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Self-organisation of microbial soil organic matter turnover

Periodic Reporting for period 2 - SomSOM (Self-organisation of microbial soil organic matter turnover)

Período documentado: 2020-11-01 hasta 2022-04-30

Soil microbes mediate the largest flux of carbon (C) from land to the atmosphere by breaking down and respiring plant-derived organic matter as CO2. In addition, soil microbes also contribute to the stabilization of C in the soil by transforming plant-derived organic C into better protected microbial residues and products. This drove, over thousands of years, the buildup of the huge present stock of soil organic C which, on a global scale, exceeds the amount of C in the atmosphere and all vegetation combined. Despite the known importance of soil microbes for global C cycling, however, the underlying mechanisms of microbial turnover and buildup of soil organic matter are still not fully understood.

One reason for this is that microbial activities happen at microbial scales, which are by their nature difficult to investigate. In soil, various individual microbes interact with each other within um-sized soil pores and on the surface of soil aggregates (mm-sized conglomerates of soil minerals, organic matter and microbes) in a physically and chemically heterogenous micro-environment. This makes the soil microbial ecosystem a prime example of a complex system. It is known that complex systems exhibit ‘self-organisation’, which means that a system behavior of a new quality is emerging from interactions among individual parts of the system. The key question of our project is if and how such phenomena influence soil C cycling, or in other words “Does self-organization of microbial decomposers affect organic matter turnover in soil?”. We aim to address this question by shifting the perspective for investigating the mechanisms of microbial soil organic matter turnover from traditional soil science to complex systems science.
In the first phase of the project we laid the foundations to investigate microbial self-organisation at several spatial scales. First, we established protocols that allow us to visualize the spatial arrangement of selected strains of soil microbes that jointly degrade substrate particles, made of cellulose or chitin (two polymers that are naturally occurring in soils). In parallel, we simulated this system with an individual-based computer model, with the aim to explore the mechanisms of spatial self-organisation during the decomposition process. Moreover, we used a mathematical model to explore synergies among microbes with different abilities to decompose polymeric substrate, and how they affect the overall degradation process. In a later experiment, we added substrate particles to soil, which allowed us to identify natural consortia of microbial decomposers from soil.

On the next level of complexity, we explored co-occurrences of microbes at the scale of small (mm-sized) soil aggregates. For this we measured the composition of microbial communities (who is there), as well as the chemical composition (what is the aggregate made of) of a large number of individual, 1-2 mm sized soil aggregates sampled from a forest soil. We use microbial network analysis to link microbial community composition to soil organic matter chemistry at that small scale, which will allow us to get a better understanding on potential functional consortia of microbes that have evolved within an aggregate to degrade certain organic compounds. Towards that goal, we evaluated various algorithms for network construction that are commonly applied to soil microbial datasets and showed how they may affect ecological conclusions (Guseva et al, Soil Biology and Biochemistry, 2022, https://doi.org/10.1016/j.soilbio.2022.108604 preprint: https://doi.org/10.1101/2021.12.14.472586). We also explored whether mycorrhizal fungi (a widespread and important symbiosis partner for plants) and other fungi that colonize root tips of young Beech trees shape the bacterial and archeal communities around them. Further, we explored the spatial organization of root-associated fungi across a forest site, which revealed that mycorrhizal fungi follow different patterns of spatial distribution across the forest floor compared to other types of soil fungi.

Relating to a larger spatial scale, I discuss the concept that emergent behavior of the soil microbial ecosystem may act as potential driver of soil organic matter turnover, in a Perspectives Paper which has resulted from a workshop on modelling soil organic matter turnover (Lehmann et al, Nature Geoscience, 2020, https://doi.org/10.1038/s41561-020-0612-3)
We gained interesting first results from applying network analysis at the mm-scale in the soil. We will continue this direction to get deeper insights into the fine-scale organization of the soil microbiome.
In the second phase of the project we plan to extend our work investigating synergies and interactions among soil microbial decomposers at the microscale by implementing a ‘decomposer chip’ using microfluidics. Microfluidics is a promising novel technique in soil microbial ecology which allows to create artificial, controllable and observable environments for microbes. By linking such a ‘decomposer chip’ to our individual-based computer model we expect deeper insights into potential mechanisms of spatial self-organisation of microbial consortia collectively degrading a complex substrate.
In addition, we will apply the framework of complex systems science to soil microbial ecology in a series of experiments that are currently being developed.
Microscopic visualisation of different bacterial strains colonizing chitin-containing substrate bead