Damage repair versus aging in biofilms

Abstract

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.