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«LINKING DIFFUSIONAL HETEROGENEITY AND AQUATIC HABITAT FRAGMENTATION WITH MICROBIAL COEXISTENCE AND DIVERSITY IN THE VADOSE ZONE A dissertation ...»

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DISS. ETH NO. 20455

LINKING DIFFUSIONAL HETEROGENEITY AND AQUATIC HABITAT FRAGMENTATION WITH

MICROBIAL COEXISTENCE AND DIVERSITY IN THE VADOSE ZONE

A dissertation submitted to

ETH ZURICH

for the degree of

Doctor of Sciences

presented by

GANG WANG

MSc in Applied Chemistry, University of Science & Technology of China, China born March 29, 1979 citizen of China accepted on the recommendation of Prof. Dr. Dani Or, examiner Prof. Dr. Hauke Harms, co-examiner Prof. Dr. Martin Ackermann, co-examiner … to my family

ACKNOWLEDGEMENT

There have been so many people helping me during my PhD study! I would now take the opportunity to send my everlasting feeling of gratefulness and thankfulness to all of you. These will be no chance for me to finish my PhD study without your persistent and most kindly help!

It is difficult to overstate my gratitude to my PhD supervisor, Prof. Dr. Dani Or. With his brilliant mind, his inspiration, and his great efforts to explain things clearly and simply, he has helped to make physics and little animals fun for me. Throughout my PhD study time, I would have been lost without his enthusiasm, encouragements, good teaching, and many excellent ideas and advice.

I also would like to thank Prof. Martin Ackermann, the co-examiner of my PhD study. I always enjoyed the fruitful discussions with Martin and his group scientist Dr. Johnson David.

My gratitude also goes to co-examiner of my PhD study, Prof. Hauke Harms. I would like to thank him for many last minute proof document sessions on various occasions. I would also like to thank Prof. Barth Smets, Dr. Arnaud Dechesne and Dr. Ganz Gülez, my research partners from the Technical University of Denmark (DTU), for their assistance and productive collaboration. Thanks also go to Prof. Martin Schroth and his research members, Dr. Ruth Henneberger, and Mr. Fabio Ugolini, for their kindly assistance in soil bacteria visualization experiments.

Especially I would like to thank Mr. Daniel Breitenstein and Mr. Hans Wunderli, the great technicians, together with whom we have made interesting laboratory experiments. I would also like to send my gratitude to Mr. Gernot Michlmayr, who is not only sharing the office room with me throughout the last four years, but also a good friend for all sorts of discussions. Spatial thank is due to Ms Christina Häfliger, who is not only my friend, but excellent sources of administrative assistance and many other helps. I would thank my colleagues and fellow PhD students at LASEP (EPF Lausanne) and STEP (ETH Zurich) for providing friendly studying environment and participating in stimulating group exercises developing solutions to all kinds of problems in a wide range of interests. Spatially, I would like to thank Dr. Peter Lehmann and Dr. Stanislaus Schymanski for many fruitful discussions, and also thank Ms Franziska Möbius and Mr. Jonas von Rütte for their numerous kindly assistance for scientific and also for daily problems. Thank is also due to Dr. Yan Jin, from whom I had received many interesting stories about colloids dynamics sometime behaviors similar with my little animals. Spatial thank also goes to Mr. Fabian Rüdy for his nice graphics distributed throughout the chapters.

I enjoyed my PhD experience that has been extensively interesting, and I would like to express my spatial gratitude to Dr. Papritz Andreas, with whom we have shared many excursion experiences from Swiss mountains and forest.

I wish to gratefully thank my entire extended family for providing a loving environment for me.

Lastly, I wish to thank my parents, they bore me, raised me, taught me, and love me; thank my parents-in-law, who constantly support me and love me; and most importantly, I wish to thank my wife, Guowei Chen and my son, Yizhou Wang, together with whom we have now the most lovely family. To them I dedicate this thesis.

–  –  –

Abstract

ZUSAMMENFASSUNG

Chapter 1 General Introduction

1.1 Microbial diversity and function in soil

1.2 Modeling hydro-physical microbial interactions in soil

1.3 Ecological challenges for microbial function in unsaturated soil

1.3.1 Hydration functions, microbial motility and dispersal on rough surfaces

1.3.2 Hydration fluctuations, microbial growth and species coexistence on rough surfaces 3 1.3.3 Linking soil biodiversity with environmental variables, a biophysical metric.............. 4 1.3.4 Trophic interactions, microbial diversity and ecological functions on rough surfaces 4 References

Chapter 2 Hydration Controlled Bacterial Motility and Dispersal on Surfaces

2.1 Introduction

2.2 Materials and Methods

2.2.1 Bacterial strains

2.2.2 Experiments on the Porous Surface Model

2.2.3 Modeling bacterial motility and growth on rough surfaces

2.3 Results and Discussion

2.3.1 Bacterial motility on rough surface – experimental observations

2.3.2 Simulation models of bacterial motility on rough surfaces

2.3.3 Conclusions and implications





Acknowledgments

References

–  –  –

Chapter 3 Aqueous Films Limit Bacterial Cell Motility and Colony Expansion on Partially Saturated Rough Surfaces

3.1 Introduction

3.2 Theoretical Considerations

3.2.1 Model of heterogeneous rough surface

3.2 2 Water configuration on surface roughness network

3.2.3 Bacterial motility on partially-saturated rough surface

3.2.4 Bacterial growth on partially-saturated rough surface

3.2.5 Linking bacterial colony expansion rates with cell motility

3.3 Results and Discussion

3.3.1 Bacterial cell motility on partially-saturated surface roughness network.................. 41 3.3.2 Bacterial growth on partially-saturated surface roughness network

3.3.3 Bacterial colony expansion rates on rough surfaces

3.4 Conclusions

Acknowledgements

References

Appendix S1: Capillary pinning force acting on a bacterial cell

Appendix S2: Growth kinetics of individual bacterial cell

Appendix S3: Bacterial motility on partially-saturated rough surface

Chapter 4 Hydration Dynamics Promote Bacterial Coexistence on Rough Surfaces

4.1 Introduction

4.2 Materials and Methods

4.2.1 Modeling heterogeneous rough surface and water configuration

4.2 2 Nutrient diffusion and bacterial motility on partially hydrated rough surfaces.......... 65

–  –  –

4.3 Results

4.3.1 BMicrobacterial growth and competition on rough surfaces under static hydration conditions

4.3.2 Effects of hydration dynamics on microbial growth and species coexistence............. 70

4.4 Discussion

Acknowledgements

References

Chapter 5 A Hydration-Based Biophysical Index for the Onset of Soil Microbial Coexistence........... 81

5.1 Introduction

5.2 Methods

5.2.1 Aqueous-phase configuration on rough surface and analytical prediction................. 84 5.2.2 Analytical solutions of nutrient diffusivity on rough surfaces

5.2.3 Microbial motility and generation length inhabiting unsaturated rough surfaces...... 85 5.2.4 The definition of predictive microbial coexistence index

5.3 Results

5.4 Discussion

Acknowledgements

References

Supplementary information

Chapter 6 Trophic Interactions and Self-organization of Microbial Consortia on Unsaturated Surfaces

6.1 Introduction

6.2 Methods

6.2.1 Modeling microbial growth on rough surfaces

–  –  –

6.3 Results and Discussion

6.3.1 Microbial dynamics and self-organizations of trophically-interacting consortia..... 109 6.3.2 Hydration and spatial heterogeneity and nutrient concentrations affecting selforganization dynamics

6.3.3 Microbial dynamics and self-organizations with multitrophic interactions.............. 112

6.4 Summary and Conclusions

Acknowledgements

References

Chapter 7 Summary and Outlook

7.1 Summary

7.2 Outlook

Curriculum Vitae

–  –  –

Notwithstanding the inhospitable and nutrient poor environment and the vagaries of ambient and hydration conditions, soil is the most biologically active compartment of the biosphere, hosting unparalleled biodiversity at all scales. Present understanding of soil as a complex and dynamic habitat for microbial life is sketchy and often suffers from misconceptions regarding what constitutes favourable or unfavourable environments. Consequently, understanding of the original patterns of soil microbial diversity represents an immense and uncharted scientific frontier. Progress in resolving mechanisms that promote the unparalleled soil biodiversity and sustain the immense soil ecosystem functions requires transformation of heuristic ecological concepts into process-based models that consider dynamic biophysical interactions at appropriate spatial and temporal scales.

We developed a hybrid modeling framework that couples individual-based modeling approach with diffusion-consumption elements for microbial growth and nutrient consumption, and trophic interactions at individual cell scale on rough surfaces. The model resolves spatial and temporal nutrients diffusion fields defined by boundary conditions, surface geometry features and by local nutrients interceptions by individual cells, and explicitly tracks motions and life histories of individual cells considering primary hydrodynamic and capillary constraints to motility. It enables systematic estimating the effects of hydration status and surface geometrical properties on bacterial cell motility and impacts on surface-attached bacterial colony growth and expansion, and the influence of variable hydration conditions on microbial population interactions and community dynamics on partially hydrated rough surfaces, as well as the effects of trophic interactions on shaping microbial population dynamics and community structure, and their impacts on microbial ecological functioning in unsaturated soils.

Combined experimental observation with simulation models, we have demonstrated that hydration-induced aqueous phase configuration coupling surface geometry properties impose significant physical constraints (cell-wall hydrodynamic and capillary forces) upon microbial cell motility on partially-hydrated rough surfaces, and couples nutrient diffusion limitations, control microbial growth and colony development. The results defined a surprisingly narrow range of hydration conditions (within a few kPa of matric potential value) where motility confers ecological advantage upon microbial life on natural surfaces (seeing chapters 2 and 3).

The rapid fragmentation of soil aqueous phase under most natural conditions suppresses microbial growth and cell dispersion thereby balances conditions experienced by competing populations. Additionally, hydration fluctuations intensify localized interactions that lead to V promotion of coexistence by affecting disproportionally densely populated regions during dry periods thereby affecting microbial population dynamics far beyond responses predicted from equivalent stationary hydration values (chapter 4). Based on the knowledge gained from the systematic study of microbial dynamics inhabiting unsaturated rough surfaces, we have successfully developed a novel biophysically-based metric capable for predicting the onset of microbial species coexistence and diversity in soils based on solely quantifiable biophysical variables. The model predicted a surprisingly narrow range of hydration conditions that mark a sharp transition from suppression to promotion of microbial diversity irrespective of soil type or details of surface roughness geometry for the onset of microbial coexistence consistent with limited experimental results and with individual-based simulation models (chapter 5).

Simulation models of microbial trophic interactions revealed that trophic interactions among multiple species may increase ecological niche dimensionality through spatial self-organization of microbial consortium. Spatial organization is strongly influenced by the geometry of primary nutrient fluxes and by the nature and rate of release of byproducts essential for other members in the consortium. Not surprisingly, hydration conditions and spatial heterogeneity impose diffusion constraints and motility limitations that influence levels and rates of self-organization.

Concentration gradients and inhibitory functions of various substrates relative to species growth rates and tolerance levels are clearly manifested in the emerging spatial patterns of consortia (chapter 6).

The study lay at the intersection of environmental microbiology, vadose zone hydrology, and soil physics. The quantitative estimates offered a potential for improved understanding of microbiological interactions in the most active compartment of the biosphere, and it has broad impact in cutting across disciplinary boundaries and in offering new insights into long standing environmental questions that are critical to soil and water resources quality, the fate of biogenic and anthropogenic contaminants, and global biogeochemical cycles, specifically, shedding lights into the origins of the unparallel soil biodiversity maintenance. The proposed framework would offer instrumental tool in guiding future experiments and data collection.

VI ZUSAMMENFASSUNG



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