Atmospheric trace gases support primary production in Antarctic desert surface soil

Abstract

Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities 1-3 . Given that phototroph abundance varies across these Antarctic soils 2,4 , an enduring question is what supports life in those communities with low photosynthetic capacity 3,5 . Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities. We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation 6,7 . Soil microcosms aerobically scavenged atmospheric H 2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO 2 fixation. We propose that atmospheric H 2 , CO 2 and CO provide dependable sources of energy and carbon to support these communities, which suggests that atmospheric energy sources can provide an alternative basis for ecosystem function to solar or geological energy sources 8,9 . Although more extensive sampling is required to verify whether this process is widespread in terrestrial Antarctica and other oligotrophic habitats, our results provide new understanding of the minimal nutritional requirements for life and open the possibility that atmospheric gases support life on other planets.Terrestrial Antarctica is among the most extreme environments on Earth. Its inhabitants experience the cumulative stresses of freezing temperatures, limited carbon, nitrogen and water availability, strong UV radiation, and frequent freeze-thaw cycles 2,10,11 . Although it was once believed that these conditions restrict life, we now know that the continent hosts a surprising diversity of macrofauna and microbiota 1,2,12 . Surveys indicate that the phylum-level composition of microbial communities in Antarctic soils is similar to those of temperate soils 3 , but Antarctic communities are highly specialized at the species level and strongly structured by physicochemical factors 1,3,10 . In many Antarctic soils, microorganisms are thought to live in dormant states 2 , with metabolic energy directed towards cell maintenance rather than growth 13 . However, it is unclear how these communities obtain the energy and carbon needed for maintenance, given that these soils are often low in organic carbon and contain few classical primary producers 2,5 .

Species interactions and distinct microbial communities in high Arctic permafrost affected cryosols are associated with the CH4 and CO2 gas fluxes

“…The candidate phylum AD3 was also detected in active layer and permafrost soils of an upland Alaskan boreal forest, similar to our study the prevalence of this phylum increased with depth (Taş et al, 2014). Little is known about this uncultured candidate phylum, other than that it is often present in the active layers of permafrost affected Arctic, alpine and Antarctic desert soils (Tas¸et al, 2014;Frey et al, 2016;Ji et al, 2017). Verrumicrobia and Gemmatimonadetes were at a higher relative abundance at the IWP site than in other permafrost affected soils (Gittel et al, 2014;Taş et al, 2014), these phyla were also at a relatively higher abundance in the deeper soils.…”

A vision for a ‘microbcentric’ future

“…The evolutionary processes have generated way more lineages and lifestyles than are known, and in acknowledgement of this, the literature speaks of the extent of undiscovered ‘microbial dark matter’ (Rinke et al ., ). As omic efforts uncover more and more lineages (Castelle and Banfield, ), so do discoveries (not all omics‐based) of unexpected microbial ‘lifestyles’ – nitrogen‐fixing bacteria producing methane (Zheng et al ., ), Antarctic soil bacteria scavenging atmospheric hydrogen (Ji et al ., ), filamentous sediment bacteria transporting electrons over centimetre distances (Pfeffer et al ., ), Antarctic membrane vesicle encapsulated archaeal plasmids disseminating like viruses (Erdmann et al ., ) – lots of wonderful examples. So, one wise step forward would be to resist using pigeon‐holed expectations and instead let the systems openly report back about which microbes are present, what they are doing and how they are being so extraordinary.…”

H2 clumped isotope measurements at natural isotopic abundances

“…H 2 has a strong link with microbial life; for example, it is produced in soils and in the ocean in the process of bacterial N 2 fixation, and in microbial fermentation processes. It is an important subsistence source of energy for soil microbes, which makes soil uptake the most important sink for atmospheric H 2 ; it is also an important source of energy for other (chemoautotrophs, extremophiles) microbes . It is involved in anoxic methane formation, for example in wetlands.…”