A multiphase theory for spreading microbial swarms and films.

Siddarth Srinivasan,C Nadir Kaplan,L Mahadevan

doi:10.7554/elife.42697

Abstract

Bacterial swarming and biofilm formation are collective multicellular phenomena through which diverse microbial species colonize and spread over water-permeable tissue. During both modes of surface translocation, fluid uptake and transport play a key role in shaping the overall morphology and spreading dynamics. Here we develop a generalized two-phase thin-film model that couples bacterial growth, extracellular matrix swelling, fluid flow, and nutrient transport to describe the expansion of both highly motile bacterial swarms, and sessile bacterial biofilms. We show that swarm expansion corresponds to steady-state solutions in a nutrient-rich, capillarity dominated regime. In contrast, biofilm colony growth is described by transient solutions associated with a nutrient-limited, extracellular polymer stress driven limit. We apply our unified framework to explain a range of recent experimental observations of steady and unsteady expansion of microbial swarms and biofilms. Our results demonstrate how the physics of flow and transport in slender geometries serve to constrain biological organization in microbial communities.

Highlights

Bacteria employ sophisticated surface translocation machinery to actively swarm, twitch, glide or slide over solid surfaces (Kearns, 2010; Mattick, 2002; Spormann, 1999; Holscher and Kovacs, 2017)
These include measurements in B. subtilis swarms in this work, and in E. coli swarms previously reported by Darnton et al (2010) and Wu and Berg (2012) that are summarized in Table A2 in Appendix 2
We have presented a multi-phase theory that quantitatively describes the expansion dynamics of microbial swarms and biofilms and considers variations in the colony thickness, an aspect of colony expansion that has often been overlooked in many theories (Korolev et al, 2012; Ghosh et al, 2015; Wang et al, 2017)

Summary

Introduction

Bacteria employ sophisticated surface translocation machinery to actively swarm, twitch, glide or slide over solid surfaces (Kearns, 2010; Mattick, 2002; Spormann, 1999; Holscher and Kovacs, 2017). For both swarms and biofilms, the active phase (i.e., swarm cells or the EPS matrix) is generated within the bacterial colony by converting nutrient in the underlying substrate to biomass. These include measurements in B. subtilis swarms in this work, and in E. coli swarms previously reported by Darnton et al (2010) and Wu and Berg (2012) that are summarized in Table A2 in Appendix 2. Our generalized multiphase model is able to quantitatively rationalize the expansion curves, transition time and localized biological activity observed experimentally, and demonstrates that nutrient availability and diffusive transport governs the dynamics of Bacillus subtilis macrocolonies grown on agar

Discussion

Funding Funder National Science Foundation

Materials and methods

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