Prokaryotic colonization of soil during early-stage aggregation and of soil microaggregates

Abstract

Soil is a complex mixture of minerals, gas, water and organic materials that assemble into aggregates and define pore spaces, therewith providing connective and isolated habitats for microorganisms. The soil microorganisms drive the biogeochemical cycling in terrestrial ecosystems and are likewise involved in soil aggregation. However, due to the complexity and heterogeneity of soil aggregates, the colonization patterns of prokaryotic cells during soil aggregation and in soil aggregates are not fully understood. Therefore, in this thesis, I studied 1) the prokaryotic communities that establish after the early-stage of soil aggregation dependent on different organic matter (OM) types and soil textures and their potential role during soil aggregation; 2) whether prokaryotic cells can be found inside soil microaggregates (MAs) and if so, whether specific prokaryotic taxa prefer to locate within MAs; 3) whether different fractions of soil MAs have an effect on the prokaryotic community and 4) whether some specific taxa of dead prokaryotic cells accumulate in particular with soil MAs.<br /> To investigate the prokaryotic colonization patterns during early-stage aggregation, I firstly analyzed the prokaryotic community abundance and structure in an artificial soil incubation experiment with three soil textures and three types of OM, including bacterial necromass and two sizes of particulate OM. OM types exerted a stronger effect on the bacterial community structure and abundance than texture. The bacterial necromass supported the most distinct bacterial community with the highest abundance and lowest diversity, as well as the most intense formation of water-stable MAs in comparison to the particulate OM originated from plant debris. Most of the abundant prokaryotic taxa in all samples are known to be extracellular polymeric substances (EPS) producers, indicating that functional redundancy warrants aggregation by gluing agents despite community compositional differences. An investigation of the bacterial cell distribution in cross-sectioned soil microaggregates was performed by epi-fluorescence microscopy, confirming the existence of bacterial cells and even some micro-colonies inside of MAs. Based on the analysis of MAs obtained from soils of a pedosequence, differences were found in the prokaryotic colonization of the total MAs compared to the MA interior. More than 50% and often more than 80% of the prokaryotic cells colonized the surface of soil MAs. Further, the prokaryotic community abundance and alpha diversity were mainly determined by MA size fractions, whereas the prokaryotic community composition was mostly affected by the location of MAs in relation to macroaggregates, i.e. as separate units (free) or occluded within macroaggregates. The variation in prokaryotic community composition within MAs, as well as across different fractions of MAs, suggests that differences in prokaryotic colonization patterns result from varying aeration, OM types and accessibility in different micro-habitats. Different hyphae forming taxa were detected among the MA associated prokaryotic taxa, especially in those occluded within macroaggregates or on the surface of MAs, which suggests their contribution to aggregate stability by hyphal enmeshment. The enriched taxa in the specifically analyzed extracellular DNA fraction are known for bio-weathering activities, which might have played a role at the early stages of pedogenesis, whereas the more prominent taxa in the intracellular DNA fraction indicated a higher prevalence of cells crucial for governing biochemical cycles.<br /> In synthesis, my results show that soil OM, texture, MA size and MA location in soil as free or occluded units, as well as the specific spatial distribution of cells within and on MAs contribute to the diversification of prokaryotic colonization in soils. In this context, soil prokaryotes not only benefit from the diverse microhabitats provided by MAs, but are also very likely involved in aggregation processes at the MA scale via the production of EPS or hyphal entanglement. This underlines the fundamental importance of prokaryotic communities and their role at the MA scale.