Interaction-dependent effects of surface structure on microbial spatial self-organization

Philos Trans R Soc Lond B Biol Sci. 2020 May 11;375(1798):20190246. doi: 10.1098/rstb.2019.0246. Epub 2020 Mar 23.

Abstract

Surface-attached microbial communities consist of different cell types that, at least to some degree, organize themselves non-randomly across space (referred to as spatial self-organization). While spatial self-organization can have important effects on the functioning, ecology and evolution of communities, the underlying determinants of spatial self-organization remain unclear. Here, we hypothesize that the presence of physical objects across a surface can have important effects on spatial self-organization. Using pairs of isogenic strains of Pseudomonas stutzeri, we performed range expansion experiments in the absence or presence of physical objects and quantified the effects on spatial self-organization. We demonstrate that physical objects create local deformities along the expansion frontier, and these deformities increase in magnitude during range expansion. The deformities affect the densities of interspecific boundaries and diversity along the expansion frontier, and thus affect spatial self-organization, but the effects are interaction-dependent. For competitive interactions that promote sectorized patterns of spatial self-organization, physical objects increase the density of interspecific boundaries and diversity. By contrast, for cross-feeding interactions that promote dendritic patterns, they decrease the density of interspecific boundaries and diversity. These qualitatively different outcomes are probably caused by fundamental differences in the orientations of the interspecific boundaries. Thus, in order to predict the effects of physical objects on spatial self-organization, information is needed regarding the interactions present within a community and the general geometric shapes of spatial self-organization that emerge from those interactions. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

Keywords: denitrification; microbial ecology; pattern formation; range expansion; self-organization; surface structure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Microbiota / physiology*
  • Pseudomonas stutzeri / physiology*

Associated data

  • figshare/10.6084/m9.figshare.c.4853211