Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

Abstract

Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, hydrogen oxidising bacteria support primary production through a novel carbon fixation process reliant on the chemoautotrophy-associated RuBisCO form IE. Here, biochemical assays show that atmospheric chemosynthesis occurs globally for primary production, contributing significantly to autotrophic carbon fixation throughout arid to hyperarid deserts in Antarctica, the high Arctic, and the Tibetan Plateau. Taxonomic and functional analyses were performed on 230 dereplicated medium-to-high quality metagenome-assembled genomes (MAGs) derived from 18 cold desert metagenomes and an additional 24,080 publicly available genomes. We infer that atmospheric chemosynthetic bacteria are widespread across environmental and clinical samples, increasing our knowledge of the bacterial phyla genetically capable of atmospheric chemosynthesis to seven, with key enzymes co-occurring within MAGs from four previously unidentified phyla; Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota. We informatically identify an additional group of high-affinity hydrogenases, group 1m [NiFe]-hydrogenase using phylogenetics, gene structure analysis and homology modelling and reveal substantial new genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity groups 1h and 1l [NiFe]-hydrogenases. Finally, we conclude that atmospheric chemosynthesis is a global phenomenon, extending throughout and beyond cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental and clinical reservoirs.

Geology defines microbiome structure and composition in nunataks and valleys of the Sør Rondane Mountains, East Antarctica

“…Moraines are characterized by a mixture of different bedrock types. Actinomycetota were found to be conspicuously more abundant than photoautotrophs in moraine substrates, with abundances up to 50% of the bacterial reads, which is consistent with studies from other hyper-arid regions of Antarctica (Bay et al, 2021;Ortiz et al, 2021;Ray et al, 2022), other cold deserts across the globe (An et al, 2013;Gupta et al, 2015) as well as hot deserts (see Raimond and Cowan 2022 and references therein). Species of this phylum are known to be able to outcompete other groups under the most arid conditions in oligotrophic soils, likely due to their high resistance to desiccation and starvation conditions (Battistuzzi and Hedges, 2008;Jones and Lennon, 2010).…”

“…Indeed, other highly abundant phylotypes of moraine substrates belonged to the Chloroflexota phylum, which is also often encountered in extremely arid and ultra-oligotrophic Antarctic environments (Ji et al, 2015). In such cyanobacteria-poor soils, part of the bacterial primary production might also be attributed to atmospheric H 2 , CO 2 and CO consumption by phylotypes of the Actinomycetota (including the order Solirubrobacterales), Chloroflexota and other taxa (Ji et al, 2017;Ortiz et al, 2021;Greening et al, 2022;Ray et al, 2022). Surprisingly, even in these very dry soils, Chlorophyta were the dominant eukaryotes, together with Cercozoa.…”

“…In top-soils of hyper-arid areas in the Antarctic, Chlorophyta, Ciliophora and Cercozoa are the most abundant eukaryotic phyla recorded, while Actinomycetota, Acidobacteriota, Bacillota and Chloroflexota are often the dominant bacterial phyla, similarly to edaphic niches of hot deserts (Ramond and Cowan, 2022). Some phylotypes of these bacterial phyla were recently found to be genetically equipped for the consumption of molecular hydrogen (H 2 ), CO 2 and CO from the atmosphere as energy and carbon sources (Ji et al, 2017;Ortiz et al, 2021;Greening et al, 2022;Ray et al, 2022). Actinomycetota are also abundant in environments with a higher organic carbon and moisture content, such as biological soil crusts (BSCs) or lithic niche refugia (i.e., hypolithic, endolithic habitats or wind protected rock cavities).…”

Microbial diversity in Antarctic Dry Valley soils across an altitudinal gradient

“…To infer the importance of trace gas chemotrophs (TGCs) and phototrophs to the interactions with the soil microbial communities of the sample sites, these were manually assigned to ASVs based on their genus level taxonomy. To identify potential TGCs within our dataset, a list of genera that have been shown to have the capability to perform hydrogen oxidation was compiled from previous studies (Supplementary Table S5) (Ortiz et al, 2021;Ray et al, 2022). All ASVs belonging to the classes Cyanobacteriia and Chloroflexia were considered phototrophic.…”

“…As suggested by the correlations between phyla abundance and altitude, soils in high altitudes were enriched in photosynthetic genera, including common cyanobacterial residents in the Antarctic continent such as Tychonema (Salmaso et al, 2016) and Phormidium (Lumian et al, 2021). By comparison, low altitude soils were enriched in Truepera, which is a multi-stress tolerant bacterial genus (Albuquerque et al, 2005), as well as the genera Rubrobacter and Ornithinicoccus, both of which have been recently associated with the capability to scavenge trace-gases from the atmosphere in cold deserts (Ortiz et al, 2021;Ray et al, 2022) (Figure 4A). In the case of soil fungal populations, the low altitude were dominated by fungi ASVs of unknown taxonomy (Figure 4B).…”