Functional exploration of natural product metabolism and metatranscriptomic analyses in uncultivated soil bacteria from the Talabre-Lejía transect (Atacama desert)

Abstract

Soils are heterogeneous and complex environments, and bacterial competition, cooperation, and communication dynamics there are mediated through the secretion of natural products (NPs) synthesized in specialized pathways allowing diverse survival strategies to arise in oligotrophic conditions. Due to the vast array of thriving mechanisms, classification of compound classes and comparative approaches turn out necessary means to assess specialized metabolism (SM) in evolutionary and ecological contexts. Complementing current advances in the field of genome mining with transcriptional data enables better understanding of how often these metabolites are produced in natural settings and what stimuli set their production off. Here, a dataset of 190 biosynthetic gene clusters (BGCs) of mainly unknown functions was obtained from six metagenomic samples of the Atacama Desert revealing site- and/or phylum-specific behaviours. Acidobacteria was found to be the most abundant and the most SM-enriched taxa in these soils. A complete hybrid region of ~130 kb was fully predicted making it one of the largest to be directly recovered from an environmental sample. Examination of functional annotation of essential and accessory specialized genes showed association between biosynthetic classes of compounds and categories of orthologs such as NRPS/T1PKS with transposases and binding protein-dependant transport systems, and terpenes with the arsenic regulator ArsR and the iron transporter TonB. Manual curation of protein family domains of reference BGCs from gene cluster families (GCFs) suggest that shared biological functions of the Talabre-Lejía transect are mainly advocated to antibiotic biosynthesis, nitrogen metabolism, oxidative stress, and metal resistance. This study provides insights on functional co-occurrence patterns of NP-encoding repertories obtained from genomic analyses of 53 metagenome-assembled drafts (MAGs) recovered from a rare natural environment throughout a scalable pipeline constructed upon considerations for researchers with no bioinformatic background.