Abstract
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.
Highlights
The rate of desertification across our planet is accelerating as the result of human activity and climate change
Functional metagenomic reconstruction was carried out on two rock substrates, calcite and ignimbrite, and the context for the interpretation of the molecular data was provided by the examination of water availability, the mineralogical composition, and the type of colonization for the two types of rock
The Valle de la Luna and Lomas de Tilocalar sampling sites are located in the hyperarid zone of the Atacama Desert and, as such, both locations experience rare precipitations (DiRuggiero et al, 2013; Wierzchos et al, 2013)
Summary
The rate of desertification across our planet is accelerating as the result of human activity and climate change. The susceptibility of rocks to colonization depends on the architecture of the lithic substrate (Wierzchos et al, 2015), including factors such as translucence, which allows transmission of photosynthetically active radiation (PAR), thermal conductivity, the presence of a network of pores and/or fissures connected to the rock surface, which is linked to the capacity at retaining water, and chemical composition. These factors are likely to impact greatly microbial colonization and diversity (Walker and Pace, 2007; Herrera et al, 2009; Cockell et al, 2011; Wierzchos et al, 2012). The taxonomic and functional composition of the communities were characterized and interpreted within the context of the structural properties of each rock type
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