Vo Lam, Avgidis Fotios, Mattingly Henry H, Edmonds Karah, Burger Isabel, Balasubramanian Ravi, Shimizu Thomas S, Kazmierczak Barbara I, Emonet Thierry
bioRxiv. 2024 Nov 21:2024.01.02.573956. doi: 10.1101/2024.01.02.573956.
Cell populations must adjust their phenotypic composition to adapt to changing environments. One adaptation strategy is to maintain distinct phenotypic subsets within the population and to modulate their relative abundances via gene regulation. Another strategy involves genetic mutations, which can be augmented by stress-response pathways. Here, we studied how a migrating bacterial population regulates its phenotypic distribution to traverse diverse environments. We generated isogenic populations with varying distributions of swimming behaviors and observed their phenotype distributions during migration in liquid and porous environments. We found that the migrating populations became enriched with high-performing swimming phenotypes in each environment, allowing the populations to adapt without requiring mutations or gene regulation. This adaptation is dynamic and rapid, reversing in a few doubling times when migration ceases. By measuring the chemoreceptor abundance distributions during migration towards different attractants, we demonstrated that adaptation acts on multiple chemotaxis-related traits simultaneously. These measurements are consistent with a general mechanism in which adaptation results from a balance between cell growth generating diversity and collective migration eliminating under-performing phenotypes. Thus, collective migration enables cell populations with continuous, multi-dimensional phenotypes to flexibly and rapidly adapt their phenotypic composition to diverse environmental conditions.
Conventional cell adaptation mechanisms, like gene regulation and stochastic phenotypic switching, act swiftly but are limited to a few traits, while mutation-driven adaptations unfold slowly. By quantifying phenotypic diversity during bacterial collective migration, we discovered an adaptation mechanism that rapidly and reversibly adjusts multiple traits simultaneously. By balancing the generation of diversity through growth with the loss of phenotypes unable to keep up, this process tunes the phenotypic composition of migrating populations to the environments they traverse, without gene regulation or mutations. Given the prevalence of collective migration in microbes, cancers, and embryonic development, non-genetic adaptation through collective migration may be a universal mechanism for populations to navigate diverse environments, offering insights into broader applications across various fields.
细胞群体必须调整其表型组成以适应不断变化的环境。一种适应策略是在群体中维持不同的表型亚群，并通过基因调控来调节它们的相对丰度。另一种策略涉及基因突变，应激反应途径可增强这种突变。在这里，我们研究了迁移的细菌群体如何调节其表型分布以穿越不同的环境。我们生成了具有不同游泳行为分布的同基因群体，并观察了它们在液体和多孔环境中迁移时的表型分布。我们发现，迁移的群体在每个环境中都富集了高性能的游泳表型，使群体能够在无需突变或基因调控的情况下适应环境。这种适应是动态且快速的，在迁移停止后的几个倍增时间内就会逆转。通过测量向不同引诱剂迁移过程中的化学感受器丰度分布，我们证明适应作用于多个与趋化性相关的性状。这些测量结果与一种普遍机制一致，即适应是由产生多样性的细胞生长与消除表现不佳的表型的集体迁移之间的平衡所导致的。因此，集体迁移使具有连续、多维度表型的细胞群体能够灵活、快速地调整其表型组成以适应不同的环境条件。
传统的细胞适应机制，如基因调控和随机表型转换，作用迅速但仅限于少数性状，而突变驱动的适应则进展缓慢。通过量化细菌集体迁移过程中的表型多样性，我们发现了一种能够同时快速且可逆地调节多个性状的适应机制。通过平衡生长产生的多样性与跟不上的表型的丧失，这个过程将迁移群体的表型组成调整到它们所穿越的环境，而无需基因调控或突变。鉴于集体迁移在微生物、癌症和胚胎发育中普遍存在，通过集体迁移进行的非遗传适应可能是群体在不同环境中导航的一种普遍机制，为跨领域的更广泛应用提供了见解。
