Soil, the living terrestrial skin of the Earth, plays a central role in supporting life and is home to an unimaginable diversity of microorganisms. This review explores key drivers for microbial life in soils under different climates and land-use practices at scales ranging from soil pores to landscapes. We delineate special features of soil as a microbial habitat (focusing on bacteria) and the consequences for microbial communities. This review covers recent modeling advances that link soil physical processes with microbial life (termed biophysical processes). Readers are introduced to concepts governing water organization in soil pores and associated transport properties and microbial dispersion ranges often determined by the spatial organization of a highly dynamic soil aqueous phase. The narrow hydrological windows of wetting and aqueous phase connectedness are crucial for resource distribution and longer range transport of microorganisms. Feedbacks between microbial activity and their immediate environment are responsible for emergence and stabilization of soil structure-the scaffolding for soil ecological functioning. We synthesize insights from historical and contemporary studies to provide an outlook for the challenges and opportunities for developing a quantitative ecological framework to delineate and predict the microbial component of soil functioning.

Biophysical processes supporting the diversity of microbial life in soil.

The type 6 secretion system (T6SS) is a nanomachine used by many Gram-negative bacteria, including Vibrio cholerae, to deliver toxic effector proteins into adjacent eukaryotic and bacterial cells. Because the activity of the T6SS is dependent on direct contact between cells, its activity is limited to bacteria growing on solid surfaces or in biofilms. V. cholerae can produce an exopolysaccharide (EPS) matrix that plays a role in adhesion and biofilm formation. In this work, we investigated the effect of EPS production on T6SS activity between cells. We found that EPS produced by V. cholerae cells functions as a unidirectional protective armor that blocks exogenous T6SS attacks without interfering with its own T6SS functionality. This EPS armor is effective against both same-species and heterologous attackers. Mutations modulating the level of EPS biosynthesis gene expression result in corresponding modulation in V. cholerae resistance to exogenous T6SS attack. These results provide insight into the potential role of extracellular biopolymers, including polysaccharides, capsules, and S-layers in protecting bacterial cells from attacks involving cell-associated macromolecular protein machines that cannot readily diffuse through these mechanical defenses.

https://www.pnas.org/content/pnas/115/31/7997.full.pdf

Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system.

Biofilms are dynamic habitats which constantly evolve in response to environmental fluctuations and thereby constitute remarkable survival strategies for microorganisms. The modulation of biofilm functional properties is largely governed by the active remodeling of their three-dimensional structure and involves an arsenal of mircrobial self-produced components and interconnected mechanisms. The production of matrix components, the spatial reorganization of ecological interactions, the generation of physiological heterogeneity, the regulation of motility, the production of actives enzymes are for instance some of the processes enabling such spatial organization plasticity. In this contribution, we discussed the foundations of architectural plasticity as an adaptive driver of biofilms through the review of the different microbial strategies involved. Moreover, the possibility to harness such characteristics to sculpt biofilm structure as an attractive approach to control their functional properties, whether beneficial or deleterious, is also discussed.

/pdf/spatial-organization-plasticity-as-an-adaptive-driver-of-2ik5zq1u6v.pdf

Spatial Organization Plasticity as an Adaptive Driver of Surface Microbial Communities.

Volume microscopy has become an important method in cellular biology. In contrast to tedious serial sectioning volumes can now far more conveniently be obtained with serial-block face and focussed ion beam scanning electron microscopy. Serial-block face scanning electron microscopy is the instrument of choice for large volumes whereas focussed ion beam scanning electron microscopy has its merits in high voxel resolution. These aspects are discussed along with some specific applications of a focussed ion beam scanning electron microscope.

Volume microscopy in biology: FIB-SEM tomography.

Collective cell movement is critical to the emergent properties of many multicellular systems, including microbial self-organization in biofilms, embryogenesis, wound healing, and cancer metastasis However, even the best-studied systems lack a complete picture of how diverse physical and chemical cues act upon individual cells to ensure coordinated multicellular behavior Known for its social developmental cycle, the bacterium Myxococcus xanthus uses coordinated movement to generate three-dimensional aggregates called fruiting bodies Despite extensive progress in identifying genes controlling fruiting body development, cell behaviors and cell-cell communication mechanisms that mediate aggregation are largely unknown We developed an approach to examine emergent behaviors that couples fluorescent cell tracking with data-driven models A unique feature of this approach is the ability to identify cell behaviors affecting the observed aggregation dynamics without full knowledge of the underlying biological mechanisms The fluorescent cell tracking revealed large deviations in the behavior of individual cells Our modeling method indicated that decreased cell motility inside the aggregates, a biased walk toward aggregate centroids, and alignment among neighboring cells in a radial direction to the nearest aggregate are behaviors that enhance aggregation dynamics Our modeling method also revealed that aggregation is generally robust to perturbations in these behaviors and identified possible compensatory mechanisms The resulting approach of directly combining behavior quantification with data-driven simulations can be applied to more complex systems of collective cell movement without prior knowledge of the cellular machinery and behavioral cues

https://www.pnas.org/content/pnas/114/23/E4592.full.pdf

Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development.

The myxobacteria are a family of soil bacteria that form biofilms of complex architecture, aligned multilayered swarms or fruiting body structures that are simple or branched aggregates containing myxospores. Here, we examined the structural role of matrix exopolysaccharide (EPS) in the organization of these surface-dwelling bacterial cells. Using time-lapse light and fluorescence microscopy, as well as transmission electron microscopy and focused ion beam/scanning electron microscopy (FIB/SEM) electron microscopy, we found that Myxococcus xanthus cell organization in biofilms is dependent on the formation of EPS microchannels. Cells are highly organized within the three-dimensional structure of EPS microchannels that are required for cell alignment and advancement on surfaces. Mutants lacking EPS showed a lack of cell orientation and poor colony migration. Purified, cell-free EPS retains a channel-like structure, and can complement EPS- mutant motility defects. In addition, EPS provides the cooperative structure for fruiting body formation in both the simple mounds of M. xanthus and the complex, tree-like structures of Chondromyces crocatus. We furthermore investigated the possibility that EPS impacts community structure as a shared resource facilitating cooperative migration among closely related isolates of M. xanthus.

/pdf/exopolysaccharide-microchannels-direct-bacterial-motility-4l4pdf2w29.pdf

Angela Zhang

Papers

Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior