Microbial competition reduces metabolic interaction distances to the low µm-range

Microbial competition reduces metabolic interaction distances to the low µm-range

van Tatenhove-Pel, R.J. (Vrije Universiteit Amsterdam)
Rijavec, Tomaž (Jozef Stefan Institute)
Lapanje, Aleš (Jozef Stefan Institute)
van Swam, Iris (Vrije Universiteit Amsterdam)
Zwering, Emile (Vrije Universiteit Amsterdam)
Hernandez-Valdes, Jhonatan A. (Rijksuniversiteit Groningen)
Kuipers, Oscar P. (Rijksuniversiteit Groningen)
Picioreanu, C. (TU Delft BT/Environmental Biotechnology)
Teusink, Bas (Vrije Universiteit Amsterdam)
Bachmann, Herwig (Vrije Universiteit Amsterdam; NIZO food research)

2020

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 µm-sized metabolite producer, receiver, and competitor cells in different spatial structures. We show that receivers cannot interact with producers located on average 15 µm 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 µm-range, highlighting the importance of concentration gradients as physical constraint for cellular interactions.

http://resolver.tudelft.nl/uuid:78756dd7-1cad-4ef3-84e8-17dad89f5ce1

https://doi.org/10.1038/s41396-020-00806-9

1751-7362

The ISME Journal: multidisciplinary journal of microbial ecology, 15 (3), 688-701

Institutional Repository

journal article

© 2020 R.J. van Tatenhove-Pel, Tomaž Rijavec, Aleš Lapanje, Iris van Swam, Emile Zwering, Jhonatan A. Hernandez-Valdes, Oscar P. Kuipers, C. Picioreanu, Bas Teusink, Herwig Bachmann