Viral Community Structure and Potential Functions in the Dried-Out Aral Sea Basin Change along a Desiccation Gradient.

Abstract

The dried-out Aral Sea basin represents an extreme environment due to a man-made ecological disaster. Studies conducted in this unique environment revealed high levels of pollution and a specifically adapted microbiota; however, viral populations remained entirely unexplored. By employing an in-depth analysis based on the sequencing of metagenomic DNA recovered from rhizosphere samples of Suaeda acuminata (C. A. Mey.) Moq. along a desiccation gradient of 5, 10, and 40 years, we detected a diverse viral community comprising 674 viral populations (viral operational taxonomic units [vOTUs]) dominated by Caudovirales. Targeted analyses highlighted that viral populations in this habitat are subjected to certain dynamics that are driven mainly by the gradient of desiccation, the corresponding salinity, and the rhizosphere bacterial populations. In silico predictions linked the viruses to dominant prokaryotic taxa in the Aral Sea basin, such as Gammaproteobacteria, Actinomycetia, and Bacilli. The lysogenic lifestyle was predicted to be predominant in areas that dried out 5 years ago, representing the early revegetation phase. Metabolic prediction of viral auxiliary metabolic genes (AMGs) suggests that viruses may play a role in the biogeochemical cycles, stress resilience, and competitiveness of their hosts due to the presence of genes that are involved in biofilm formation. Overall, our study provides important insights into viral ecology in an extreme environment and expands our knowledge related to virus occurrence in terrestrial systems. IMPORTANCE Environmental viruses have added a wealth of knowledge to ecological studies with the emergence of metagenomic technology and approaches. They are also becoming recognized as important genetic repositories that underpin the functioning of terrestrial ecosystems but have remain moslty unexplored. Using shotgun metagenome sequencing and bioinformatic tools, we found that the viral community structure was affected during natural revegetation in the dried-up Aral Sea area, a model habitat for investigating natural ecological restoration but still understudied. In this study, we highlight the importance of viruses, elements that are overlooked, for their potential contribution to terrestrial ecosystems, i.e., nutrient cycles, stress resilience, and host competitiveness, during natural revegetation.