Clegg, R. J. | bioRxiv Science

bioRxiv2023

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

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. Author summaryMicrobes are fascinating in their own right and play a tremendously important role in ecosystems. They often form complex, self-organized communities with spatial heterogeneity that is changing over time. Such complexity is challenging to understand and manage without the help of mathematical models. Individual-based models are one type of mathematical model that is particularly suited if differences between individual microbes, local interactions and adaptive behavior are important. We have developed a completely overhauled version of iDynoMiCS, a software that allows users to develop, run and analyze a wide range of individual-based models without having to program the software themselves. There are several capability enhancements and numerous small improvements, for example the ability to model different shapes of cells combined with physically realistic mechanical interactions between neighboring cells. We showcase this by simulating the competition between filaments, long chains of cells, with single cells and find that filaments outcompete single cells as they can spread quickly to new territory with higher levels of resources. Users now have a wider choice of platforms so we provide guidance on which platform might be most suitable for a given purpose.

ecology↗

bioRxiv2020

Damage repair versus aging in biofilms

The extent of senescence due to damage accumulation (or aging) is evidently evolvable as it varies hugely between species and is not universal, suggesting that its fitness advantages depend on life history and environment. In contrast, repair of damage is present in all organisms studied. Repair and segregation of damage have not always been considered as alternatives, despite the fundamental trade-off between investing resources into repair or growth. For unicellular organisms, unrepaired damage could be divided asymmetrically between daughter cells, leading to aging of one and rejuvenation of the other. Repair of unicells has been shown to be advantageous in well-mixed environments such as chemostats. However, most microorganisms live in spatially structured systems such as biofilms with gradients of environmental conditions and cellular physiology as well as clonal population structure. We asked whether this clonal structure might favor aging by damage segregation as this can be seen as a division of labor strategy, akin to the germline soma division in multicellular organisms. We used an individual-based model with a newly developed adaptive repair strategy where cells respond to their current intracellular damage levels by investing into repair machinery accordingly. We found that the new adaptive repair strategy was advantageous whenever efficient and optimal, both in biofilms and chemostats. Thus, biofilms do not favor a germline soma-like division of labor between daughter cells in terms of damage segregation. We suggest that damage segregation is only beneficial when active and effective, extrinsic mortality is high and a degree of multicellularity is present. IMPORTANCEDamage is an inevitable consequence of life, leading to a trade-off between allocating resources into damage repair or into growth whilst allowing aging, i.e., segregation of damage upon cell division. Few studies considered repair as an alternative to aging. Moreover, all previous studies merely considered well-mixed environments, although the vast majority of unicellular organisms live in spatially structured environments, exemplified by biofilms, and fitness advantages in well-mixed systems often turn into disadvantages in spatially structured systems. We compared the fitness consequences of aging versus damage repair in biofilms with an individual-based model implementing an adaptive repair mechanism based on sensing damage. We found that aging is not beneficial. Instead, it is useful as a stress response to deal with damage that failed to be repaired when (i) clearly asymmetric cell division is feasible; (ii) extrinsic mortality is high; and (iii) a degree of multicellularity is present.

microbiology↗