Leave no stone unturned: individually adapted xerotolerant Thaumarchaeota sheltered below the boulders of the Atacama Desert hyperarid core

Abstract

Background The hyperarid core of the Atacama Desert is an extremely harsh environment thought to be colonized by only a few heterotrophic bacterial species. Current concepts for understanding this extreme ecosystem are mainly based on the diversity of these few species, yet a substantial area of the Atacama Desert hyperarid topsoil is covered by expansive boulder accumulations, whose underlying microbiomes have not been investigated so far. With the hypothesis that these sheltered soils harbor uniquely adapted microbiomes, we compared metagenomes and geochemistry between soils below and beside boulders across three distantly located boulder accumulations in the Atacama Desert hyperarid core. Results Genome-resolved metagenomics of eleven samples revealed substantially different microbial communities in soils below and beside boulders, despite the presence of shared species. Archaea were found in significantly higher relative abundance below the boulders across all samples within distances of up to 205 km. These key taxa belong to a novel genus of ammonia-oxidizing Thaumarchaeota, Candidatus Nitrosodeserticola. We resolved eight mid-to-high quality genomes of this genus and used comparative genomics to analyze its pangenome and site-specific adaptations. Ca. Nitrosodeserticola genomes contain genes for ammonia oxidation, the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, and acetate utilization indicating a chemolithoautotrophic and mixotrophic lifestyle. They also possess the capacity for tolerating extreme environmental conditions as highlighted by the presence of genes against oxidative stress and DNA damage. Site-specific adaptations of the genomes included the presence of additional genes for heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins. Conclusion We provide the first genomic characterization of hyperarid soil microbiomes below the boulders in the Atacama Desert, and report abundant and highly adapted Thaumarchaeaota with ammonia oxidation and carbon fixation potential. Ca. Nitrosodeserticola genomes provide the first metabolic and physiological insight into a thaumarchaeal lineage found in globally distributed terrestrial habitats characterized by various environmental stresses. We consequently expand not only the known genetic repertoire of Thaumarchaeota but also the diversity and microbiome functioning in hyperarid ecosystems.

Candidatus Nitrosopolaris, a genus of putative ammonia-oxidizing archaea with a polar/alpine distribution

“…Nitrosocosmicus, and Ca . Nitrosodeserticola, the three described genera in the family Nitrososphaeraceae (Stieglmeier et al ., 2014; Lehtovirta-Morley et al ., 2016; Hwang et al ., 2021) (Fig. 2a; Suppl.…”

A novel order-level lineage of ammonia-oxidizingThaumarchaeotais widespread in marine and terrestrial environments

“…Recent AOA comparative population genomics and phylogenomic analyses have shown that V-type ATPase genes were widely distributed among deep-sea water column [11] and sedimentary [76] Nitrosopumilales AOA and desert Nitrososphaerales AOA populations [77]. Apart from the experimentally tested function in low pH adaptation, AOA V-type ATPase may be also coupled to sodium (Na + ) motive force at high pH levels and protect cells from high-salt stress [24, 77]. The ATPase subunit phylogenetic trees show that the AOA V-type ATPase subgroup rooted with Nitrosomirales AOA variants (Fig.…”

Geographically Disperse, Culturable Seed-Associated Microbiota in Forage Plants of Alfalfa (Medicago sativa L.) and Pitch Clover (Bituminaria bituminosa L.): Characterization of Beneficial Inherited Strains as Plant Stress-Tolerance Enhancers

“…In spite of this scenario, in recent decades, some alternatives have been developed to improve this situation. The use of beneficial bacteria as biotreatments is on the rise, since they are a sustainable and ecologically friendly alternative [ 30 , 31 , 32 ]. Among other mechanisms, these bacteria improve the response to different stresses by protecting the roots (exopolysaccharides and biofilms) and improving their number, length and distribution through the production of auxins, thereby reaching less accessible water sources.…”

“…Among other mechanisms, these bacteria improve the response to different stresses by protecting the roots (exopolysaccharides and biofilms) and improving their number, length and distribution through the production of auxins, thereby reaching less accessible water sources. In addition, they are capable of regulating other phytohormones such as ethylene through the production of ACC (1-aminocyclopropane-1-carboxylate) deaminase [ 30 , 33 ]. The action of this enzyme prevents the accumulation of ethylene during periods of drought, thus reducing the loss of leaves and roots, which allows more complex root architecture to be maintained [ 34 ].…”

“…Thus far, the most common sources of drought-tolerant enhancer bacteria have been desert soils or the rhizosphere of adapted plants [ 30 , 36 , 37 ], but new emerging isolation sources could be even more suitable. In this sense, the microbiota associated with seeds may represent a great advancement in these types of treatments [ 38 ].…”