Is atmospheric chemosynthesis an overlooked microbial process in soil?
Dr. Belinda Ferrari
Associate Professor, University of New South Wales, Australia
Angelique Ray
PhD Candidate, University of New South Wales, Australia
Figure 1. Image of Dr Belinda Ferrari, PhD candidate Eden Zhang (at front) and Dr Daniel Wilkins sampling soils from Mitchell Peninsula, in the Windmill Islands region of Eastern Antarctica during their 2019 expedition. Photo credit: Catherine King.
In Antarctica, soil bacteria dominate and drive ecosystem processes, particularly carbon and nitrogen cycling. In Eastern Antarctica, a proportion of bacteria appear to survive the freezing and severe carbon and moisture-limited conditions by depending on a hydrogen-oxidation strategy that energetically supports primary production via a new lineage of RuBisCO, Type 1E. This novel mode of chemoautotrophy, coined ‘atmospheric chemosynthesis’, is distinct from photosynthesis or geothermal chemotrophy where the consumption of ubiquitous trace levels of atmospheric gases (H2, CO & CO2), provide the energy and carbon needs for bacteria to literally ‘live on air’.
The initial discovery of atmospheric chemosynthesis was made from soil microbiomes in two sites in Eastern Antarctica. Therefore, many questions remain; is this new mode of primary production restricted to East Antarctica, or is it a global, overlooked microbial process in soil? To answer this question, we used quantitative PCR to quantify key genetic determinants of this proposed metabolic process; RuBisCO Type 1E (rbcL1E) and high affinity 1h-[NiFe]-hydrogenase (hhyL), relative to overall bacterial community size as indicated through 16S rRNA gene quantification. We analysed 122 soils sampled from 12 sites that span the ‘three poles’ and found that indeed, trace gas oxidation and carbon fixation genes are ubiquitous, with the genetic determinants present in soils that lack traditional phototrophs (McMurdo Dry Valleys) and as well as in sites that are richer in phototrophs such as plants, algae and cyanobacteria (High-Arctic, Tibetan Plateau).
Figure 2. Robinson Ridge Hut, in the Windmill Islands region, Eastern Antarctica. Atmospheric chemosynthesis was first discovered in soils from this nutrient-limited, arid desert. Photo credit: Belinda Ferrari.
For the Antarctic and High-Arctic sites, we used correlation analyses against 26 measured soil physiochemical environmental parameters to find that RuBisCO Type 1E and high affinity 1h-[NiFe]-hydrogenase genes were associated with lower soil moisture, carbon and nitrogen content. This finding was not unexpected, given that atmospheric chemosynthesis was first discovered in the cold, arid and hyper-arid soils of the Windmill Island’s and Vestfold Hills regions of Eastern Antarctica. To date, the pathways for this new metabolic process are theoretical, in part because bacteria with this capacity are proving difficult to culture in the laboratory. What we have found from this research, is a widespread genetic potential for desert soil microbiomes to be supported by this minimalistic mode of primary production. The implications of this carbon fixation process as being more common to microbial communities, rather than a being a unique specialist process, is substantial, with the contributions to soil carbon sequestration likely to be more significant than we first realised. Moreover, the fact that bacteria can use trace gases to survive is opening up new avenues in the search for biosignatures for microbial life on other planets.
Publication: Ray A, Zhang E, Terauds A, Ji M, Kong W and Ferrari BC (2020) Soil Microbiomes With the Genetic Capacity for Atmospheric Chemosynthesis Are Widespread Across the Poles and Are Associated With Moisture, Carbon, and Nitrogen Limitation. Frontiers in Microbiology 11: 1936. https://doi.org/10.3389/fmicb.2020.01936