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. 2023 Nov 20;11(11):2819.
doi: 10.3390/microorganisms11112819.

Diversity, Taxonomic Novelty, and Encoded Functions of Salar de Ascotán Microbiota, as Revealed by Metagenome-Assembled Genomes

Marcelo Veloso  1 , Angie Waldisperg  1 , Patricio Arros  1 , Camilo Berríos-Pastén  1 , Joaquín Acosta  1 , Hazajem Colque  1 , Macarena A Varas  1   2 , Miguel L Allende  2 , Luis H Orellana  3 , Andrés E Marcoleta  1
Affiliations

Diversity, Taxonomic Novelty, and Encoded Functions of Salar de Ascotán Microbiota, as Revealed by Metagenome-Assembled Genomes

Marcelo Veloso et al. Microorganisms. .

Abstract

Salar de Ascotán is a high-altitude arsenic-rich salt flat exposed to high ultraviolet radiation in the Atacama Desert, Chile. It hosts unique endemic flora and fauna and is an essential habitat for migratory birds, making it an important site for conservation and protection. However, there is limited information on the resident microbiota's diversity, genomic features, metabolic potential, and molecular mechanisms that enable it to thrive in this extreme environment. We used long- and short-read metagenomics to investigate the microbial communities in Ascotán's water, sediment, and soil. Bacteria predominated, mainly Pseudomonadota, Acidobacteriota, and Bacteroidota, with a remarkable diversity of archaea in the soil. Following hybrid assembly, we recovered high-quality bacterial (101) and archaeal (6) metagenome-assembled genomes (MAGs), including representatives of two putative novel families of Patescibacteria and Pseudomonadota and two novel orders from the archaeal classes Halobacteriota and Thermoplasmata. We found different metabolic capabilities across distinct lineages and a widespread presence of genes related to stress response, DNA repair, and resistance to arsenic and other metals. These results highlight the remarkable diversity and taxonomic novelty of the Salar de Ascotán microbiota and its rich functional repertoire, making it able to resist different harsh conditions. The highly complete MAGs described here could serve future studies and bioprospection efforts focused on salt flat extremophiles, and contribute to enriching databases with microbial genome data from underrepresented regions of our planet.

Keywords: extremophiles; hybrid metagenomic assembly; novel archaea; resistance; salt flat.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Microbial diversity in Salar de Ascotán soil, sediment, and water, as revealed by 16S rRNA metabarcoding and shotgun sequencing. Relative abundance of bacterial phyla (A) and genera (B) determined using the 16S rRNA Bakt_341F and Bakt_805R primers (V3–V4 region). Only the 30 most abundant genera in each sample were included for simplicity. The percentage of the total reads classified under these 30 genera corresponds to 81% in the case of soil, 58% in sediment, and 93% in water. * Genera present in two samples (mainly sediment and water). (C): Relative abundance of archaeal genera present in Ascotán’s soil, as determined using the Arc_787F and Arc_1059R primers (V5-V6 region). (D): Total (alpha) diversity according to the Shannon and Simpson indexes (calculated from the 16S rRNA gene metabarcoding data), and the Nonpareil Nd index from the analysis of shotgun metagenomic reads. (E): Nonpareil estimation of the metagenome coverage reached with the sequencing effort made for each sample. The circles correspond to the sequencing effort and the coverage reached for each sample, while the curves correspond to the fit according to the Nonpareil model. (F): Distance tree inferred from the MASH sequence composition analysis.
Figure 2
Figure 2
Phylogenetic relationships between the bacterial MAGs recovered from Salar de Ascotán’s soil, sediment, and water. The distance tree was inferred from the multiple sequence alignment of 120 bacterial marker proteins, as defined by the Genome Taxonomy Database classifier (GTDB-Tk). The colors of the branches correspond to different phyla, which were sorted in the legend according to the clockwise order they appear in the tree, starting from ASO40. The tracks (from inner to outer) denote the MAGs quality, number of contigs, and the lowest taxonomic rank at which it could be classified according to GTDB-Tk (F: family; G: genus; S: species), corresponding to the name shown in the outer track.
Figure 3
Figure 3
Phylogenetic relationships and AAI values among five Halobacteria MAGs recovered in this study (pointed with red arrows) and the 313 NCBI reference archaeal genomes from this class. The distance tree was inferred from the multiple sequence alignment of 53 archaeal marker proteins, as defined by the GTDB-Tk tool. The bootstrap values were omitted for more clarity. The different families are indicated with colors.
Figure 4
Figure 4
Phylogenetic relationships and AAI values among the MAG ASO22 (pointed with a red arrow) and the 30 NCBI reference archaeal genomes from the class Thermoplasmata. The distance tree was inferred from the multiple sequence alignment of 53 archaeal marker proteins, as defined by the GTDB-Tk tool. The bootstrap values correspond to 1000 iterations.
Figure 5
Figure 5
Predicted molecular functions encoded in the bacterial MAGs recovered from Salar de Ascotán. (A): Categorization of the metabolic pathways and molecular functions (selected categories) according to DRAM analysis. The heatmap denotes the presence/absence of the genes required for the corresponding function (panels to the right show). (B): Treemap showing the relative proportion of metal and biocide resistance genes found among the sum of the bacterial MAGs. The colors represent the element(s) and compound(s) to which the respective gene confers resistance.
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