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.
Keywords: aging; division of labor; evolution; mathematical modeling; senescence; trade-offs.
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