Spatiotemporal establishment of dense bacterial colonies growing on hard agar.

Mya R Warren,Hui Sun,Terence Hwa,Yue Yan,Jonas Cremer,Bo Li

doi:10.7554/elife.41093

Abstract

The physical interactions of growing bacterial cells with each other and with their surroundings significantly affect the structure and dynamics of biofilms. Here a 3D agent-based model is formulated to describe the establishment of simple bacterial colonies expanding by the physical force of their growth. With a single set of parameters, the model captures key dynamical features of colony growth by non-motile, non EPS-producing E. coli cells on hard agar. The model, supported by experiment on colony growth in different types and concentrations of nutrients, suggests that radial colony expansion is not limited by nutrients as commonly believed, but by mechanical forces. Nutrient penetration instead governs vertical colony growth, through thin layers of vertically oriented cells lifting up their ancestors from the bottom. Overall, the model provides a versatile platform to investigate the influences of metabolic and environmental factors on the growth and morphology of bacterial colonies.

Highlights

Bacteria often form dense biofilms with complex spatiotemporal structures (Costerton et al, 1995; Nadell et al, 2016; O’Toole et al, 2000; Stoodley et al, 2002)
We develop a conceptually simple, yet physically realistic three-dimensional computational model, incorporating the elements of nutrient diffusion, cell-cell and cell-agar mechanical interactions, and introducing a unique cell-level model of surface tension
To describe the morphology and dynamics of these growing colonies in the linear regime, we focus on several main elements in the process: the supply of nutrient and interaction driven by the physical growth of cells

Summary

Introduction

Bacteria often form dense biofilms with complex spatiotemporal structures (Costerton et al, 1995; Nadell et al, 2016; O’Toole et al, 2000; Stoodley et al, 2002). Biofilms often play important roles in diverse settings ranging from environment to human health (Costerton et al, 1999; Jayaraman and Wood, 2008; Potera, 1999) They are notoriously difficult to study experimentally because of their opaqueness, high heterogeneity and complex organization, involving multiple spatial and temporal scales (Roberts et al, 2015; Stewart and Franklin, 2008). Various computational models have been constructed to capture different aspects of biofilm development (Alpkvist et al, 2006; Espeso et al, 2015; Ginovart et al, 2002; Klapper and Dockery, 2002; Kreft et al, 2001; Kreft et al, 1998; Picioreanu et al, 2004; Seminara et al, 2012; Tierra et al, 2015) Most of these models are ‘descriptive’ in nature – the complexity of the biofilms makes it difficult to make quantitative comparison between experimental data and model predictions. The simplest among these is the growth of a simple bacterial colony on hard agar surface, with cells pushing against each other by the force of their own physical growth, without

Methods

Results

Conclusion