Abstract

ABSTRACTViruses 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.

Highlights

  • Viruses play an essential role in shaping microbial community structures and serve as reservoirs for genetic diversity in many ecosystems

  • With little water availability and extended periods of drought, hyperarid desert soils present a distinct model for studying viral persistence and dispersal

  • We predicted viral scaffolds in 11 assembled metagenomes (4.1 Gbp in total) from three different boulder fields (Lomas Bayas [L], Maria Elena [M], and Yungay [Y]), which were previously studied for the impact of boulder cover on the soil microbiome, uncovering highly adapted microbes sheltered below the boulders of expansive boulder fields in the Atacama Desert hyperarid core [29]

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Summary

Introduction

Viruses play an essential role in shaping microbial community structures and serve as reservoirs for genetic diversity in many ecosystems. 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. Understanding the abundance and diversity of viruses as well as their interactions with extremotolerant microbes in environments can highlight the unique roles viruses may play in driving the adaptation of their hosts and reveal the dispersal and diversification of viruses in sparsely populated and harsh environments. With little water availability and extended periods of drought, hyperarid desert soils present a distinct model for studying viral persistence and dispersal. In these ecosystems, viral mobility is limited compared to that in aquatic environments, in which both viruses and hosts freely diffuse [14]

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