Leave no stone unturned: The hidden potential of carbon and nitrogen cycling by novel, highly adapted Thaumarchaeota in the Atacama Desert hyperarid core

Abstract

The hyperarid core of the Atacama Desert is an extremely harsh environment previously thought to be colonized by only a few heterotrophic bacterial species. In addition, carbon and nitrogen cycling in these highly oligotrophic ecosystems are poorly understood. Here we genomically resolved a novel genus of Thaumarchaeota, Ca. Nitrosodesertus, found below boulders of the Atacama hyperarid core, and used comparative genomics to analyze their pangenome and site-specific adaptations. Their genomes contain genes for ammonia oxidation and the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, indicating a chemolithoautotrophic lifestyle. Ca. Nitrosodesertus possesses the capacity for tolerating extensive environmental stress highlighted by the presence of genes against oxidative stress, DNA damage and genes for the formation of biofilms. These features are likely responsible for their dominance in samples with extremely low water content across three different boulder fields and eight different boulders. Genome-specific adaptations of the genomes included the presence of additional genes for UV resistance, heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins. Our results suggest that Thaumarchaeota mediate important carbon and nitrogen cycling in the hyperarid core of the Atacama and are part of its continuous and indigenous microbiome.

Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil

“…We predicted viral genomes in eleven assembled metagenomes (4.09 Gbp in total) from three different boulder fields (Lomas Bayas, L; Maria Elena, M; Yungay; Y) and two different soil compartments (Below boulder, B; Controlexposed soil adjacent to Boulder, C) (for analysis workflow see Figure 1, for the map of sampling locations see Figure 2). The metagenomes 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 (25). In total, 6809 out of 707,509 examined scaffolds were predicted to be viral.…”

“…In the studied metagenomes, only 17% of the high quality MAGs contained CRISPR arrays. In extreme environments such as the Atacama Desert, where only slow microbial replication is supported (25,26), it is plausible that CRISPR-Cas may not yield fast enough immune responses (36) for it to be prevalent. To predict possible host-virus interactions for hosts that lack CRISPR systems, VirHostMatcher (37) identified 3897 putative interactions between 73 MAGs and 132 viral scaffolds using d2* threshold of 0.3 (Figure 3b shows highest confidence interactions with d2* threshold of 0.25 for visualisation, Table S3 contains sample specific overview).…”

“…Detailed sampling procedure, DNA extraction and Illumina library preparation and sequencing can be found in Hwang et al (25).…”

“…The Atacama Desert is one of the harshest environments on Earth with its hyperarid core experiencing extreme desiccation with mean annual precipitation < 2 mm (24). The surface soil of the Atacama hyperarid core generally contains less than 1 wt% of water, and experiences high daily ultraviolet (UV) radiation (30 J⋅m −2 ), extreme diurnal temperature fluctuation (~ 60℃) (25) and additional osmotic pressure from the accumulation of salts (26,27). Scarce populations of highly adapted microbial communities consisting of Actinobacteria, Firmicutes, Chloroflexi (26)(27)(28) and more recently, Thaumarchaeota (25) were found to inhabit soils of the Atacama hyperarid core.…”

“…The surface soil of the Atacama hyperarid core generally contains < 1 wt % of water, and experiences high daily ultraviolet (UV) radiation (30 J⋅m −2 ) (28), extreme diurnal temperature fluctuations (~ 60℃) (29) and additional osmotic pressure from the accumulation of salts (28,30). Scarce populations of highly adapted microbial communities consisting of Actinobacteria, Firmicutes, Chloroflexi (28,30,31) and more recently, Thaumarchaeota (29) were found to inhabit soils of the Atacama hyperarid core. However, very little is known about viruses from these desert soil microbiomes.…”