Is it selfish to be filamentous in biofilms? Individual-based modeling links microbial growth strategies with morphology using the new and modular iDynoMiCS 2.0

PLoS Comput Biol. 2024 Feb 29;20(2):e1011303. doi: 10.1371/journal.pcbi.1011303. eCollection 2024 Feb.

Abstract

Microbial communities are found in all habitable environments and often occur in assemblages with self-organized spatial structures developing over time. This complexity can only be understood, predicted, and managed by combining experiments with mathematical modeling. Individual-based models are particularly suited if individual heterogeneity, local interactions, and adaptive behavior are of interest. Here we present the completely overhauled software platform, the individual-based Dynamics of Microbial Communities Simulator, iDynoMiCS 2.0, which enables researchers to specify a range of different models without having to program. Key new features and improvements are: (1) Substantially enhanced ease of use (graphical user interface, editor for model specification, unit conversions, data analysis and visualization and more). (2) Increased performance and scalability enabling simulations of up to 10 million agents in 3D biofilms. (3) Kinetics can be specified with any arithmetic function. (4) Agent properties can be assembled from orthogonal modules for pick and mix flexibility. (5) Force-based mechanical interaction framework enabling attractive forces and non-spherical agent morphologies as an alternative to the shoving algorithm. The new iDynoMiCS 2.0 has undergone intensive testing, from unit tests to a suite of increasingly complex numerical tests and the standard Benchmark 3 based on nitrifying biofilms. A second test case was based on the "biofilms promote altruism" study previously implemented in BacSim because competition outcomes are highly sensitive to the developing spatial structures due to positive feedback between cooperative individuals. We extended this case study by adding morphology to find that (i) filamentous bacteria outcompete spherical bacteria regardless of growth strategy and (ii) non-cooperating filaments outcompete cooperating filaments because filaments can escape the stronger competition between themselves. In conclusion, the new substantially improved iDynoMiCS 2.0 joins a growing number of platforms for individual-based modeling of microbial communities with specific advantages and disadvantages that we discuss, giving users a wider choice.

MeSH terms

  • Adaptation, Psychological*
  • Algorithms*
  • Altruism
  • Benchmarking
  • Biofilms
  • Humans

Grants and funding

TF, RJC, KA and JUK would like to thank the United Kingdom National Centre for the Replacement, Refinement & Reduction of Animals in Research (NC3Rs) for funding our development of individual-based modeling platforms for the gut environment (Grants NC/K000683/1 and NC/R001707/1). BJRC and BFS would like to thank the Integrated Water Technology (InWaTech) project, which promotes collaborative research between DTU and KAIST, for funding our work on work on microbial aggregation and granular biofilms. SA was funded by a University of Nottingham Vice Chancellor’s Scholarship. The funders had no role in study design, data collection and interpretation, decision to publish, or preparation of the manuscript.