Impact of hypertonic osmotic stress on bacterial cell physicochemical properties and the consequences for soil wetting properties

  • The wettability of soil particles defines important soil processes such as water infiltration in the soil and sorption of various substances on mineral surfaces. Soil water repellency (SWR) significantly impacts soil-water dynamics, often leading to reduced growth rates and crop yields. This phenomenon arises from hydrophobic coatings formed on soil particles by non-living organic compounds such as waxes, alkanes, fatty acids, free lipids and amphiphilic molecules. While previous research on soil microorganisms mainly focused on their degradation activities, recent findings indicate a neglected aspect: the direct involvement of these microorganisms in hydrophobic interactions with soil particles modifying soil wettability. Specifically, it was found that the coverage of mineral particles by Gram-negative soil bacteria is associated with high water repellency of the produced cell-mineral association. Moreover, bacterial adaptation to drought stress increases cell surface hydrophobicity, suggesting a potential intensification of microbial induced SWR under changing environmental conditions. However, the mechanism, extent, and persistence of SWR caused by bacteria are poorly understood. The aim of this work is thus to understand how a hypothesized increase of bacterial surface hydrophobicity, as an adaptation strategy to stress, affects cell adsorption onto mineral surfaces. My results are linked to scientific findings about cell growth processes under variations in soil moisture to estimate the short and long-term consequences of the drought stress on soil wetting properties. Key information at the single-cell level including cell size, stiffness, roughness and adhesion, obtained by improved atomic force microscopy (AFM) techniques, were linked to the stress induced changes of the bacterial surface hydrophobicity and surface composition obtained by contact angle and X-ray photoelectron spectroscopy (XPS) analyses, respectively. In addition, for the first time, a new AFM approach was developed to perform direct cell-mineral adhesion measurements taking the effect of contact area of these irregular materials into account. This helped to understand how cell growth environment and mineral type affect adhesion. The findings of this study provide valuable contributions to both environmental sciences and biology by enhancing our understanding of soil-water dynamics. This knowledge helps to understand how the response of the ecosystem to environmental stress affects biological activities. In addition, it contributes to a broader understanding of soil processes such as the transport of fluids and the sorption of organic molecules and microorganisms on minerals surfaces. The results showed that stressed cells exhibit smaller size, higher stiffness and elevated protein content relative to unstressed cells. In addition, stress increases the contact angle in many strains, which indicates enhanced hydrophobicity due to the changes of the cell envelope structure. Such structural changes at the cell envelope also resulted to higher single-cell adhesion to hydrophobic than hydrophilic nanosurfaces (AFM tips) for stressed cells compared to unstressed cells. It is discussed that cell shrinkage induces protein crowding in the lipid bilayer while potentially releasing lipopolysaccharides (LPS) and lipids as membrane vesicles (MVs). The higher protein content increases the number of hydrophobic nanodomains per surface area, which enhances hydrophobic interactions and reduces affinity towards aqueous solution. Considering that by stress the ability of water to spread on cell surfaces becomes weaker, it is addressed that, during drought conditions, cells tend to minimize exposure to the stressful medium (aqueous solution). This is confirmed by increased adhesion pressure of montmorillonite and goethite versus stressed compared to unstressed cells due to increased hydrophobic interactions. In other words, the cells shield themselves from the stressful medium by adsorption to the mineral phase. The role of hydrophobic interactions is evident by the absence of stress induced increase of adhesion pressure towards quartz. Hence, quartz with high hydrophilicity consistently exhibits surface wetting during separation from the cell surface regardless of cell condition. Nevertheless, the unexpected weaker adhesion pressure towards kaolinite under stress could not only be described by its wetting characteristics. The interfacial properties of this mineral are highly affected by the specific surface (basal, edge or both planes) interacting with the cell surface as discussed in the thesis. Based on my findings and other research, a comprehensive model that elucidates bacterial behavior and function throughout a drying-rewetting cycle is introduced. In conclusion, a microbial induced soil hydrophobizing effect is suggested, albeit its persistence appears to be sensitive to drought periods, showing only transient impacts among frequent shifts in moisture content. Furthermore, the observed increase in cell surface hydrophobicity plays a critical role in enhancing bacterial survival, fostering dynamic “beneficial” interactions within the soil which maintain plant productivity under stress conditions. Nonetheless, extended periods of severe dehydration, surpassing seasonal fluctuations, could lead to the cumulation of hydrophobic materials in the soil matrix upon cell decay, which could feedback into persistent hydrophobizing effect. This emphasizes the importance of understanding the balance between the dynamics of soil microbes and the prolonged environmental stressors for sustaining soil health and productivity.

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Author:Abd Alaziz Abu Quba
URN:urn:nbn:de:hbz:386-kluedo-85085
DOI:https://doi.org/10.26204/KLUEDO/8508
Referee:Gabriele E. Schaumann, Doerte Diehl
Advisor:Doerte Diehl
Document Type:Doctoral Thesis
Cumulative document:Yes
Language of publication:English
Date of Publication (online):2024/11/25
Date of first Publication:2024/11/29
Publishing Institution:Rheinland-Pfälzische Technische Universität Kaiserslautern-Landau
Granting Institution:Rheinland-Pfälzische Technische Universität Kaiserslautern-Landau
Acceptance Date of the Thesis:2024/11/15
Date of the Publication (Server):2024/11/29
Tag:Chemische Kraftmikroskopie; Extrazelluläre polymere Substanzen; Osmotischer Schock; Röntgenphotoelektronenspektroskopie
Atomic force microscopy (AFM); Bacteria; Cell-mineral association; Chemical force microscopy (CFM); Contact angle; Droughts; Environmental scanning electron microscope (ESEM); Extracellular polymeric substances; Force spectroscopy; Hydrophobicity; Hypertonic osmotic stress; Minerals; Pseudomonas fluorescens; Soil water repellency (SWR); X-ray photoelectron spectroscopy (XPS)
GND Keyword:BakterienGND; MineralGND; HydrophobieGND; RasterkraftmikroskopGND; Pseudomonas fluorescensGND; RandwinkelGND; DürreGND
Page Number:110, 5 Seiten
Faculties / Organisational entities:Landau - Fachbereich Natur- und Umweltwissenschaften
DDC-Cassification:5 Naturwissenschaften und Mathematik / 500 Naturwissenschaften
MSC-Classification (mathematics):92-XX BIOLOGY AND OTHER NATURAL SCIENCES
Licence (German):Creative Commons 4.0 - Namensnennung (CC BY 4.0)