between fungi and minerals with emphasis on the role of silicate minerals as the metal donor for the precipitation of secondary mineral. Herein, two magnesium-bearing silicate minerals with different structures, forsterite and talc, were added to the submerged cultures of Aspergillus niger (A. niger). It is shown that forsterite exhibits a better solubilization effect than talc, and the secondary mineral glushinskite only precipitates in the presence of forsterite substrates. Oxalic acid excreted by A. niger plays a key role in the biological leaching and mineralization processes. Moreover, the forsterite particles with certain size added to the cultures tend to inhibit the aggregation of fungal biomass, and therefore affect the morphology of A. niger aggregates in the submerged culture. With varying forsterite particle size, distinct fungal morphological forms including mycelial pellets and freely dispersed hyphae can be formed, which have a direct impact on fungal metabolism and ultimately result in varied crystallization habits of the neo-minerals. Particularly in the culture with ?40/+60 mesh forsterite particles, the mineralized glushinskite mainly exhibit tubular forms; whereas when forsterite particles were at ?100/+120 mesh or ?200 mesh, pyramidal prisms are obtained. We show that the environmental factors such as the particle size of mineral substrate could influence the fungal morphology and metabolic activities, thereby leading to different morphological neo-minerals. The dependence of biomineral morphology on the environmental factors can open up a novel avenue to understanding the microorganism-environment interactions.     

The absorption and fluorescence spectra of the cyanobacterial phycobilins of cryptoendolithic lichens in the high-polar region of Antarctica

The algologically pure cultures of the green-brown cyanobacterium Chroococcidiopsis sp. and three cyanobacteria of the genus Gloeocapsa, the blue-green Gloeocapsa sp.1, the brown Gloeocapsa sp.2, and the red-orange Gloeocapsa sp.3, were isolated from sandstones and rock fissures in the high-polar regions of Antarctica. These cyanobacteria are the most widespread phycobionts of cryptoendolithic lichens in these regions. The comparative analysis of the absorption and the second-derivative absorption spectra of the cyanobacteria revealed considerable differences in the content of chlorophyll a and in the content and composition of carotenoids and phycobiliproteins. In addition to phycocyanin, allophycocyanin, and allophycocyanin B, which were present in all of the cyanobacteria studied, Gloeocapsa sp.2 also contained phycoerythrocyanin and Gloeocapsa sp.3 phycoerythrocyanin and C-phycoerythrin (the latter pigment is typical of nitrogen-fixing cyanobacteria). The fluorescence spectra of Gloeocapsa sp.2 and Gloeocapsa sp.3 considerably differed from the fluorescence spectra of the other cyanobacteria as well. The data obtained suggest that various zones of the lichens may be dominated either by photoheterotrophic or photoautotrophic cyanobacterial phycobionts, which differ in the content and composition of photosynthetic pigments.     

Water relations and photosynthesis in the cryptoendolithic microbial habitat of hot and cold deserts

Two cryptoendolithic microbial communities, lichens in the Ross Desert of Antarctica and cyanobacteria in the Negev Desert, inhabit porous sandstone rocks of similar physical structure. Both rock types adsorb water vapor by physical mechanisms unrelated to biological processes. Yet the two microbial communities respond differently to water stress: cryp-toendolithic lichens begin to photosynthesize at a matric water potential of –46.4 megaPascals (MPa) [70% relative humidity (RH) at 8°C], resembling thallose desert lichens. Cryptoendolithic cyanobacteria, like other prokaryotes, photosynthesize only at very high matric water potentials [> –6.9 MPa, 90% RH at 20°C].     

Diversity of endolithic fungal communities in dolomite and limestone rocks from Nanjiang Canyon in Guizhou karst area, China

The endolithic environment, the tiny pores and cracks in rocks, buffer microbial communities from a number of physical stresses, such as desiccation, rapid temperature variations, and UV radiation. Considerable knowledge has been acquired about the diversity of microorganisms in these ecosystems, but few culture-independent studies have been carried out on the diversity of fungi to date. Scanning electron microscopy of carbonate rock fragments has revealed that the rock samples contain certain kinds of filamentous fungi. We evaluated endolithic fungal communities from bare dolomite and limestone rocks collected from Nanjiang Canyon (a typical karst canyon in China) using culture-independent methods. Results showed that Ascomycota was absolutely dominant both in the dolomite and limestone fungal clone libraries. Basidiomycota and other eukaryotic groups (Bryophyta and Chlorophyta) were only detected occasionally or at low frequencies. The most common genus in the investigated carbonate rocks was Verrucaria. Some other lichen-forming fungi (e.g., Caloplaca, Exophiala, and Botryolepraria), Aspergillus, and Penicillium were also identified from the rock samples. The results provide a cross-section of the endolithic fungal communities in carbonate rocks and help us understand more about the role of microbes (fungi and other rock-inhabiting microorganisms) in rock weathering and pedogenesis.     

Subaerial biofilms on granitic historic buildings: microbial diversity and development of phototrophic multi-species cultures

Microbial communities of natural subaerial biofilms developed on granitic historic buildings of a World Heritage Site (Santiago de Compostela, NW Spain) were characterized and cultured in liquid BG11 medium. Environmental barcoding through next-generation sequencing (Pacific Biosciences) revealed that the biofilms were mainly composed of species of Chlorophyta (green algae) and Ascomycota (fungi) commonly associated with rock substrata. Richness and diversity were higher for the fungal than for the algal assemblages and fungi showed higher heterogeneity among samples. Cultures derived from natural biofilms showed the establishment of stable microbial communities mainly composed of Chlorophyta and Cyanobacteria. Although most taxa found in these cultures were not common in the original biofilms, they are likely common pioneer colonizers of building stone surfaces, including granite. Stable phototrophic multi-species cultures of known microbial diversity were thus obtained and their reliability to emulate natural colonization on granite should be confirmed in further experiments.     

贵阳地区碳酸盐岩表生地衣调查初报

对贵阳地区碳酸盐岩表生地衣资源进行初步调查,鉴定出4科,4属,共计7个种。其中两个是中国新记录种,即:蓝藻橙衣和石灰瓶口衣。瓶口衣属、黄烛衣属、凹盘衣属以及该文所描述的7个种都是贵州首次报道。对壳状地衣体在碳酸盐岩风化过程中的作用进行了初步分析。     

Mineralogical transformation and neoformation in granite caused by the lichens Tephromela atra and Ochrolechia parella

Tephromela atra and Ochrolechia parella are among the most abundant lichens colonizing granitic monuments in the region of Galicia (northwest Spain). In this work, their interaction with a two-mica granite used in the construction of the Toxosoutos Monastery (Noia, Galicia) was studied, using optical microscopy, scanning electron microscopy (with back-scattered-electron and energy-dispersive X-ray detection), X-ray diffractometry and atomic absorption spectroscopy to evaluate their physical, mineralogical and chemical effects. Both lichens contributed to physical weathering by penetrating intermineral voids and mineral cleavage planes, disaggregating the rock and entrapping the loosened mineral grains in their thalli. Significant chemical and mineralogical weathering also occurred, including depletion of potassium from biotite, transformation of this mica into hydroxyaluminium-vermiculite, and neoformation of whewellite and calcite in the lichen thalli. Neoformation of these calcium minerals on a calcium-poor rock such as granite is noteworthy, and this is the first time calcium carbonate has been detected within a lichen colonizing a granitic rock. Precipitation of the calcium carbonate was attributed to the local pH in the thalli having been raised due to release of sodium from nearby plagioclase during weathering.     

The effect of rock composition on cyanobacterial weathering of crystalline basalt and rhyolite

The weathering of volcanic rocks contributes significantly to the global silicate weathering budget, effecting carbon dioxide drawdown and long‐term climate control. The rate of chemical weathering is influenced by the composition of the rock. Rock‐dwelling micro‐organisms are known to play a role in changing the rate of weathering reactions; however, the influence of rock composition on bio‐weathering is unknown. Cyanobacteria are known to be a ubiquitous surface taxon in volcanic rocks. In this study, we used a selection of fast and slow growing cyanobacterial species to compare microbial‐mediated weathering of bulk crystalline rocks of basaltic and rhyolitic composition, under batch conditions. Cyanobacterial growth caused an increase in the pH of the medium and an acceleration of rock dissolution compared to the abiotic controls. For example, Anabaena cylindrica increased the linear release rate () of Ca, Mg, Si and K from the basalt by more than fivefold (5.21–12.48) and increased the pH of the medium by 1.9 units. Although A. cylindrica enhanced rhyolite weathering, the increase in was less than threefold (2.04–2.97) and the pH increase was only 0.83 units. The values obtained with A. cylindrica were at least ninefold greater with the basalt than the rhyolite, whereas in the abiotic controls, the difference was less than fivefold. Factors accounting for the slower rate of rhyolite weathering and lower biomass achieved are likely to include the higher content of quartz, which has a low rate of weathering and lower concentrations of bio‐essential elements, such as, Ca, Fe and Mg, which are known to be important in controlling cyanobacterial growth. We show that at conditions where weathering is favoured, biota can enhance the difference between low and high Si‐rock weathering. Our data show that cyanobacteria can play a significant role in enhancing rock weathering and likely have done since they evolved on the early Earth.     

Nitrogen fixation in lichens is important for improved rock weathering

It is known that cyanobacteria in cyanolichens fix nitrogen for their nutrition. However, specific uses of the fixed nitrogen have not been examined. The present study shows experimentally that a mutualistic interaction between a heterotrophic N₂ fixer and lichen fungi in the presence of a carbon source can contribute to enhanced release of organic acids, leading to improved solubilization of the mineral substrate. Three lichen fungi were isolated fromXanthoparmelia mexicana, a foliose lichen, and they were cultured separately or with a heterotrophic N₂ fixer in nutrient broth media in the presence of a mineral substrate. Cells of the N₂-fixing bacteria attached to the mycelial mats of all fungi, forming biofilms. All biofilms showed higher solubilizations of the substrate than cultures of their fungi alone. This finding has bearing on the significance of the origin and existence of N₂-fixing activity in the evolution of lichen symbiosis. Further, our results may explain why there are N₂-fixing photobionts even in the presence of non-fixing photobionts (green algae) in some remarkable lichens such asPlacopsis gelida. Our study sheds doubt on the idea that the establishment of terrestrial eukaryotes was possible only through the association between a fungus and a phototroph.     

Oxidoreductases and cellulases in lichens: Possible roles in lichen biology and soil organic matter turnover

Lichens are symbiotic associations of a fungus (usually an Ascomycete) with green algae and/or a cyanobacterium. They dominate on 8 % of the world's land surface, mainly in Arctic and Antarctic regions, tundra, high mountain elevations and as components of dryland crusts. In many ecosystems, lichens are the pioneers on the bare rock or soil following disturbance, presumably because of their tolerance to desiccation and high temperature. Lichens have long been recognized as agents of mineral weathering and fine-earth stabilization. Being dominant biomass producers in extreme environments they contribute to primary accumulation of soil organic matter. However, biochemical role of lichens in soil processes is unknown. Our recent research has demonstrated that Peltigeralean lichens contain redox enzymes which in free-living fungi participate in lignocellulose degradation and humification. Thus lichen enzymes may catalyse formation and degradation of soil organic matter, particularly in high-stress communities dominated by lower plants. In the present review we synthesize recently published data on lichen phenol oxidases, peroxidases, and cellulases and discuss their possible roles in lichen physiology and soil organic matter transformations.     

A Three-Scale Analysis of Bacterial Communities Involved in Rocks Colonization and Soil Formation in High Mountain Environments

Alpha and beta diversities of the bacterial communities growing on rock surfaces, proto-soils, riparian sediments, lichen thalli, and water springs biofilms in a glacier foreland were studied. We used three molecular based techniques to allow a deeper investigation at different taxonomic resolutions: denaturing gradient gel electrophoresis, length heterogeneity-PCR, and automated ribosomal intergenic spacer analysis. Bacterial communities were mainly composed of Acidobacteria, Proteobacteria, and Cyanobacteria with distinct variations among sites. Proteobacteria were more represented in sediments, biofilms, and lichens; Acidobacteria were mostly found in proto-soils; and Cyanobacteria on rocks. Firmicutes and Bacteroidetes were mainly found in biofilms. UniFrac P values confirmed a significant difference among different matrices. Significant differences (P < 0.001) in beta diversity were observed among the different matrices at the genus–species level, except for lichens and rocks which shared a more similar community structure, while at deep taxonomic resolution two distinct bacterial communities between lichens and rocks were found.     

Organic acids,siderophores, enzymes and mechanical pressure for black slate bioweathering with the basidiomycete Schizophyllum commune

Although many fungi are known to be able to perform bioweathering of rocks and minerals, little information is available concerning the role of basidiomycetes in this process. The wood-rotting basidiomycete Schizophyllum commune was investigated for its ability to degrade black slate, a rock rich in organic carbon. Mechanical pressure of hyphae and extracellular polymeric substances was investigated for biophysical weathering. A mixed ß1-3/ß1-6 glucan, likely schizophyllan that is well known from S. commune, could be identified on black slate surfaces. Secretion of siderophores and organic acids as biochemical weathering agents was shown. Both may contribute to biochemical weathering in addition to enzymatic functions. Previously, the exoenzyme laccase was believed to attack organic the matter within the black slate, thereby releasing metals from the rock. Here, overexpression of laccase showed enhanced dissolution of quartz phases by etching and pitting. At the same time, the formation of a new secondary mineral phase, whewellite, could be demonstrated. Hence, a more comprehensive understanding of biophysical as well as biochemical weathering by S. commune could be reached and unexpected mechanisms like quartz dissolution linked to shale degradation.     

Spatial structure, rock type, and local environmental conditions drive moss and lichen distribution on calcareous boulders

Although mosses and lichens are a relevant component of the biota of rock habitats targeted for biodiversity conservation in Europe, the ecological factors driving their distribution are still poorly known. In this work, we examined the epilithic moss and lichen assemblages colonizing boulders of different types of calcareous rocks co-occurring in the same area in the Italian Alps. The goals were: (1) to evaluate if and to what extent different calcareous rocks host different assemblages; (2) to identify species associated to each rock type; (3) to quantify the relative importance of rock type, local environmental factors, and habitat spatial structure in explaining species distribution. Our results demonstrated that different calcareous rocks host different moss and lichen assemblages with some typical species, indicating that each rock type contributes to the total diversity of both mosses and lichens. Local environmental conditions influenced mosses and not lichens whose distribution is mainly associated to rock type. The patterns of both organism groups were also significantly related to habitat spatial structure, species assemblages tending to have a patchy distribution, which may reflect dispersal dynamics. Our results have implications for conservation: (1) each rock type may play a relevant role in maintaining the overall diversity contributing with unique assemblages and typical species; (2) the patchy distribution of both moss and lichen assemblages should warn from considering rock patches as a monotonous repetition of the same habitat across space.     

Reshaping of sandstone surfaces by cryptoendolithic cyanobacteria: bioalkalization causes chemical weathering in arid landscapes

We report a novel weathering mechanism in South African sandstone formations, where cryptoendolithic cyanobacteria induce weathering by substrate alkalization during photosynthesis. As a result, the upper rock part is loosened and then eroded away by physical forces such as wind, water, trampling. This special type of ‘exfoliation’ is widely distributed and affects the geomorphology of whole sandstone mountain ranges and outcrops across several biomes. We show, that this weathering type is initiated by bioalkalization because of the photosynthesis of cryptoendolithic (i.e. those organisms living in small tight open spaces between the sand grains) cyanobacteria causing pH values high enough to enhance silica solution in the cryptoendolithic zone. As modern cyanobacteria are the initial photoautotrophic colonizers of bare rocks in arid and semiarid landscapes, it is possible that they may also have played a significant role in shaping sandstone landscapes in the geological past.     

Approaches to modelling mineral weathering by fungi

Fungi are agents of geochemical change in the environment and play important roles in the soil, the plant-root zone, and in rock and mineral habitats. Modelling may serve as a tool to quantify fungal weathering under natural conditions. This paper provides a review of existing mycelial growth models and examines how these can be adapted to describe weathering by ectomycorrhizal and other fungi in mineral soil.