Remarkable technological advances have revealed ever more properties and behaviours of individual microorganisms, but the novel data generated by these techniques have not yet been fully exploited. In this Opinion article, we explain how individual-based models (IBMs) can be constructed based on the findings of such techniques and how they help to explore competitive and cooperative microbial interactions. Furthermore, we describe how IBMs have provided insights into self-organized spatial patterns from biofilms to the oceans of the world, phage-CRISPR dynamics and other emergent phenomena. Finally, we discuss how combining individual-based observations with IBMs can advance our understanding at both the individual and population levels, leading to the new approach of microbial individual-based ecology (μIBE).
BackgroundHow aging, being unfavourable for the individual, can evolve is one of the fundamental problems of biology. Evidence for aging in unicellular organisms is far from conclusive. Some studies found aging even in symmetrically dividing unicellular species; others did not find aging in the same, or in different, unicellular species, or only under stress. Mathematical models suggested that segregation of non-genetic damage, as an aging strategy, would increase fitness. However, these models failed to consider repair as an alternative strategy or did not properly account for the benefits of repair. We used a new and improved individual-based model to examine rigorously the effect of a range of aging strategies on fitness in various environments.ResultsRepair of damage emerges as the best strategy despite its fitness costs, since it immediately increases growth rate. There is an optimal investment in repair that outperforms damage segregation in well-mixed, lasting and benign environments over a wide range of parameter values. Damage segregation becomes beneficial, and only in combination with repair, when three factors are combined: (i) the rate of damage accumulation is high, (ii) damage is toxic and (iii) efficiency of repair is low. In contrast to previous models, our model predicts that unicellular organisms should have active mechanisms to repair damage rather than age by segregating damage. Indeed, as predicted, all organisms have evolved active mechanisms of repair whilst aging in unicellular organisms is absent or minimal under benign conditions, apart from microorganisms with a different ecology, inhabiting short-lived environments strongly favouring early reproduction rather than longevity.ConclusionsAging confers no fitness advantage for unicellular organisms in lasting environments under benign conditions, since repair of non-genetic damage is better than damage segregation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0052-x) contains supplementary material, which is available to authorized users.
The extent of senescence due to damage accumulation—or aging—is evidently evolvable as it differs 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. Despite the fundamental trade-off between investing resources into repair or into growth, repair and segregation of damage have not always been considered alternatives. For unicellular organisms, unrepaired damage could be divided asymmetrically between daughter cells, leading to senescence of one and rejuvenation of the other. Repair of “unicells” has been predicted to be advantageous in well-mixed environments such as chemostats. Most microorganisms, however, live in spatially structured systems, such as biofilms, with gradients of environmental conditions and cellular physiology as well as a clonal population structure. To investigate whether this clonal structure might favor senescence by damage segregation (a division-of-labor strategy akin to the germline-soma division in multicellular organisms), we used an individual-based computational model and developed an adaptive repair strategy where cells respond to their current intracellular damage levels by investing into repair machinery accordingly. Our simulations showed that the new adaptive repair strategy was advantageous provided that growth was limited by substrate availability, which is typical for biofilms. 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 beneficial only when extrinsic mortality is high, a degree of multicellularity is present, and an active mechanism makes segregation effective. IMPORTANCE Damage is an inevitable consequence of life. For unicellular organisms, this leads to a trade-off between allocating resources into damage repair or into growth coupled with segregation of damage upon cell division, i.e., aging and senescence. Few studies considered repair as an alternative to senescence. None considered biofilms, where the majority of unicellular organisms live, although fitness advantages in well-mixed systems often turn into disadvantages in spatially structured systems such as biofilms. We compared the fitness consequences of aging versus an adaptive repair mechanism based on sensing damage, using an individual-based model of a generic unicellular organism growing in biofilms. We found that senescence is not beneficial provided that growth is limited by substrate availability. Instead, it is useful as a stress response to deal with damage that failed to be repaired when (i) extrinsic mortality was high; (ii) a degree of multicellularity was present; and (iii) damage segregation was effective.
Modelling all three spatial dimensions is often much more computationally expensive than modelling a two-dimensional simplification of the same system. Researchers comparing these approaches in individual-based models of microbial biofilms report quantitative, but not qualitative, differences between 2D and 3D simulations. We show that a large part of the discrepancy is due to the different space packing densities of circles versus spheres, and demonstrate methods to compensate for this: the internal density of individuals or the distances between them can be scaled. This result is likely to be useful in similar models, such as smoothed particle hydrodynamics.
38The extent of senescence due to damage accumulation (or aging) is evidently evolvable as it 39 varies hugely between species and is not universal, suggesting that its fitness advantages 40 depend on life history and environment. In contrast, repair of damage is present in all 41 organisms studied. Repair and segregation of damage have not always been considered as 42 alternatives, despite the fundamental trade-off between investing resources into repair or 43 growth. For unicellular organisms, unrepaired damage could be divided asymmetrically 44 between daughter cells, leading to aging of one and rejuvenation of the other. Repair of 45 unicells has been shown to be advantageous in well-mixed environments such as chemostats. 46However, most microorganisms live in spatially structured systems such as biofilms with 47 IMPORTANCE 58 Damage is an inevitable consequence of life, leading to a trade-off between allocating 59 resources into damage repair or into growth whilst allowing aging, i.e., segregation of damage 60 upon cell division. Few studies considered repair as an alternative to aging. Moreover, all 61 previous studies merely considered well-mixed environments, although the vast majority of 62 unicellular organisms live in spatially structured environments, exemplified by biofilms, and 63 fitness advantages in well-mixed systems often turn into disadvantages in spatially structured 64 systems. We compared the fitness consequences of aging versus damage repair in biofilms 65with an individual-based model implementing an adaptive repair mechanism based on sensing 66 damage. We found that aging is not beneficial. Instead, it is useful as a stress response to deal 67 with damage that failed to be repaired when (i) clearly asymmetric cell division is feasible; (ii) 68 extrinsic mortality is high; and (iii) a degree of multicellularity is present. 69 70
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