Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation

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.

Keywords: atmospheric chemosynthesis; carbon fixation; environmental drivers; photosynthesis; quantitative PCR; trace gases.

Figure 1

Map of the 14 sites studied with approximate sampling locations across the Vestfold Hills and Windmill Island regions of Eastern Antarctica, as well as the high Arctic and the Tibetan Plateau. Satellite image (Quantarctica v3 GIS package in QGIS 3.4.7).

Figure 2

Relative abundances of target genes associated with atmospheric chemosynthesis within polar desert soils. The proposed genetic determinants of this process were widely distributed across all 14 sites spanning Antarctica, the high Arctic, and Tibetan Plateau (A). Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) type IE (rbcL1E; B). 1h-[NiFe]-hydrogenase large subunit gene (hhyL). Large solid black lines indicate average relative abundances per site; the dotted black line indicates the mean relative abundance of all 14 sites (36.68% for rbcL1E and 5.22% for hhyL); the small, solid black lines represent individual data points; polygons represent the estimated density of the data.

Figure 3

Soil bacterial community diversity at a phylum level across all 14 cold desert sites, and their locations throughout the (A) Vestfold Hills, (B) Windmill Islands, (C) Norway, (D) Canada, and (E) Tibetan Plateau. Actinobacteria dominated all soils, with average site-level relative abundances ranging from 23.6% at The Ridge to 58.6% at Herring Island. Proteobacteria, Chloroflexi, Bacteroidetes, and Acidobacteria were also highly abundant. In contrast, Cyanobacteria were present in low relative abundances accounting for <1% of the bacterial communities in eight sites, increasing to 5–9% within the Alexandra Fjord Highlands, Rookery Lake, Casey station, and Browning Peninsula. Within the Windmill Islands region, Candidatus Eremiobacterota was present in high relative abundances, with site-level averages ranging between 0.02% at Herring Island and 7.42% at Mitchell Peninsula. Similarly, Candidatus Dormibacterota was also present in high relative abundances in the Windmill Islands only.

Figure 4

NMDS plots showing the relationships among samples on a regional and local scale for (A,C) measured soil physicochemical parameters and (B,D) bacterial community composition at phylum level. Soil samples displayed greater environmental and bacterial community similarities within rather than between regions, as indicated by the formation of regional-level clustering. Bacterial communities within the high Arctic samples (Norway and Canada) were highly similar to each other with the clusters overlapping. Soil samples clustered according to site, indicating that soils from the same location share similar environmental conditions and bacterial community structures. For both environmental and bacterial communities, the greatest dissimilarity was observed within the Windmill Islands although variation in physicochemical parameters was also observed across the high Arctic sites, predominantly Alexandra Fjord Highlands.

Figure 5

Spearman correlations between the relative abundance of the two target genes, rbcL1E and hhyL, against all 26 measured physicochemical parameters for the 117 Antarctic and high Arctic soils. rbcL1E and hhyL each produced positive correlations with soil conductivity, pH, and sand composition as well as with greater abundances of various oxides. rbcL1E and hhyL both occurred in higher abundance within samples of low moisture, total carbon (TC), and total nitrogen (TN). rbcL1E also occurred in higher abundance within samples of low NO₃⁻ and mud composition.