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Microbial interactions with soil minerals – effects on extracellular enzyme activity and aggregation

Microorganisms interact with different soil components, such as varying substrates and soil minerals, to drive soil processes and functionality. They can be influenced by the environment, but they themselves can influence their environment by their activities, for example through the production of extracellular enzymes and extracellular polymeric substances (EPS). The formation and stability of aggregates as the backbone of the soil structure, for instance, are thought to be largely influenced by soil microorganisms, or vice versa. There remain, however, open questions as to whether and how microorganisms can influence soil aggregation. While microbes are influencing their environment their interaction with the soil minerals could also change their responses upon adsorption - affecting their influence on soil aggregation. Therefore, the overarching goal of this thesis was to investigate the effect of soil minerals, in particular clay content, on the composition and activity of soil microbial community, with a specific focus on enzyme activities and EPS. Finally, the microbial control of soil aggregation through the influence of substrate availability was explored.
In total, two adsorption experiments and two incubation experiments were conducted using soils manipulated experimentally with increasing clay content. The sandy soil was amended with different amounts of soil minerals (i.e. montmorillonite) to achieve a gradient in clay content. For the first incubation experiment, organic substrates differing in decomposability (i.e., starch and cellulose) were added to the soil to stimulate microbial activities and incubated for 80 days. Soil samples from the first incubation experiment were analysed after 0, 3, 10, 20, 40 and 80 days for enzyme activities, microbial community composition, biomass C, EPS-protein and polysaccharide. Additionally, the geometric mean diameter and mean weight diameter of the soil aggregates were determined as measures of aggregate formation and stability, respectively. The first adsorption experiment examined the effect of soil mineral phases on the activities of extracellular enzymes using commercially available extracellular enzymes (α-glucosidase) added to the soil. The second adsorption and incubation experiment investigated the persistence of extracellular enzyme activities (commercially available α-amylase and cellulase) affected by soil minerals. For further insight into how other soil minerals affect extracellular enzymes, kaolinite and goethite in addition to montmorillonite were included in the second adsorption and incubation experiment. The prepared complexes (enzyme + soil and/or soil minerals) from the second adsorption experiment were incubated for 100 days. Further analytical methods include the determination of enzyme activities, microbial biomass C, extraction and quantification of the soil EPS, protein analyses, DNA isolation, DGGE, qPCR and Illumina sequencing.
The adsorption experiment showed that extracellular enzyme activities decreased with increasing clay contents. In contrast, such an inhibitory effect on microbial enzyme activity was only observed directly in the incubation experiment after the stimulation of in-situ microorganisms for extracellular enzyme production through substrate addition. Higher extracellular enzyme activities at later incubation days in soils with high clay content suggested an adaptation of the microbial community in response to soil clay content and/ or persistence of extracellular enzymes by adsorption to mineral surfaces. However, the second adsorption experiment showed that the high specific activity and persistence of the enzymes were constrained by the availability of sorption sites. It is therefore reasonable to assume that soil mineral phases support microorganisms in less-sorptive environments by sparing energy on enzyme production, since even a small enzyme release could already propel sufficient activities to degrade target carbon substrates. Starch amendment accelerated respiration and microbial biomass much more than cellulose. While microbial community differed depending on the C substrate (starch or cellulose) added, clay addition had a stronger influence on alpha diversity than substrate addition. Although the production of EPS-protein was closely linked to the provision of additional substrates, the addition of clay minerals resulted in more EPS production than when no additional clay was present. By correlating soil aggregation (stability and formation) with the recorded microbial parameters (that is biomass C, EPS-protein and EPS-polysaccharide), both EPS-protein and EPS-polysaccharide exhibited a significant control on aggregate formation and microbial processes, though, surprisingly, more strongly with high clay content. It was observed that EPS is only a transient compound, which initiates aggregate formation, but clay content plays a more significant role in long-term aggregate stabilization.
Overall, this thesis contributed to our knowledge about the interaction of microorganisms with the soil mineral phase and their influence on soil structural stability. The findings established that soil minerals shape the composition and activity of microbial communities. In turn, the microbial production of EPS seems to be more significant for aggregate formation than stability. The results on the effect of soil minerals on extracellular activities provided a paradigm that the persistence of enzyme activities by adsorption does not always hold. Producing EPS might contribute to microbial adaptation that mitigates the negative effect of adsorption on extracellular enzymes. It might also be probable that the EPS become a substance of degradation for the extracellular enzymes. Overall, the results indicated that in clay-rich soils the process leading to extracellular enzyme persistence can be stochastic, depending on multiple factors including sorption sites and substrate availability. Labile organic C clearly plays a role in aggregate formation by supporting EPS production. However, increasing clay content enhanced aggregate stability, promoted the development of distinct microbial communities and increased EPS production. The discrepancy so observed in the contribution of the two EPS parameters, EPS polysaccharide and protein, on soil aggregation points to the need for inclusion of different EPS compositions in future studies relating to soil aggregation.

Identiferoai:union.ndltd.org:DRESDEN/oai:qucosa:de:qucosa:81858
Date26 October 2022
CreatorsOlagoke, Folasade Kemi
ContributorsKalbitz, Karsten, Vogel, Cordula, Poll, Christian, Nannipieri, Paolo, Technische Universität Dresden
Source SetsHochschulschriftenserver (HSSS) der SLUB Dresden
LanguageEnglish
Detected LanguageEnglish
Typeinfo:eu-repo/semantics/publishedVersion, doc-type:doctoralThesis, info:eu-repo/semantics/doctoralThesis, doc-type:Text
Rightsinfo:eu-repo/semantics/openAccess

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