Pseudomonas sp. GM17 Raw sequence reads. Pseudomonas sp. GM17

Horizontal gene transfer (HGT) is a fundamental evolutionary process that plays a key role in bacterial evolution. The likelihood of a successful transfer event is expected to depend on the precise balance of costs and benefits resulting from pathway acquisition. Most experimental analyses of HGT have focused on phenotypes that have large fitness benefits under appropriate selective conditions, such as antibiotic resistance. However, many examples of HGT involve phenotypes that are predicted to provide smaller benefits, such as the ability to catabolize additional carbon sources. We have experimentally reproduced one such HGT event in the laboratory, studying the effects of transferring a pathway for catabolism of the plant-derived aromatic compound salicyl alcohol into soil isolates from the Pseudomonas genus. We find that pathway acquisition enables rapid catabolism of salicyl alcohol with only minor disruptions to existing metabolic and regulatory networks of the new host. However, this new catabolic potential does not confer a measurable fitness advantage during competitive growth in the rhizosphere. We conclude that the phenotype of salicyl alcohol catabolism is readily transferred by HGT but is selectively neutral under environmentally-relevant conditions. We propose that this condition is common and that HGT of many pathways will be self-limiting because the selective benefits are small and negative frequency-dependent.

水平基因转移（Horizontal gene transfer, HGT）是一类核心进化过程，在细菌进化中发挥关键作用。成功的转移事件发生概率，取决于获取代谢通路所带来的成本与收益间的精确平衡。目前多数针对水平基因转移的实验分析，均聚焦于在适宜选择条件下可带来显著适应度收益的表型，例如抗生素抗性。然而，诸多水平基因转移的实例所涉及的表型，其预期收益相对有限，比如分解额外碳源的能力。本研究在实验室中复刻了一例此类水平基因转移事件，探究将植物源芳香化合物水杨醇的分解代谢通路，转入假单胞菌属（Pseudomonas）土壤分离菌株后的影响。研究发现，获取该代谢通路可使宿主快速分解水杨醇，且仅对新宿主原有的代谢与调控网络造成极轻微的扰动。但在根际环境的竞争性生长条件下，这一新获得的分解代谢能力并未带来可检测的适应度优势。综上，水杨醇分解代谢的表型可通过水平基因转移轻松实现转移，但在符合环境相关性的条件下，该表型呈现选择中性。本研究据此提出，此类选择中性的水平基因转移事件较为普遍，且诸多代谢通路的水平基因转移会呈现自我限制特性——因其选择收益有限，且存在负频率依赖效应。