Metabolic activity affects response of single cells to a nutrient switch in structured populations

Abstract

Microbes live in ever-changing environments where they need to adapt their metabolism to different nutrient conditions. Many studies have characterized the response of genetically identical cells to nutrient switches in homogenous cultures, however in nature microbes often live in spatially structured groups such as biofilms where cells can create metabolic gradients by consuming and releasing nutrients. Consequently, cells experience different local microenvironments and vary in their phenotype. How does this phenotypic variation affect the ability of cells to cope with nutrient switches? Here we address this question by growing dense populations of Escherichia coli in microfluidic chambers and studying a switch from glucose to acetate at the single cell level. Before the switch, cells vary in their metabolic activity: some grow on glucose while others cross-feed on acetate. After the switch, only few cells can resume growth after a period of lag. The probability to resume growth depends on a cells' phenotype prior to the switch: it is highest for cells crossfeeding on acetate, while it depends in a non-monotonic way on growth rate for cells growing on glucose. Our results suggest that the strong phenotypic variation in spatially structured populations might enhance their ability to cope with fluctuating environments.

Spatial organization in microbial range expansion emerges from trophic dependencies and successful lineages

“…In contrast to advection dominated planktonic life style, bacterial cells in diffusion dominated systems often self-engineer their immediate surroundings (a process frequently termed niche construction 20 ). For example, single species biofilms engage in cross-feeding interactions through divergent behavior of spatially segregated subpopulations experiencing fundamentally different growth conditions 21,22 . Overall, trophic interactions have the potential to shape the emerging community patterns during bacterial range expansion.…”

Challenges and approaches in assessing the interplay between microorganisms and their physical micro-environments

“…While there are many more examples of the use of X-ray CT for assessing soil structure [31] , [29] , [13] , [52] , [19] , the applications to structured environments go beyond soils. Bradley et al [6] used X-ray nanotomography – X-ray CT at sub-micron resolution – with Zernike phase-contrast (to enhance the subject/background contrast) for examining the distribution and depth of human fibroblast cells grown on polymer scaffolding.…”

“…Microfluidics has been used to establish biofilms and monitor growth and inherent metabolic dynamics under controlled conditions. In a recent study, E. coli monolayers were cultured in a device designed to establish a glucose gradient in a series of dead-end chambers containing the bacteria (measuring 40 µm × 60 µm) after introducing flow perpendicular to the chamber opening [13] . Fluorescence analysis of gene reporter expression indicated that cells at the front of the chamber metabolised glucose and secreted acetate whereas cells towards the back of the chamber (which were glucose limited) could metabolise the secreted acetate.…”

“…These structures can facilitate the persistence of biofilm-forming organisms after physical perturbation, such as when mechanically cleaning a surface or when fluid flow generates shear forces [15] . Biofilms themselves can be considered highly structured environments encompassing the spatial division of different species, of labour within a monospecies biofilm, and of gradients in nutrients or secreted-metabolites from cells (with the metabolites from some cells serving as substrates for others) [13] .…”

Growing, evolving and sticking in a flowing environment: understanding IgA interactions with bacteria in the gut

“…Moreover, generating or altering community structure through sIgA‐mediated clumping may influence cross‐feeding and therefore growth rates in both targeted and untargeted species, as has been observed in biofilms . Finally, highly cooperative species may actually grow faster when kin‐association is enforced by enchained growth.…”