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The role of the Earth’s mycelial community and enzyme activity on global atmospheric CO2 and COS budgets

Periodic Reporting for period 2 - COSMYCA (The role of the Earth’s mycelial community and enzyme activity on global atmospheric CO2 and COS budgets)

Periodo di rendicontazione: 2024-01-01 al 2025-06-30

Forests across the world remove a third of our fossil fuel CO2 emissions from the atmosphere every year. A rate predicted by land surface models to have increased over the past century in response to CO2 fertilisation. However, there is evidence that for certain groups of tree species rising CO2 does not stimulate biomass increase and these differing growth responses to CO2 may be linked to the belowground mycorrhizal fungal partners that the trees interact with. As nutrient limitations and climate feedbacks start to impact forest-fungal interactions and ecosystem productivity, predicting the fate of the land C sink reliably is of societal importance.

To provide insights on forest-fungal interactions and their future response to rising CO2 the COSMYCA project proposes to use carbonyl sulphide (COS), a natural trace gas in the atmosphere that shares a structural resemblance to CO2. Historical patterns in atmospheric COS concentrations are preserved in ice cores and atmospheric sampling stations and satellites are monitoring its more recent behaviour across the planet. Like CO2, COS is removed in large quantities from the atmosphere during the summer because plants also consume COS with the same enzyme, carbonic anhydrase during photosynthesis, providing a unique and independent constraint on the photosynthetic activity of the terrestrial biosphere over time. However, fungi and soil organisms also contain carbonic anhydrases and may also be important sinks for atmospheric COS. Furthermore, N fertilisation reduces the activity of carbonic anhydrases and thus COS uptake, highlighting a more complex, historically dynamic relationship between photosynthesis, belowground communities and COS than previously considered.

The overall objectives of COSMYCA will be to characterise and quantify how changes in atmospheric CO2 and soil nutrient characteristics drive changes in plant-fungal metabolism and how forest ecosystems impact the exchange of COS and CO2 with the atmosphere, now, and over the last century.
The ERC project COSMYCA is currently unveiling how diverse tree species that partner with either arbuscular mycorrhizal fungi or ectomycorrhizal fungi have distinct metabolisms that give rise to different leaf and soil chemical traits that impact C allocation in forests and the exchange of C between the biosphere and the atmosphere. Using a collection of mycorrhizal fungi with differing growth traits and forest arboretums in Europe containing diverse tree species that partner with different mycorrhizal fungi, we are measuring the thousands of biochemicals that they synthesise, to distinguish the metabolic differences between plants that partner with different mycorrhizal partners for the first time. We are now also measuring how the metabolism of the fungi and the plant differs when grown alone or in symbiosis and how this impacts the atmosphere using a combined CO18O and CO34S tracing approach. So far, we have discovered that from ~7000 metabolic compounds found in the trees, a particular class of metabolites called flavonoids can distinguish and predict whether a tree species has a preference to partner with arbuscular mycorrhizal fungi or ectomycorrhizal fungi for the first time. We are now using a similar approach in controlled microcosm studies to understand how the fungal partner responds metabolically and enzymatically to the process of mycorrhisation with trees and assessing how the fungi impact the atmospheric concentrations of CO18O, 13CO2 and COS.

Using a similar framework and diverse soils from across Europe, we are also studying how the metabolic features of soils can be linked to the presence of key fungal and bacterial community members and how collectively these community properties relate to measured differences in the exchange of COS and CO2, in addition to enzymatic activities. We have constructed a novel set of machine learning and mechanistic models that can be compared and used to predict how land use and soil property variations impact COS fluxes and soil community carbonic anhydrase activity. Our first results indicate pronounced differences in the metabolic composition of soils across European biomes for the first time and have also shown that some metabolic compounds and soil community members present across all the European soils are strong predictors of COS fluxes and enzyme activities. Our next steps will be to develop a scaling framework to map these features spatially across Europe and beyond.

Another important objective of this project involved developing a framework to trace the interaction of atmospheric COS with the biosphere developing a technique to measure the isotopic discrimination of sulphur isotopes (33S and 34S) in COS during gas exchange with plants and the hyphosphere. This would provide a novel tool to trace and quantify the interactions of COS molecules in the atmosphere with the biosphere, the oceans and human activities. This is a challenge as the concentration of COS in the atmosphere is very low and measuring the isotopic composition of such low concentrations can be difficult to detect with the available instruments. However, with collaborators in the Netherlands we have successfully developed a gas exchange approach to measure isotopic variations during plant gas exchange and we have successfully developed a novel mechanistic framework to describe the fractionation of 34S during COS exchange with leaves.
In the COSMYCA project we have already produced a number of key findings that go beyond the current state-of-the-art describing how the mycorrhizal association of trees can be detected from a set of metabolic and spectral markers that provide insights into differences in the metabolic pathways of trees that may have evolved in response to mycorrhizal colonisation. In addition, COSMYCA is developing a range of numerical and machine learning models that can predict the exchange of COS and CO2 between soils and the atmosphere with a range of predictors that can be easy to measure from soil samples reducing the need for extensive field gas exchange measurements at different sites and providing tools to map enzyme activities spatially for the first time, going beyond the state-of-the-art as this information is currently not available to the research community representing a key knowledge gap curtailing the use of COS and CO18O as independent constraints in large scale Land Surface Models. Finally, we have also developed a novel modelling framework to explain variations in the isotopic fractionation of 34S measured during plant gas exchange using a novel gas exchange approach, both results going beyond the state-of-the-art.
Future expected results in COSMYCA will come from new experiments that will manipulate different tree species growing with different mycorrhizal partners in different CO2 concentrations to explore how the plant and fungal metabolism, growth and gas exchange respond. Furthermore, we will use results from our different experiments to interpret changes in atmospheric COS at large scales and over time using a novel multi-tracer modelling approach. This will lead to new constrained estimates of changes in CO2 fluxes between the biosphere and atmosphere in the last century and provide novel insights on how different forest tree species will respond to changes in rising CO2 in the future.
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