Systems Microbiology & Microbial Ecology
We are an interdisciplinary research group aiming at enhancing our understanding of the microbial world.
We combine theory, models and simulations with wet lab experiments and analysis of samples from the field.
Our research builds upon cutting-edge technology including:
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Advanced automated microscopy and state of the art image analysis.
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Modeling and computer simulations based on massively parallel cloud computing.
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Next generation sequencing.
We aim at revealing general principles that govern natural systems across multiple levels: from individual cells and organisms through populations and communities and up to ecosystems. We strive to combine knowledge from disparate fields, e.g. physics, computer science, chemistry and biology, to synthesize novel concepts that enable better understanding of complex biological systems.
Our research is based on, and inspired by, a few model systems - a central one is the phyllosphere.
Bacterial life on plant leaf surfaces - the phyllosphere
Leaves are inhabited by diverse microorganisms, mostly bacteria. Although these microbial communities collectively constitute one of the largest microbe-populated surface area on earth, we know very little about them. We do know that only a fraction cause plant disease, yet, the contribution of these microbial communities to plant health is far from being understood.
The phyllosphere is a microbial habitat which is both spatially heterogeneous and which experiences significant temporal changes in environmental variables such as temperature, radiation and hydration conditions, making them an ideal model ecosystem to study how microbial communities cope with spatial and temporal environmental variation.
Leaves are also an excellent model to study bacterial life on unsaturated surfaces (i.e. not constantly water saturated) – which characterize other important terrestrial microbial habitats including soil and roots.
We believe that a deeper and better understanding of the microbial life on plant leaves is essential for fighting plant disease, the development of bio-control approaches, and for improving sustainable agriculture.
To understand the microbial life of the phyllosphere research methods require crossing a range of timescales (from milliseconds of water flow, to minutes or hours of bacterial subdivision rates, to months of a typical leaf lifespan), as well as spatial scales (from 1µm bacteria to tens of µm of leaf surface heterogeneity, to centimetres or meters of plant size and kilometres of biogeography).
Bacterial life in microscopic surface wetness
The varying hydration conditions on the leaf surface and the resulting microscopic dynamics of the waterscape are central features of the leaf surface as a microbial habitat. We recently revealed that microscopic droplets are formed around bacterial cells and aggregates on surface drying under moderate humidities, due to capillary pinning and deliquescence properties of salts [Grinberg et al eLife 2019]. Deliquescent compounds are common on leaves (e.g. from aerosols) and were suggested to form thin liquid films and microdroplets during daytime as a result of the moderate relative humidity on the leaf surface (due to transpiration).
We also study the effect of this dynamic waterscape, which creates a fragmented landscape during daytime that becomes connected only at night (when the leaf is water-saturated), through multi wet-dry cycle experiments, coupled with modelling. This largely overlooked phenomenon has crucial consequences for bacterial life on leaves. It limits cell spreading outside of droplets, and restricts most cell-to-cell interactions within droplets.
Current ongoing research projects in the lab aim at studying the impact of microscopic surface wetness on additional key aspects of bacterial life, including motility, communication, antibiotic tolerance [Beizman-Magen et al ISME Journal 2021], competition, interactions, and exchange of genetic material [Orevi et al ISME COMMS 2022] . See also our recent Perspective [Orevi & Kashtan Frontiers in Microbiology 2021].
Self-organization and collective properties of bacterial populations and communities
We seek to better understand the interplay between individual-cell behavior, self-organization, and collective emergent properties of populations and communities. We recently developed the concept of "aggregate enrichment mechanisms" (AEMs) – mechanisms that accelerate the growth of bacterial aggregates beyond reproductive growth. We hypothesized that AEMs are common and play an important role in the formation of large aggregates, that provide protection from various stresses (e.g. desiccation, antibiotics and predation), particularly in nutrient poor environments, such as the leaf surface. We show, using individual-based models and computer simulations, that during early surface colonization, a simple preferential attachment (PA) strategy to dense sites on the surface, can significantly improve fitness under periodic stress conditions [Grinberg et al PLOS Comp. Biol. 2019]. We observe indications of PA in our experiments with natural leaf microbiota [Steinberg et al ISME Journal 2020].
Another main research direction aims at understanding the robust self-organization of bacterial communities, composed of hundreds of species, on the leaf. Similar to other complex biological systems (e.g. gene regulation, multi-cellular organism developmental), leaf microbiota somehow overcome inherent stochasticity and show robust patterns of self-organization. To study this robust assembly we have developed a method to extract the natural microbiota from a leaf. This allows us to study µ-scale interactions between 'model strains', including pathogens, with their native (and non-native) plant microbiota [Steinberg et al ISME Journal 2020].
Microscale interactions within and between populations
We seek to understand what microscale interactions commonly occur between bacterial cells on leaf surfaces and what is the role of such microscale interactions in the robust non-random self-organization of the population on the leafs surface. As an example we have found evidence for Preferential attachment of immigrant bacteria to native plant leaf microbiota [Steinberg et al ISME Journal 2020].
