From microbes to humans, organisms perform numerous tasks for their survival, including food acquisition, migration, and reproduction. A complex biological task can be performed by either an autonomous organism or by cooperation among several specialized organisms. However, it remains unclear how autonomy and cooperation evolutionarily switch. Specifically, it remains unclear whether and how cooperative specialists can repair deleted genes through direct genetic exchange, thereby regaining metabolic autonomy. Here, we address this question by experimentally evolving a mutualistic microbial consortium composed of two specialists that cooperatively degrade naphthalene. We observed that autonomous genotypes capable of performing the entire naphthalene degradation pathway evolved from two cooperative specialists and dominated the community. This evolutionary transition was driven by the horizontal gene transfer (HGT) between the two specialists. However, this evolution was exclusively observed in the fluctuating environment alternately supplied with naphthalene and pyruvate, where mutualism and competition between the two specialists alternated. The naphthalene-supplied environment exerted selective pressure that favors the expansion of autonomous genotypes. The pyruvate-supplied environment promoted the coexistence and cell density of the cooperative specialists, thereby increasing the likelihood of HGT. Using a mathematical model, we quantitatively demonstrate that environmental fluctuations facilitate the evolution of autonomy through HGT when the relative growth rate and carrying capacity of the cooperative specialists allow enhanced coexistence and higher cell density in the competitive environment. Together, our results demonstrate that cooperative specialists can repair deleted genes through a direct genetic exchange under specific conditions, thereby regaining metabolic autonomy.

中文翻译：

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波动环境中两位合作专家的自主性演变


从微生物到人类，生物体为了生存执行许多任务，包括食物获取、迁移和繁殖。复杂的生物任务可以由自主生物体或通过几个专门生物体之间的合作来执行。然而，目前尚不清楚自主和合作如何演变。具体来说，目前尚不清楚合作专家是否以及如何通过直接基因交换来修复删除的基因，从而重新获得代谢自主权。在这里，我们通过实验进化出一个由两位合作降解萘的专家组成的互惠微生物联盟来解决这个问题。我们观察到，能够执行整个萘降解途径的自主基因型是从两个合作专家进化而来的，并在社区中占主导地位。这种进化转变是由两位专家之间的水平基因转移（HGT）驱动的。然而，这种演变仅在萘和丙酮酸交替供应的波动环境中观察到，其中两种专家之间的互利共生和竞争交替出现。提供萘的环境施加了有利于自主基因型扩展的选择压力。提供丙酮酸的环境促进了合作专家的共存和细胞密度，从而增加了 HGT 的可能性。使用数学模型，我们定量地证明，当合作专家的相对增长率和承载能力允许在竞争环境中增强共存和更高的细胞密度时，环境波动通过 HGT 促进自主进化。 总之，我们的结果表明，合作专家可以在特定条件下通过直接基因交换来修复删除的基因，从而重新获得代谢自主权。