Trophic Interactions of a Chitin-Degrading Microbiome of an Aerated Agricultural Soil

Chitin is the second most abundant polysaccharide after cellulose and is subject to rapid microbial turnover in the environment. Microbial degradation of chitin in soil substantially contributes to carbon cycling and release in terrestrial ecosystems. In aerated soil ecosystems, chitin occurs as a structural component in protists, arthropods, and fungi. Thereby, fungi represent the main source of chitin in such soils as fungi have cell walls with up to 25% chitin and account for up to 60-90% of the microbial biomass in aerated soils. Chitin degradation can theoretically occur via two major degradation pathways. It can be deacetylated to chitosan or can be hydrolyzed to N,N'-diacetylchitobiose and oligomers of N-acetylglucosamine by aerobic and anaerobic microorganisms. Which pathway of chitin hydrolysis is preferred by soil microbiomes was unknown prior to this thesis. Therefore, processes, metabolic responses and degradation products associated with chitin and chitosan hydrolysis were assessed. Chitin was immediately broken down by the tested microbiome, but chitosan only with a considerable time delay, which suggests that the microbiome is adjusted to chitin as a substrate, and the degradation of chitin probably likely does not take place via the deacetylation to chitosan. Another objective of this study was to study the trophic interactions and dynamics of members of a chitin-degrading microbiome and the influence of oxygen on the carbon flow from chitin degradation, as these topics are largely uninvestigated in aerated soils. Therefore, a time-resolved 16S rRNA stable isotope probing experiment was conducted to label and identify those members of a soil microbiome that are involved in the aerobic and anaerobic degradation of chitin. [13C]-chitin was largely mineralized within 20 days, and Cellvibrio, Massilia, and several Bacteroidetes families were identified as initial active chitin degraders under oxic conditions. Subsequently, Planctomycetes and Verrucomicrobia were labeled by assimilating carbon either directly from chitin or from the degradation of cell wall polysaccharides, biofilm-associated exopolysaccharides, and small metabolic byproducts of chitinolytic bacteria. Bacterial predators (e.g., Bdellovibrio and Bacteriovorax) were labeled and non-labeled micro-eukaryotic predators (Alveolata) increased in relative abundance towards the end of the incubation (70 days), indicating that chitin degraders were subject to predation. Under anoxic conditions, trophic interactions differed substantially compared to oxic conditions. Various fermentation types occurred along with iron respiration. While Acidobacteria and Chloroflexi were initially labeled, Firmicutes and uncultured Bacteroidetes were predominantly labeled, suggesting that the latter two bacterial groups were mainly responsible for the degradation of chitin, and also provided substrates for iron reducers. The collective data indicated (a) that hitherto unrecognized Bacteria were involved in the chitin-degrading food web of an agricultural soil, (b) that trophic interactions of the chitin-degrading microbial food web were substantially shaped by the oxygen availability, and (c) that predation was restricted to oxic conditions. The functional redundancy of the soil microbiome and the catabolic diversity likely enable continued biopolymer degradation independent of oxygen concentration. Furthermore, chitin was readily and nearly completely degraded, suggesting that chitin is not as recalcitrant as it is sometimes believed to be. Thus, ‘recalcitrance’ of chitin is relative, rather than absolute and a matter of accessibility to the soil microbiome that is collectively adapted to degrade ubiquitous and abundant naturally occurring structural polysaccharides like chitin and cellulose