Phylogenetic and functional substrate specificity for endolithic microbial communities in hyper-arid environments

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 genomespecific 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 substrateschasmoendolithic 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.

Diversity and mineral substrate preference in endolithic microbial communities from marine intertidal outcrops (Isla de Mona, Puerto Rico)

“…3) but so far we cannot ascertain a factor that would drive the observed separation beyond the fact that it is not substrate type. While it would be of interest to compare our communities to other endolithic communities, such as those studied by Chacón et al (2006), Crits-Christoph et al (2016), Horath and Bachofen (2009) and De la Torre et al (2003), this is not technically possible given that all of those studies used alternative methods for commu-nity analyses (Clone libraries, DGGE, metagenomes) that do not allow direct comparisons.…”

Response of endolithic Chroococcidiopsis strains from the polyextreme Atacama Desert to light radiation

“…This work provides a new insight into the behavior of cyanobacteria in endolithic communities under extreme solar radiation, as happens in the hyper-arid core of the Atacama Desert. Despite the sole development of lithobiontic microbial communities in endolithic habitats in different lithic substrates in this desert (39,(55)(56)(57) which act as a first line of defense against the damage provoked by high light exposure, the presence of second and third lines of cyanobacterial defense (39,40,42) points to the existence of specific, not previously characterized, adaptations to the harmful effects of high PAR and UVR, too.…”

Lithic cyanobacterial communities in the polyextreme Sahara Desert: implications for the search for the limits of life

“…Although Chroococcidiopsis is the dominant cyanobacterium in endolithic habitats in hot deserts, such as the Atacama (Dong et al, 2007;Crits-Christoph et al, 2016;Meslier et al, 2018;Ertekin et al, 2020;Qu et al, 2020;Casero et al, 2021), Negev (Israel) and Namib (southern Africa) Deserts (Qu et al, 2020), other coccoid taxa have also been found in endolithic assemblages from the Atacama Desert, such as Gloeocapsa (Crits-Christoph et al, 2016;Ertekin et al, 2020.;Casero et al, 2021) and Halothece (Ertekin et al, 2020). Recent culture-dependent and culture-independent studies, also in the Atacama Desert, have shown the occurrence of Synechococcus, Gloeocapsopsis (Casero et al, 2021), Aliterella, and Pleurocapsa minor (Jung et al, 2019).…”