Journal
ISME JOURNAL
Volume 15, Issue 3, Pages 688-701Publisher
SPRINGERNATURE
DOI: 10.1038/s41396-020-00806-9
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Funding
- Netherlands Organisation for Scientific Research (NWO) [13858]
- Slovenian Research Agency [J4-7640, J1-9194, N1-0100]
- Helmholtz-Zentrum Dresden-Rossendorf
- European Commission [826312]
- European Regional Development Fund [UIA02-228]
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Metabolic interactions between cells are influenced by the distance between cells, and in a three-dimensional system, these interactions are constrained by competition or removal of metabolites, reducing the metabolic interaction distances in the low micrometer range.
Metabolic interactions between cells affect microbial community compositions and hence their function in ecosystems. It is well-known that under competition for the exchanged metabolite, concentration gradients constrain the distances over which interactions can occur. However, interaction distances are typically quantified in two-dimensional systems or without accounting for competition or other metabolite-removal, conditions which may not very often match natural ecosystems. We here analyze the impact of cell-to-cell distance on unidirectional cross-feeding in a three-dimensional aqueous system with competition for the exchanged metabolite. Effective interaction distances were computed with a reaction-diffusion model and experimentally verified by growing a synthetic consortium of 1 mu m-sized metabolite producer, receiver, and competitor cells in different spatial structures. We show that receivers cannot interact with producers located on average 15 mu m away from them, as product concentration gradients flatten close to producer cells. We developed an aggregation protocol and varied the receiver cells' product affinity, to show that within producer-receiver aggregates even low-affinity receiver cells could interact with producers. These results show that competition or other metabolite-removal of a public good in a three-dimensional system reduces metabolic interaction distances to the low mu m-range, highlighting the importance of concentration gradients as physical constraint for cellular interactions.
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