Octavio Artieda

Adaptation strategies of endolithic chlorophototrophs to survive the hyperarid and extreme solar radiation environment of the Atacama Desert

The Atacama Desert, northern Chile, is one of the driest deserts on Earth and, as such, a natural laboratory to explore the limits of life and the strategies evolved by microorganisms to adapt to extreme environments. Here we report the exceptional adaptation strategies of chlorophototrophic and eukaryotic algae, and chlorophototrophic and prokaryotic cyanobacteria to the hyperarid and extremely high solar radiation conditions occurring in this desert. Our approach combined several microscopy techniques, spectroscopic analytical methods, and molecular analyses. We found that the major adaptation strategy was to avoid the extreme environmental conditions by colonizing cryptoendolithic, as well as, hypoendolithic habitats within gypsum deposits. The cryptoendolithic colonization occurred a few millimeters beneath the gypsum surface and showed a succession of organized horizons of algae and cyanobacteria, which has never been reported for endolithic microbial communities. The presence of cyanobacteria beneath the algal layer, in close contact with sepiolite inclusions, and their hypoendolithic colonization suggest that occasional liquid water might persist within these sub-microhabitats. We also identified the presence of abundant carotenoids in the upper cryptoendolithic algal habitat and scytonemin in the cyanobacteria hypoendolithic habitat. This study illustrates that successful lithobiontic microbial colonization at the limit for microbial life is the result of a combination of adaptive strategies to avoid excess solar irradiance and extreme evapotranspiration rates, taking advantage of the complex structural and mineralogical characteristics of gypsum deposits—conceptually called “rocks habitable architecture.” Additionally, self-protection by synthesis and accumulation of secondary metabolites likely produces a shielding effect that prevents photoinhibition and lethal photooxidative damage to the chlorophototrophs, representing another level of adaptation.

Ignimbrite textural properties as determinants of endolithic colonization patterns from hyper-arid Atacama Desert

This study explores the photosynthetic microbial colonization of rhyolitic ignimbrites in Lomas de Tilocalar, a hyper-arid region of the Atacama Desert, Chile. Colonization appeared in the form of a green layer a few millimeters beneath the ignimbrite surface. Some ignimbrite rocks revealed two distinct micromorphological areas of identical mineralogical and chemical composition but different textural properties. According to texture, colonization patterns varied in terms of the extension and depth of colonization. The diversity of photosynthetic microorganisms was assessed by denaturing gradient gel electrophoresis (DGGE) of the 23S rRNA gene and by generating clone libraries of the 16S rRNA gene. We observed a low diversity of photosynthetic microorganisms colonizing the ignimbrite microhabitat. Most rRNA gene sequences recovered greatly resembled those of Chroococcidiopsis hypolith clones from arid deserts. These results point to highly restrictive conditions of the hyper-arid Atacama Desert conditioning the diversity of cyanobacteria, and suggest that microbial colonization and composition patterns might be determined by the microscale physico-chemical properties of the ignimbrite rocks.

Phylogenetic and Functional Substrate Specificity for Endolithic Microbial Communities in Hyper-Arid Environments

Under extreme water deficit, endolithic (inside rock) microbial ecosystems are considered environmental refuges for life in cold and hot deserts, yet their diversity and functional adaptations remain vastly unexplored. The metagenomic analyses of the communities from two rock substrates, calcite and ignimbrite, revealed that they were dominated by Cyanobacteria, Actinobacteria, and Chloroflexi. The relative distribution of major phyla was significantly different between the two substrates and biodiversity estimates, from 16S rRNA gene sequences and from the metagenomic data, all pointed to a higher taxonomic diversity in the calcite community. While both endolithic communities showed adaptations to extreme aridity and to the rock habitat, their functional capabilities revealed significant differences. ABC transporters and pathways for osmoregulation were more diverse in the calcite chasmoendolithic community. In contrast, the ignimbrite cryptoendolithic community was enriched in pathways for secondary metabolites, such as non-ribosomal peptides (NRP) and polyketides (PK). Assemblies of the metagenome data produced population genomes for the major phyla found in both communities and revealed a greater diversity of Cyanobacteria population genomes for the calcite substrate. Draft genomes of the dominant Cyanobacteria in each community were constructed with more than 93% estimated completeness. The two annotated proteomes shared 64% amino acid identity and a significantly higher number of genes involved in iron update, and NRPS gene clusters, were found in the draft genomes from the ignimbrite. Both the community-wide and genome-specific differences may be related to higher water availability and the colonization of large fissures and cracks in the calcite in contrast to a harsh competition for colonization space and nutrient resources in the narrow pores of the ignimbrite. Together, these results indicated that the habitable architecture of both lithic substrates- chasmoendolithic versus cryptoendolithic – might be an essential element in determining the colonization and the diversity of the microbial communities in endolithic substrates at the dry limit for life.

Discovery of carotenoid red-shift in endolithic cyanobacteria from the Atacama Desert

The biochemical responses of rock-inhabiting cyanobacteria towards native environmental stresses were observed in vivo in one of the Earth’s most challenging extreme climatic environments. The cryptoendolithic cyanobacterial colonization, dominated by Chroococcidiopsis sp., was studied in an ignimbrite at a high altitude volcanic area in the Atacama Desert, Chile. Change in the carotenoid composition (red-shift) within a transect through the cyanobacteria dominant microbial community (average thickness ~1 mm) was unambiguously revealed in their natural endolithic microhabitat. The amount of red shifted carotenoid, observed for the first time in a natural microbial ecosystem, is depth dependent, and increased with increasing proximity to the rock surface, as proven by resonance Raman imaging and point resonance Raman profiling. It is attributed to a light-dependent change in carotenoid conjugation, associated with the light-adaptation strategy of cyanobacteria. A hypothesis is proposed for the possible role of an orange carotenoid protein (OCP) mediated non-photochemical quenching (NPQ) mechanism that influences the observed spectral behavior. Simultaneously, information about the distribution of scytonemin and phycobiliproteins was obtained. Scytonemin was detected in the uppermost cyanobacteria aggregates. A reverse signal intensity gradient of phycobiliproteins was registered, increasing with deeper positions as a response of the cyanobacterial light harvesting complex to low-light conditions.

Soils of the Temperate Humid Zone

This chapter presents a detailed and updated scientific view of the Soils of the Temperate Humid Zone, which comprises a wide territory located in the Northwest (Galicia) and the North of Spain (Asturias, Cantabria, and the Basque Country). These territories, representing altogether a surface of 53.000 km2 (with near 2,400 km of coastline bathed by the Atlantic Ocean in the west and the Cantabrian Sea in the North), show common climatic characteristics, with abundance of rainfall that limits the summer dryness. However, due to the different orography of the territory, variations in the climate are observed, which are mainly due to great differences in altitude (from the sea level to above 2,500 m a.s.l.) and to Mediterranean and continental climates influence eliminate locally in some areas. In this context of temperate humid climate, with contrasts in temperature and precipitation conditioned by relief and altitude, a remarkable diversity in the soil forming factors and land use, determines a wide variety of soil types according with the World Reference Base for Soil Resources (WRB 2006, updated 2007) classification system. Four wide Sections conform the chapter structure: Soil research history for the zone, extended from 1934 until nowadays; soil forming factors, climatology, lithology, geomorphology, and vegetation and main factors of soil degradation, mainly forest fires and its consequences, post-fire erosion, and soil losses; major soil types in the temperate humid zone, comprising the identification and description of the main Reference Soil Groups (RSGs) and second-level units of the WRB in the study zone (based on the morphological, physical and chemical characteristics of the soil types, and their geographical distribution); and main biochemical and biological characteristics of the soils of the zone. The description of 18 RSGs present in the study area is accompanied by 14 Tables with data from 140 soil profiles, including 56 benchmark profiles. All the Sections include related pictures.

Endolithic microbial habitats as refuges for life in polyextreme environment of the Atacama Desert

The extremely harsh conditions of hyperarid deserts are a true challenge for microbial life. Microorganisms thriving in such polyextreme environments are fascinating as they can tell us more about life, its strategies and its boundaries than other groups of organisms. The Atacama Desert (North Chile) holds two world records of extreme environmental characteristics: the lowest rainfall and greatest surface ultraviolet radiation and total solar irradiance ever measured on Earth. Despite these limiting conditions for life, we recently identified several remarkable examples of endolithic habitats colonized by phototrophic and heterotrophic microorganisms in the hyperarid core of the Atacama Desert.

Fine scale diversification of endolithic microbial communities in the hyper-arid Atacama Desert

The expansion of desertification across our planet is accelerating as the result of human activity and global climate change. In hyper-arid deserts, endolithic microbial communities colonize the rocks’ interior as a survival strategy. Yet, the composition of these communities and the drivers promoting their assembly are still poorly understood. Using a sampling strategy that minimized climate regime and biogeography effects, we analyzed the diversity and community composition of endoliths from four different lithic substrates – calcite, gypsum, ignimbrite and granite – collected in the hyper-arid zone of the Atacama Desert, Chile. By combining microscopy, mineralogy, and high throughput sequencing, we found these communities to be highly specific to their lithic substrate, although they were all dominated by the same four main phyla, Cyanobacteria, Actinobacteria, Chloroflexi and Proteobacteria. This finding indicates a fine scale diversification of the microbial reservoir driven by substrate properties. Our data suggest that the overall rock chemistry is not an essential driver of community structure and we propose that the architecture of the rock, i.e. the space available for colonization and its physical structure, linked to water retention capabilities, is ultimately the driver of community diversity and composition at the dry limit of life. Originality-Significance Statement In this study, we demonstrated that endolithic microbial communities are highly specific to their substrates, suggesting a fine scale diversification of the available microbial reservoir. By using an array of rock substrates from the same climatic region, we established, for the first time, that the architecture of the rock is linked to water retention and is ultimately the driver of community diversity and composition at the dry limit for life.