Molecular and cellular bases of adaptation to a changing environment in microorganisms

Abstract

Environmental heterogeneity constitutes an evolutionary challenge for organisms. While evolutionary dynamics under variable conditions has been explored for decades, we still know relatively little about the cellular and molecular mechanisms involved. It is of paramount importance to examine these molecular bases because they may play an important role in shaping the course of evolution. In this review, we examine the diversity of adaptive mechanisms in the face of environmental changes. We exploit the recent literature on microbial systems because those have benefited the most from the recent emergence of genetic engineering and experimental evolution followed by genome sequencing. We identify four emerging trends: (i) an adaptive molecular change in a pathway often results in fitness trade-off in alternative environments but the effects are dependent on a mutation's genetic background; (ii) adaptive changes often modify transcriptional and signalling pathways; (iii) several adaptive changes may occur within the same molecular pathway but be associated with pleiotropy of different signs across environments; (iv) because of their large associated costs, macromolecular changes such as gene amplification and aneuploidy may be a rapid mechanism of adaptation in the short-term only. The course of adaptation in a variable environment, therefore, depends on the complexity of the environment but also on the molecular relationships among the genes involved and between the genes and the phenotypes under selection.

Keywords: adaptive strategies; cellular and molecular mechanisms of adaptation; fitness trade-offs; fluctuating environments; gene regulation; pleiotropy.

Figure 1.

Anticipation regulation of carbon source succession in E. coli from Mitchell et al. [12]. Wild-type E. coli shows asymmetric anticipation by low-level activation of the maltose operon during lactose exposure (a). In maltose conditions, cells show no lactose operon activation (b). The response is only asymmetric in association with the ecological alternation of lactose and maltose. After laboratory evolution of E. coli cells for 500 generations in high lactose concentration, the capacity of anticipation is lost and maltose operons are not activated (c). Anticipatory regulation may be costly and maladaptive in conditions other than the particular successions encountered in the digestive tract of mammals.