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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.

SUBMITTER: Hwang Y

PROVIDER: S-EPMC8269230 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The Atacama Desert is one of the driest deserts in the world and its soil, with extremely low moisture, organic carbon content, and oxidizing conditions, is considered to be at the dry limit for life. RESULTS: Analyses of high throughput DNA sequence data revealed that bacterial communities from six geographic locations in the hyper-arid core and along a North-South moisture gradient were structurally and phylogenetically distinct (ANOVA test for observed operating taxonomic units at 97% similarity (OTU0.03), P <0.001) and that communities from locations in the hyper-arid zone displayed the lowest levels of diversity. We found bacterial taxa similar to those found in other arid soil communities with an abundance of Rubrobacterales, Actinomycetales, Acidimicrobiales, and a number of families from the Thermoleophilia. The extremely low abundance of Firmicutes indicated that most bacteria in the soil were in the form of vegetative cells. Integrating molecular data with climate and soil geochemistry, we found that air relative humidity (RH) and soil conductivity significantly correlated with microbial communities' diversity metrics (least squares linear regression for observed OTU0.03 and air RH and soil conductivity, P <0.001; UniFrac PCoA Spearman's correlation for air RH and soil conductivity, P <0.0001), indicating that water availability and salt content are key factors in shaping the Atacama soil microbiome. Mineralization studies showed communities actively metabolizing in all soil samples, with increased rates in soils from the southern locations. CONCLUSIONS: Our results suggest that microorganisms in the driest soils of the Atacama Desert are in a state of stasis for most of the time, but can potentially metabolize if presented with liquid water for a sufficient duration. Over geological time, rare rain events and physicochemical factors potentially played a major role in selecting micro-organisms that are most adapted to extreme desiccating conditions.

Project description:The extreme environmental conditions and lack of water on the soil surface in hyperarid deserts hamper microbial life, allowing only highly specialized microbial communities to the establish colonies and survive. Until now, the microbial communities that inhabit or have inhabited soils of hyperarid environments at greater depths have been poorly studied. We analyzed for the first time the variation in microbial communities down to a depth of 3.4 m in one of the driest places of the world, the hyperarid Yungay region in the Atacama Desert, and we related it to changes in soil physico-chemical characteristics. We found that the moisture content changed from 2 to 11% with depth and enabled the differentiation of three depth intervals: (i) surface zone A (0-60 cm), (ii) intermediate zone B (60-220 cm), and (iii) deep zone C (220-340 cm). Each zone showed further specific physicochemical and mineralogical features. Likewise, some bacterial phyla were unique in each zone, i.e., members of the taxa Deinococcota, Halobacterota, and Latescibacterota in zone A; Crenarchaeota, Fusobacteriota, and Deltaproteobacterium Sva0485 in zone B; and Fervidibacteria and Campilobacterota in zone C, which indicates taxon-specific preferences in deep soil habitats. Differences in the microbiota between the zones were rather abrupt, which is concomitant with abrupt changes in the physical-chemical parameters. Overall, moisture content, total carbon (TC), pH, and electric conductivity (EC) were most predictive of microbial richness and diversity, while total sulfur (TS) and total phosphorous (TP) contents were additionally predictive of community composition. We also found statistically significant associations between taxa and soil properties, most of which involved moisture and TC contents. Our findings show that under-explored habitats for microbial survival and existence may prevail at greater soil depths near water or within water-bearing layers, a valuable substantiation also for the ongoing search for biosignatures on other planets, such as Mars.

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

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