Project

4406

Chief Investigator

FERRARI, A/Prof. Belinda - University of New South Wales

Title

Atmospheric carbon fixation: a novel strategy driving niche development and climate adaptation in polar desert soils

Project aims

The aim of this project is to challenge our global understanding of carbon fixation. In most ecosystems, phototrophic carbon fixation by plants, algae and cyanobacteria is the primary production strategy supporting higher trophic life. Yet no genetic evidence for photosynthesis exists in desert soils in the Windmill Islands, Antarctica. Our objective is to establish what primary production process dominates these nutrient-starved soils. We propose that atmospheric chemotrophy, i.e. the consumption of atmospheric hydrogen and CO gas supplies energy to support maintenance of these communities and the carbon to sustain biomass production. Secondly, we will determine if these processes are structuring soil microbial communities, particularly in response to climate change. The intended outcome is to arrive at a paradigm shift in our understanding of primary production by describing a third mode of carbon fixation distinct from phototrophy or geothermal chemotrophy for the first time.

Project gallery


Project Summary of the Season 2017/18

We have confirmed our hypothesis and confirmed that atmospheric gases alone are providing the carbon, reductant and energy needs required to support life in nutrient-poor desert soils of eastern Antarctica. Our discovery of bacteria living on air is paradigm shifting as it provides new understanding of the nutritional limits required for life and extends the possibility for life not only on Earth but on other planets. Our research used a multidisciplinary approach, integrating metagenomics, molecular biology and biogeochemistry to find that trace levels of H2, CO2 and CO provide dependable sources of energy and carbon to support communities surviving in soils from Robinson Ridge, in the Windmill Islands and Adams Flat, in the Vestfold Hills region of east Antarctica. We propose that trace gas chemosynthesis is providing an alternative basis for ecosystem function to solar or geothermal energy sources. The next stage of the project is to extend this work to more Antarctic sites to determine if this is an isolated or a global phenomenon.

Project Summary of the Season 2018/19

Progress of this project has been substantial over the last 12 months. First, we completed an extremely successful field season where we resampled over 500 soils from Browning Peninsula, Robinson Ridge and the Mitchell Peninsula, east Antarctica. We also captured drone footage of all three sites which will be invaluable when interpreting changes to community structure over time. We will now determine how these soil microbiomes have shifted after 14 years of global change. At the same time we have completed an analysis of the original soil samples where we have found that the genetic determinants of trace gas chemosynthesis are indeed widespread, present in cold desert soils from east Antarctica, the Arctic and the Tibetan Plateau. This provides the new evidence that the capacity for bacteria to "live on air", that is trace levels of hydrogen, carbon dioxide and carbon monoxide, is significant and global process.

Project Summary of the Season 2019/20

Progress for this season has been significant despite challenges associated with COVID-19. We have extended our research on atmospheric chemosynthesis to cold desert sites spanning sites in Antarctica, the Arctic and Tibet, with preliminary data indicating that this novel process is indeed a global phenomenon. We now have soil microbiome and physiochemistry data for a subset of the newly sampled soils from across the Windmill Islands region. The next challenge is to integrate this metadata to understand how these sensitive microbial communities will respond in a changing environment.

Project Summary of the Season 2020/21

The overall aim of this project is to understand how atmospheric chemotrophy supports primary production and drives microbial community structure in eastern Antarctica. As part of a decadal plan to monitor community shifts and potential effects from global change, this project will also compare microbial ecosystems between 2005 and 2018 at three remote Windmill Island sites. In the last 12 months we have shown that this new primary production strategy, that is reliant on atmospheric gases for dark-carbon fixation is widespread, occurring alongside photosynthesis in arid deserts spanning the three poles; Antarctica, the Arctic and Tibet. We have now completed amplicon sequencing and soil physicochemical analysis of over 300 soils, with COVID-19 related delays meaning we have only now begun downstream analyses. The next challenge is to integrate this metadata to understand how these sensitive microbial communities will respond in a changing environment.

Final Summary of Project Achievements

This project led to the discovery of a minimalistic mode of primary production occurring at the limits for life in the desert soils of eastern Antarctica. The discovery of this novel mode of bacterial growth, now coined 'atmospheric chemosynthesis', is distinct from photosynthesis or geothermal chemotrophy, where the consumption of atmospheric gases (H2, CO & CO2) provides the energy and carbon needs for bacteria to literally 'live on thin air'. The implications of this overlooked carbon fixation process are substantial, with research now prioritising H2 and CO gas as biosignatures for life on other planets. Our initial discovery of atmospheric chemosynthesis was made from Antarctic bacteria. Since then, we have produced a body of evidence that confirms that process is ubiquitous across cold deserts, supporting primary production in soils from across the three poles. Furthermore, given Antarctica is warming at an alarming rate, we sampled soil communities from the Windmill Islands region over time. We predicted that novel bacteria, which are genetically capable of living on air and which prefer dry, nutrient poor environments will be sensitive to increased soil fertility and moisture. Our results showed that indeed over just a decade of change, these rare bacteria are sensitive, with a significant decrease in their abundance coinciding with an increase in algae and bacteria which perform traditional photosynthesis. Our study highlights the need to protect even the smallest forms of life and provides a solid foundation for future conservation planning across the region.

Project Summary of the Season 2021/22

The overall aim of this project is to understand how atmospheric chemotrophy supports primary production and drives microbial community structure in eastern Antarctica. As part of a decadal plan to monitor community shifts and potential effects from global change, this project will also compare microbial ecosystems between 2005 and 2018 at three remote Windmill Island sites. In the last 12 months we have shown that this new primary production strategy, that is reliant on atmospheric gases for dark-carbon fixation is widespread, occurring alongside photosynthesis in arid deserts spanning the three poles; Antarctica, the Arctic and Tibet. We have now completed amplicon sequencing and soil physicochemical analysis of over 300 soils, with COVID-19 related delays meaning we have only now begun downstream analyses. The next challenge is to integrate this metadata to understand how these sensitive microbial communities will respond in a changing environment.

Category 1: Peer-reviewed literature

Ji M., Greening C., van Wonterghem I., Carere C., Bay S.K., Steen J.A., Montgomery K., Lines T., Beardall J., van Dorst J., Snape I., Stott M.B., Hugenholtz I., Ferrari B.C. (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil, Nature 552(7685). 400-403; [Ref: 15993]

Ray A.E., Zhang E., Terauds A., Ji M., Kong W., Ferrari B.C. (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. .; [Ref: 16402]

Ji M., Williams T.J., Montgomery K., Wong H.L., Zaugg J., Berengut J.F. (2021) Candidatus Eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations, The ISME Journal 1-16; [Ref: 16403]

Bay S., Ferrari B., Greening C. (2018) Life without water: how do bacteria generate biomass in desert ecosystems?, Microbiology Australia 39. 28-32; [Ref: 16404]

Cowan D.A., Ferrari B.C., McKay C.P. (2022) Out of Thin Air? Astrobiology and Atmospheric Chemotrophy, Astrobiology .; [Ref: 16488]

Montgomery K., Williams T.J., Brettle M., Berengut J.F., Zhang E. (2021) Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient-poor Antarctic soils, Environmental Microbiology .; [Ref: 16489]

Ray A.E., Zaugg J., Benaud N., Chelliah D.S., Bay S., Terauds A. (2022) Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts, the ISME journal .; [Ref: 16704]