Abstract
Environmental structure describes physical structure that can determine heterogenous spatial distribution of biotic and abiotic (nutrients, stressors etc.) components of a microorganism’s microenvironment. This study investigated the impact of micrometre-scale structure on microbial stress sensing, using yeast cells exposed to copper in microfluidic devices comprising either complex soil-like architectures or simplified environmental structures. In the soil micromodels, the responses of individual cells to inflowing medium supplemented with high copper (using cells expressing a copper-responsive pCUP1-reporter fusion) could be described neither by spatial metrics developed to quantify proximity to environmental structures and surrounding space, nor by computational modelling of fluid flow in the systems. In contrast, the proximities of cells to structures did correlate with their responses to elevated copper in microfluidic chambers that contained simplified environmental structure. Here, cells within more open spaces showed the stronger responses to the copper-supplemented inflow. These insights highlight not only the importance of structure for microbial responses to their chemical environment, but also how predictive modelling of these interactions can depend on complexity of the system, even when deploying controlled laboratory conditions and microfluidics.
Highlights
Microorganisms such as bacteria and fungi are subject to temporal and spatial variation in the abiotic and biotic factors that shape their microenvironments, metabolism and proliferation (Jasinska et al, 2009, Nunan 2017)
In order to investigate the relationships between single-cell exposure to elevated copper and parameters of environmental structure, first the range over which the pCUP1-GFP reporter of copper stress could be used to report reliably on copper sensing by the cells was assayed
This study examined the impact of micrometre-scale environmental structure on microbial stress response, as environments of such scale are common in the soil pore space
Summary
Microorganisms such as bacteria and fungi are subject to temporal and spatial variation in the abiotic (nutrients, oxygen, temperature etc.) and biotic factors that shape their microenvironments, metabolism and proliferation (Jasinska et al, 2009, Nunan 2017). Other examples of porous microenvironments range from virtually all natural microbial habitats to biomedical devices (Francolini and Donelli, 2010) and hygenic surfaces (Verran et al, 2010). There are very few studies of how micrometrescale environmental structure impacts the sensing (exposure and response) by microorganisms of environmental stimuli. This is important considering that microorganisms residing in structured environments such as soil are vital for biogeochemical cycling, but are subject to stressors such as toxic pollutants (e.g., metals and microplastics) (Toth et al, 2016, Rillig et al, 2020) and other environmental perturbations such as temperature- and rainfall-fluctuations, mechanical disturbance, etc. Understanding how environmental micro-structure influences the responses of microbial communities to perturbation will enable deeper predictive understanding of the impacts of such perturbation on essential microbial services
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