Microbial life in porous systems

Microbial life in porous systems dominates the functioning of numerous ecosystems, ranging from stream sediments to soils. While these environments are characterized by structures that vary spatially over orders of magnitude, the traditional research focus has been on their macroscopic properties, such as porosity, permeability or pore connectivity. These approaches are effective in providing an overall description of the environment, but, they do not capture the impact of the spatial heterogeneity that is experienced by microorganisms. Such heterogeneity is assumed to play a major role on soil and sedimentary ecosystem functions, as well as being a driving force for selection and maintenance of microbial diversity. In order to cope with this heterogeneity microorganisms harness an arsenal of mechanisms to adapt to the prevailing conditions. They range from regulation of cell motility to modification of cell and colony morphology, production of matrix components, or generation of genetic and physiological heterogeneity. The present thesis focuses on the role of pore spatial heterogeneity and transport dynamics on microbial life in porous systems. The relevance of this thesis lies in the fact that it couples pore and near-cell scale physical mechanisms to the microbial processes at the larger landscape-scale. This multi-scale approach, obtained exploiting microfluidic experiments and time-lapse microscopy allowed me to investigate dispersal and space exploitation of microorganisms in porous systems. By means of a novel stochastic model, I combine measured pore scale trajectories of individual cells to the overall landscape transport. I show that motile cells of Pseudomonas putida disperse more efficiently, than non-motile cells, through a heterogeneous porous system. Motile cells can evade flow-imposed trajectories, enabling them to explore larger pore areas than non-motile cells. Additionally, motile cells are capable of reorienting their body towards flow direction, so increasing the population velocity and significantly impacting the overall transport properties. In case of a resident biofilm throughout the porous system, microbial transport exhibited preferential flow paths, and higher attachment rate. These two effects were more pronounced for non-motile than for motile cells. These findings suggest that motility couples with heterogeneous flows and that it can be beneficial to bacterial cells in confined environments as it enables them to actively explore space for resources or evade from regions with unfavorable conditions. In a second set of experiments, I studied the growth of a multispecies bacterial community in a porous system. Biofilms consistently differentiated into an annular base biofilm coating the grains and streamers protruding into the pore space. Different biophysical processes ruled this differentiation. While streamer growth dynamics is well explained by a filtration model, base biofilm expanded its radial growth by producing a tortuous surface, which enhances mass transfer. This architectural plasticity allowed the complementary use of the space provided by the grain-pore complexes, enhancing space exploitation at the larger scale of the porous system. Collectively, these findings unravel the biophysical underpinnings to the success of multispecies biofilms in porous environments.

Theoretical and Experimental Studies of Dendritic Metacommunities

Francesco Carrara

The present thesis deals with the understanding of the origins and the mechanisms of maintenance of biodiversity in natural landscapes, in particular by identifying key processes that define large-scale patterns of abundance and diversity. Biological communities often occur in spatially structured habitats where connectivity directly affects dispersal and metacommunity processes. Recent theoretical work suggests that dispersal constrained by the connectivity of specific habitat structures affects diversity patterns and species interactions. This is particularly relevant in dendritic networks epitomized by fluvial ecological corridors. This thesis addresses whether connectivity alone can explain observed features of biodiversity and selectively promote different components of community composition in river-like landscapes, such as local species richness or the among-community similarity. The relevance of this thesis lies in the major ecological challenges posed by the topic, and its fundamental importance to conservation biology. The studies pursued herein are also deemed relevant because of the influence of the spatial connectivity and dispersal on population dynamics and of the relevance of biodiversity to ecosystem functioning. Mechanisms of species coexistence were investigated with a blend of theoretical tools (broadly related to statistical mechanics and the theory of stochastic processes) and experimental work using laboratory microbial communities. The research tools ranged from aspects of modern coexistence theory in a local perspective to the recent concept of the metacommunity in spatial ecology, within a unified framework. The study of biodiversity in riverine ecosystems guided by observational data has been addressed by combining theoretical metacommunity models with laboratory experiments. The results are diverse. First, they show experimentally that connectivity per se shapes key components of biodiversity in metacommunities. Local dispersal in isotropic lattice landscapes homogenizes local species richness and leads to pronounced spatial persistence. By contrast, dispersal along dendritic landscapes leads to higher variability in local diversity and among-community composition. Although headwaters exhibit relatively lower species richness, they are crucial for the maintenance of regional biodiversity. By suitably arranging patch sizes within river-like networks the effect of local habitat capacity (i.e., the patch size) and dendritic connectivity on biodiversity can be experimentally disentangled in aquatic microcosm metacommunities. It is shown in this thesis that species coexistence and community assembly depend on intricate, non-trivial interactions of local community capacity and network positioning. Furthermore, an interaction of spatial arrangement of habitat capacity and dispersal along river-like networks also affects a key ecosystem descriptor, namely regional evenness. High regional evenness in community composition is found only in landscapes preserving geomorphological scaling properties of patch sizes. In riverine environments some of the rarer species sustained regionally more abundant populations and were better able to track their own niche requirements compared to landscapes with homogeneous patch size or landscapes with spatially uncorrelated patch size. All the experimental results were supported and extended by a theoretical analysis where the above mechanisms have been generalized. This thesis provides the first direct experimental evidence that spatially constrained dendritic connectivity is a key factor for community composition and population persistence in riverine landscapes. As such, this thesis assesses a longstanding issue in spatial community ecology. It offers unique insights into the ecological forces structuring natural communities in a key ecosytem, and demonstrates principles that can be further tested in theoretical metacommunity models possibly to be extended to real riverine ecosystems. Taken together, the analyses show how the structure of ecological networks interacts with the spatial environmental matrix in determining biodiversity patterns and the functioning of biological communities. The analyses also suggest that altering the natural linkage between dendritic connectivity and patch size strongly affects community properties at multiple scales. The first part of this thesis (chapters 2 and 3) addresses key aspects of biodiversity-ecosystem functioning research where the combination of theory-guided experiments and theoretical investigations shows how a stochastic implementation of population dynamics proves fundamental for key community properties such as species persistence and community stability. The diversity-productivity and diversity-stability relationships are explored. Both experimental findings and the results of a stochastic model fitted to the experimental interaction matrix, suggest the emergence of strong stabilizing forces when species from different functional groups interact in the same environment, increasing species coexistence and community biomass production. The last part (chapter 6) provides a synthesis of this thesis work, in that it aims at unifying aspects from niche-theory, usually adopted in spatially implicit models, with those characteristic of a spatially explicit context from a typical real-life mountainous regions. It is dedicated to the possible explanation for a macroecological pattern routinely observed from organisms in different domains of life, that is, the mid-elevational peak in local species richness. Guided by empirical observations on diversity of macroinvertebrates in Swiss river basins, a theoretical ansatz is provided which is deemed to capture the essential geomorphological drivers and controls relating species-fitness to altitude. A set of overarching conclusions and perspectives for future research are discussed in the concluding chapter.

EPFL2013

Benthic Biofilms in Glacier-Fed Streams from Scandinavia to the Himalayas Host Distinct Bacterial Communities Compared with the Streamwater

Tom Ian Battin, Massimo Bourquin, Jade Brandani, Susheel Bhanu Busi, Vincent Henri De Staercke, Leïla Ezzat, Stylianos Fodelianakis, Tyler Joe Kohler, Grégoire Marie Octave Edouard Michoud, Emmy Marie Oppliger, Hannes Markus Peter, Paraskevi Pramateftaki, Martina Andrea Schön, Michail Styllas, Virginia Tadei, Matteo Tolosano

Microbial life in glacier-fed streams (GFSs) is dominated by benthic biofilms which fulfill critical ecosystem processes. However, it remains unclear how the bacterial communities of these biofilms assemble in stream ecosystems characterized by rapid turnover of benthic habitats and high suspended sediment loads. Using16S rRNA gene amplicon sequence data collected from 54 GFSs across the Himalayas, European Alps, and Scandinavian Mountains, we found that benthic biofilms harbor bacterial communities that are distinct from the bacterial assemblages suspended in the streamwater. Our data showed a decrease in species richness in the benthic biofilms compared to the bacterial cells putatively free-living in the water. The benthic biofilms also differed from the suspended water fractions in terms of community composition. Differential abundance analyses highlighted bacterial families that were specific to the benthic biofilms and the suspended assemblages. Notably, source-sink models suggested that the benthic biofilm communities are not simply a subset of the suspended assemblages. Rather, we found evidence that deterministic processes (e.g., species sorting) shape the benthic biofilm communities. This is unexpected given the high vertical mixing of water and contained bacterial cells in GFSs and further highlights the benthic biofilm mode of life as one that is determined through niche-related processes. Our findings therefore reveal a "native" benthic biofilm community in an ecosystem that is currently threatened by climate-induced glacier shrinkage. IMPORTANCE Benthic biofilms represent the dominant form of life in glacier-fed streams. However, it remains unclear how bacterial communities within these biofilms assemble. Our findings from glacier-fed streams from three major mountain ranges across the Himalayas, the European Alps and the Scandinavian Mountains reveal a bacterial community associated with benthic biofilms that is distinct from the assemblage in the overlying streamwater. Our analyses suggest that selection is the underlying process to this differentiation. This is unexpected given that bacterial cells that are freely living or attached to the abundant sediment particles suspended in the water continuously mix with the benthic biofilms. The latter colonize loose sediments that are subject to high turnover owing to the forces of the water flow. Our research unravels the existence of a microbiome specific to benthic biofilms in glacier-fed streams, now under major threats due to global warming. Benthic biofilms represent the dominant form of life in glacier-fed streams. However, it remains unclear how bacterial communities within these biofilms assemble.

AMER SOC MICROBIOLOGY2022

Theoretical and Experimental Studies of Dendritic Metacommunities

Francesco Carrara

EPFL2013

Benthic Biofilms in Glacier-Fed Streams from Scandinavia to the Himalayas Host Distinct Bacterial Communities Compared with the Streamwater

AMER SOC MICROBIOLOGY2022