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 dispersal of diverse and abundant viruses that infect a wide range of hosts over 205 km across the desert. Host genomes encoded both adaptive and innate immune systems, providing evidence of viral predation being a key selective pressure along with abiotic stresses. Viral genomes carried extremotolerance features (i.e. DNA repair proteins, enzymes against oxidative damage) and other auxiliary metabolic genes, indicating that viruses could mediate the spread of microbial resilience against environmental stress across the desert. 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.ImportanceDeserts 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 indicate that viruses are abundant, diverse and 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 evolutionary dynamics that shape the unique and poorly understood host-virus relationships in desert soils.

Host-Associated Phages Disperse across the Extraterrestrial Analogue Antarctica

“…Ralstonia phages detected in Arctic viromes were shown to transduce genomic information of cold-shock proteins to their hosts (47), a clear asset for microorganisms in polar environments. However, we did not find transduction of beneficial genes, which seems to be common in extreme environments (48).…”

Host-associated phages disperse across the extraterrestrial analogue Antarctica

“…Ralstonia phages detected in Arctic viromes were shown to transduce genomic information of cold-shock proteins to their hosts (47), a clear asset for microorganisms in polar environments. However, we did not find transduction of beneficial genes, which seems to be common in extreme environments (48).…”

“…Ralstonia phages detected in Arctic viromes were shown to transduce genomic information of coldshock proteins to their hosts (49), which would be an asset for microorganisms in polar environments. Although we did not find cold shock genes on PGFs in this study, transduction of beneficial genes, which is common in extreme environments (50), could theoretically be another reason why Ralstonia hosts do not apply CRISPR defenses against their phages. Some Ralstonia phages occur as non-integrative, episomal forms, e.g., RS603, a hybrid of RSM1/3 infecting the phytopathogen Ralstonia solanacearum (51), whose genome lacks a resolvase domain (Figure 2A), but many mesophilic Ralstonia also occur as lysogens (52).…”

Prokaryotic taxonomy and functional diversity assessment of different sequencing platform in a hyper-arid Gobi soil in Xinjiang Turpan Basin, China

“…Modern high-throughput sequencing technologies classified as next generation sequencing (NGS) can not only detect very small amounts of microbial DNA, but also deliver results that are closer to the real community structure of microorganisms due to the large sequencing volume and high-throughput of these methods. Hwang et al investigated viral genomes from the Atacama Desert using Illumina HiSeq 2500 to reveal the diversity and ecological impact of viruses inhabiting hyper-arid soils (Hwang et al, 2021). Using the same sequencing platform, Le et al compared the metagenomes of soils from extreme hyper-arid deserts to understand the relation between prokaryotic communities and stress responses in soil systems (Le et al, 2016).…”