Granato Elisa T, Palmer Jacob D, Kirk Christian, Sharp Connor, Shillcock George, Foster Kevin R
Department of Biology, University of Oxford, Oxford, United Kingdom.
Department of Biochemistry, University of Oxford, Oxford, United Kingdom.
PLoS Biol. 2025 May 21;23(5):e3003095. doi: 10.1371/journal.pbio.3003095. eCollection 2025 May.
Bacteria commonly use molecular weaponry to kill or inhibit competitors. Genes encoding many weapons and their associated immunity mechanisms can be transmitted horizontally. These transfer events are striking because they appear to undermine bacterial weapons when given to competing strains. Here, we develop an ecological model of bacterial warfare to understand the impacts of horizontal gene transfer. Our model predicts that weapon gene transfer from an attacker to a target strain is possible, but will typically occur at a low rate such that transfer has a negligible impact on competition outcomes. We tested the model empirically using a transmissible plasmid encoding colicin E2, a potent antibacterial toxin produced by Escherichia coli. As predicted by the model, we find that toxin plasmid transfer is feasible during warfare, but the resulting transconjugants remain rare. However, exploring the model further reveals realistic conditions where transfer is predicted to have major impacts. Specifically, the model predicts that whenever competing strains have access to unique nutrients, transconjugants can proliferate and reach high abundances. In support of these predictions, short- and long-term experiments show that transconjugants can thrive when nutrient competition is relaxed. Our work shows how horizontal gene transfer can reshape bacterial warfare in a way that benefits a weapon gene and strains that receive it. Interestingly, we also find that there is little cost to a strain that transfers a weapon gene, which is expected to further enable the horizontal gene transfer of molecular weapons.
细菌通常会使用分子武器来杀死或抑制竞争对手。编码许多此类武器及其相关免疫机制的基因能够进行水平转移。这些转移事件颇为引人注目，因为当这些基因被转移到竞争菌株中时，似乎会削弱细菌武器的作用。在此，我们构建了一个细菌战争的生态模型，以了解水平基因转移的影响。我们的模型预测，武器基因从攻击者转移到目标菌株是有可能的，但通常发生率较低，以至于这种转移对竞争结果的影响可以忽略不计。我们使用一个编码大肠杆菌产生的强效抗菌毒素——大肠杆菌素E2的可转移性质粒，对该模型进行了实证检验。正如模型所预测的，我们发现在战争期间毒素质粒转移是可行的，但由此产生的接合子仍然很少见。然而，对该模型的进一步探究揭示了一些现实条件，在这些条件下预计转移会产生重大影响。具体而言，该模型预测，只要竞争菌株能够获取独特的营养物质，接合子就能够增殖并达到高丰度。为支持这些预测，短期和长期实验表明，当营养竞争缓和时，接合子能够蓬勃生长。我们的研究表明水平基因转移如何能够以一种有利于武器基因及接收该基因的菌株的方式重塑细菌战争。有趣的是，我们还发现转移武器基因的菌株几乎没有成本，这预计会进一步促进分子武器的水平基因转移。
