Prokaryote growth factor cross-feeding as a driver of soil biodiversity and ecosystem processes.

• Applicant: Damien Finn, Ph.D.
• Subject Area: Soil Sciences ; Bioinformatics and Theoretical Biology
• Term: since 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 522758166

Soil microbial biodiversity is associated with a number of beneficial ecosystem processes, e.g. plant productivity, biogeochemical cycling of macro-elements and resistance to perturbation. Therefore, the ecological and evolutionary mechanisms that increase biodiversity are worth consideration. Previous research has focused on niche differentiation and competitive exclusion (ecological factors) and spatial heterogeneity (environmental factors). In contrast, a role for auxotrophy arising from gene-loss events of essential growth factors (evolutionary factors) has been overlooked. Over evolutionary timescales, selection favours Prokaryotes that undergo gene-loss events as this reduces the burden of investing protein synthesis and energy into general cell maintenance. Gene-loss occurs despite the potential for taxa to be locked into obligate cross-feeding interactions with other Prokaryotes or Eukaryote hosts, e.g. plant rhizosphere. It is possible for mutualistic interactions to develop, whereby two auxotrophs provide complementary growth factors to each other as the ‘Division of Labour Hypothesis’, or commensal interactions where one taxon adopts the burden of producing essential growth factors for auxotrophs as the ‘Black Queen Hypothesis’. We predict that, not only do such interactions promote biodiversity by establishing the need for co-existence, but that auxotrophic taxa alternatively invest protein synthesis and energy into performing beneficial ecosystem processes. With a metagenomics approach that considers Prokaryotes at both community and individual (i.e. genome) scales, this project will investigate how auxotrophy-dependent cross-feeding interactions support soil biodiversity and ecosystem processes. This will be tracked over time in an agricultural soil undergoing winter wheat cropping at: 1) fallow period; 2) tillering, 3) stem elongation and 4) ripening stages, and 5) reinstitution of fallow. Genetic potential will be linked to growth via substrate-induced calorimetry and respiration of soil communities that stimulate either prototrophs or auxotrophs. This experimental design will specifically: 1) identify general assembly patterns between proto- and auxotrophs at the community scale, including functional genes associated with ecosystem processes; 2) assess the importance of plant rhizosphere in altering Prokaryote-dependent interactions, and how this affects the composition of functional genes; and 3) determine if cross-feeding interactions fit the Division of Labour or Black Queen Hypothesis, and confirm that auxotrophs are more likely to invest in functional genes that drive ecosystem processes rather than general cell maintenance. These outcomes will improve our fundamental understanding of the factors that promote biodiversity in soil microbial communities, while also investigating how gene-loss events within individual taxa ultimately have consequences for processes such as plant productivity and biogeochemical cycling.

• DFG Programme: Research Grants