Abstract
Soil microbiomes within oligotrophic cold deserts are extraordinarily diverse. Increasingly, oligotrophic sites with low levels of phototrophic primary producers are reported, leading researchers to question their carbon and energy sources. A novel microbial carbon fixation process termed atmospheric chemosynthesis recently filled this gap as it was shown to be supporting primary production at two Eastern Antarctic deserts. Atmospheric chemosynthesis uses energy liberated from the oxidation of atmospheric hydrogen to drive the Calvin-Benson-Bassham (CBB) cycle through a new chemotrophic form of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), designated IE. Here, we propose that the genetic determinants of this process; RuBisCO type IE (rbcL1E) and high affinity group 1h-[NiFe]-hydrogenase (hhyL) are widespread across cold desert soils and that this process is linked to dry and nutrient-poor environments. We used quantitative PCR (qPCR) to quantify these genes in 122 soil microbiomes across the three poles; spanning the Tibetan Plateau, 10 Antarctic and three high Arctic sites. Both genes were ubiquitous, being present at variable abundances in all 122 soils examined (rbcL1E, 6.25 × 103–1.66 × 109 copies/g soil; hhyL, 6.84 × 103–5.07 × 108 copies/g soil). For the Antarctic and Arctic sites, random forest and correlation analysis against 26 measured soil physicochemical parameters revealed that rbcL1E and hhyL genes were associated with lower soil moisture, carbon and nitrogen content. While further studies are required to quantify the rates of trace gas carbon fixation and the organisms involved, we highlight the global potential of desert soil microbiomes to be supported by this new minimalistic mode of carbon fixation, particularly throughout dry oligotrophic environments, which encompass more than 35% of the Earth’s surface.
Highlights
As a percentage of 16S ribosomal RNA (rRNA) gene copies/g soil, average relative abundances of rbcL1E were highest within the Vestfold Hills (58.1%), followed by the Tibetan Plateau (42.1%), the Windmill Islands (31.0%), and the high Arctic (10.0%)
We confirm that the genetic determinants of this new form of chemoautotrophy are widespread and abundant throughout soil microbiomes of geographically distinct polar regions throughout Antarctica, the high Arctic, and the Tibetan Plateau
These findings support the hypothesis that this minimalistic carbon fixation strategy may be considered a globally occurring phenomenon and an important widespread survival adaptation in oligotrophic desert soil ecosystems
Summary
Dry oligotrophic environments encompass more than 35% of the Earth’s surface (Mares and History, 1999). Dry environments are expected to expand to cover up to 56% of the Earth’s surface by the end of the 21st century (Cherlet et al, 2018) Despite their exposure to frequent freeze-thaw cycles, intense UV radiation, and limited carbon, nitrogen, and moisture availability (WynnWilliams, 1990; Yergeau et al, 2006; Margesin and Miteva, 2011; Pearce, 2012; Cowan et al, 2014), polar soil microbiomes are diverse and abundant, driving important ecological processes (Yergeau et al, 2006; Cowan et al, 2014; Kleinteich et al, 2017). Oligotrophic deserts comprising little to no detectable photoautotrophs are distributed worldwide, leading researchers to question what carbon and energy sources support the microbial communities functioning in these harsh ecosystems (Warren-Rhodes et al, 2006; Albertsen et al, 2013; Ferrari et al, 2015; Ji et al, 2015; Tebo et al, 2015; Zhang et al, 2020)
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