Diverse Viruses Carrying Genes for Microbial Extremotolerance in the Atacama Desert Hyperarid Soil

Abstract

Viruses play an essential role in shaping microbial community structures and serve as reservoirs for genetic diversity in many ecosystems. In hyperarid desert environments, where life itself becomes scarce and loses diversity, the interactions between viruses and host populations have remained elusive. Here, we resolved host-virus interactions in the soil metagenomes of the Atacama Desert hyperarid core, one of the harshest terrestrial environments on Earth. We show evidence of diverse viruses infecting a wide range of hosts found in sites up to 205 km apart. Viral genomes carried putative extremotolerance features (i.e., spore formation proteins) and auxiliary metabolic genes, indicating that viruses could mediate the spread of microbial resilience against environmental stress across the desert. We propose a mutualistic model of host-virus interactions in the hyperarid core where viruses seek protection in microbial cells as lysogens or pseudolysogens, while viral extremotolerance genes aid survival of their hosts. Our results suggest that the host-virus interactions in the Atacama Desert soils are dynamic and complex, shaping uniquely adapted microbiomes in this highly selective and hostile environment. IMPORTANCE Deserts are one of the largest and rapidly expanding terrestrial ecosystems characterized by low biodiversity and biomass. The hyperarid core of the Atacama Desert, previously thought to be devoid of life, is one of the harshest environments, supporting only scant biomass of highly adapted microbes. While there is growing evidence that viruses play essential roles in shaping the diversity and structure of nearly every ecosystem, very little is known about the role of viruses in desert soils, especially where viral contact with viable hosts is significantly reduced. Our results demonstrate that diverse viruses are widely dispersed across the desert, potentially spreading key stress resilience and metabolic genes to ensure host survival. The desertification accelerated by climate change expands both the ecosystem cover and the ecological significance of the desert virome. This study sheds light on the complex virus-host interplay that shapes the unique microbiome in desert soils.

Patterns and ecological drivers of viral communities in acid mine drainage sediments across Southern China

“…The relatively low species richness, broad range and steep gradients of geochemical variables promise more straight-forward establishment of ecological patterns and underlying mechanisms. The diversity and community dynamics of viruses in extreme environments such as the Atacama Desert 17 , cryosphere 18 , 19 , acid mine drainage (AMD) environment 20 , 21 , and Earth’s subsurface 7 , 22 , 23 have recently been investigated through meta-omics approaches; yet, extensive sampling and analysis of viral communities across large geographic scales to resolve their ecological distribution patterns and drivers have not been conducted. Here we strive to address this knowledge gap by utilizing a massive metagenomic data set generated from 90 AMD sediments sampled across Southern China (Fig.…”

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

“…In general, viral diversity in extreme environments is still largely unexplored ( 26 , 27 ). In comparison to other hyperarid and saline environments, i.e., the Atacama Desert ( 28 , 29 ) and the Peñahueca shallow saline lake ( 30 ), a relatively high number of vOTUs was detected in the Aral Sea basin. Viruses that were linked to distinct hosts contained auxiliary metabolic genes (AMGs) that may play roles in the biogeochemical cycles, competitiveness, and resilience against environmental stress of their putative hosts.…”

“…It was also suggested that the lysogenic lifestyle is predominant in harsh environments ( 36 ). In a recent study of the viral community in the Atacama Desert, Hwang and colleagues ( 29 ) suggested that under less favorable conditions, viruses likely undergo lysogeny cycles to seek protection in their host cells as a survival strategy. In the present study, the area that dried out 5 years ago was the soil zone that was nearest to the present shoreline of the Aral Sea and can be considered a hostile environment for most organisms due to its high salinity ( 3 ) compared to other sampling areas.…”

Heads in the clouds: marine viruses disperse bidirectionally along the natural water cycle

“…Additional MAGs that were excluded in the dRep process due to low quality in CheckM but had good contamination/completeness scores in uBin and formed their own cluster in the dRep compare mode were additionally considered for k-mer based virus-host linkages. Viral scaffolds were assigned to these MAGs using VirusHostMatcher 119 at a d2* threshold of 0.3, as previously performed 120 . Spacer-protospacer interactions and virus-host interactions based on k-mers were visualized using Cytoscape v.3.9 106 .…”