Cellular life from the three domains and viruses are transcriptionally active in a hypersaline desert community

Uritskiy, Gherman; Tisza, Michael J.; Gelsinger, Diego Rivera; Munn, Adam; Taylor, James; DiRuggiero, Jocelyne

doi:10.1111/1462-2920.15023

Cited by 22 publications

(18 citation statements)

References 68 publications

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“…Our analysis of MAGs uncovered that these population genomes harboured a more diverse metabolic potential compared to those previously reported from desert endolithic habitats (Crits‐Christoph et al ., 2016a,b; Uritskiy et al ., 2019, 2020). For example, in addition to oxygenic photosynthesis by Cyanobacteria , several Proteobacteria , Gemmatimonidetes and Chloroflexi MAGs harboured genes involved in anoxygenic phototrophy (AP).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, no other substrate than gypsum has been shown to harbour fungi in the hyper‐arid Atacama Desert, which might be linked to the higher water absorption capacity of this substrate (Wierzchos et al ., 2011). The higher abundance of algae at the KM site suggests that they might significantly contribute to the organic carbon budget of the community, as previously reported in halite endoliths using metatranscriptomics (Uritskiy et al ., 2020). However, even when algae were taken into account, the ratio of oxygenic phototrophs to heterotrophic taxa was lower at KM than at the more arid CL and MTQ sites.…”

Section: Discussionmentioning

confidence: 99%

“…In this small‐scale habitat, composed of pores, cracks and fissures of various sizes and connectedness, the rock substrate filters out UV radiation and enhances access to water (Walker and Pace, 2007; Wierzchos et al ., 2012). While in extreme deserts soils represent transitory microbial habitats (Crits‐Christoph et al ., 2013; Schulz‐Makuch et al ., 2018), lithic communities form ‘islands of life’, exhibiting unexpected species richness and primary productivity (Crits‐Christoph et al ., 2016a,b; Lacap‐Bugler et al ., 2017; Goordial et al ., 2017; Meslier et al ., 2018; Uritskiy et al ., 2019; Qu et al ., 2020a; Uritskiy et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

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Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments

Ertekin

Meslier

Browning

et al. 2020

Environmental Microbiology

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Endolithic (rock-dwelling) microbial communities are ubiquitous in hyper-arid deserts around the world and the last resort for life under extreme aridity. These communities are excellent models to explore biotic and abiotic drivers of diversity because they are of low complexity. Using high-throughput amplicon and metagenome sequencing, combined with X-ray computed tomography, we investigated how water availability and substrate architecture modulated the taxonomic and functional composition of gypsum endolithic communities in the Atacama Desert, Chile. We found that communities inhabiting gypsum rocks with a more fragmented substrate architecture had higher taxonomic and functional diversity, despite having less water available. This effect was tightly linked with community connectedness and likely the result of niche differentiation. Gypsum communities were functionally similar, yet adapted to their unique micro-habitats by modulating their carbon and energy acquisition strategies and their growth modalities. Reconstructed population genomes showed that these endolithic microbial populations encoded potential pathways for anoxygenic phototrophy and atmospheric hydrogen oxidation as supplemental energy sources.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments

Ertekin

Meslier

Browning

et al. 2020

Environmental Microbiology

Self Cite

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“…The NaCl-saturated brine films here are exposed to intense ultraviolet radiation and prone to cycles of salt efflorescencedeliquescence (Hallsworth, 2020). Combining metagenomic and metatranscriptomic analyses (in both light and dark conditions), Uritskiy et al (2021) identify microbes responsible for the essential metabolic functions. One important finding was that the only eukaryote of the community, a novel Dolichomastix alga, is the major contributor of photosynthetic transcripts.…”

Section: 'Ecophysiology Of Extremophiles' Special Issuementioning

confidence: 99%

Astrobiology of life on Earth

Hallsworth

Mancinelli

Conley

et al. 2021

Environmental Microbiology

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Summary Astrobiology is mistakenly regarded by some as a field confined to studies of life beyond Earth. Here, we consider life on Earth through an astrobiological lens. Whereas classical studies of microbiology historically focused on various anthropocentric sub‐fields (such as fermented foods or commensals and pathogens of crop plants, livestock and humans), addressing key biological questions via astrobiological approaches can further our understanding of all life on Earth. We highlight potential implications of this approach through the articles in this Environmental Microbiology special issue ‘Ecophysiology of Extremophiles’. They report on the microbiology of places/processes including low‐temperature environments and chemically diverse saline‐ and hypersaline habitats; aspects of sulphur metabolism in hypersaline lakes, dysoxic marine waters, and thermal acidic springs; biology of extremophile viruses; the survival of terrestrial extremophiles on the surface of Mars; biological soils crusts and rock‐associated microbes of deserts; subsurface and deep biosphere, including a salticle formed within Triassic halite; and interactions of microbes with igneous and sedimentary rocks. These studies, some of which we highlight here, contribute to our understanding of the spatiotemporal reach of Earth'sfunctional biosphere, and the tenacity of terrestrial life. Their findings will help set the stage for future work focused on the constraints for life, and how organisms adapt and evolve to circumvent these constraints.

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“…Crits-Christoph et al ( 32 ) identified viral sequences and their potential hosts in halite endoliths of the Atacama. Additionally, Uritskiy et al ( 33 ) detected transcriptionally active viruses potentially infecting Halobacteria also inhabiting halite salt nodules in a salar located in the Atacama Desert. These niche halite host-virus relationships highlight the need to characterize the impact of viruses in broad desert soils that represent one of the largest and rapidly expanding terrestrial ecosystems on the planet (∼35% of the Earth’s land surface [ 34 ]).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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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.

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Cellular life from the three domains and viruses are transcriptionally active in a hypersaline desert community

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 22 publications

References 68 publications

Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments

Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments

Astrobiology of life on Earth

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

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