Marchi Jacopo, Minh Chau Nguyen Ngoc, Debarbieux Laurent, Weitz Joshua S
Department of Biology, University of Maryland, College Park, Maryland, United States of America.
Institut Pasteur, Université Paris Cité, CNRS UMR6047, Bacteriophage Bacterium Host, Paris, France.
PLoS Comput Biol. 2025 Feb 4;21(2):e1012793. doi: 10.1371/journal.pcbi.1012793. eCollection 2025 Feb.
Bacteriophage (or 'phage' - viruses that infect and kill bacteria) are increasingly considered as a therapeutic alternative to treat antibiotic-resistant bacterial infections. However, bacteria can evolve resistance to phage, presenting a significant challenge to the near- and long-term success of phage therapeutics. Application of mixtures of multiple phages (i.e., 'cocktails') has been proposed to limit the emergence of phage-resistant bacterial mutants that could lead to therapeutic failure. Here, we combine theory and computational models of in vivo phage therapy to study the efficacy of a phage cocktail, composed of two complementary phages motivated by the example of Pseudomonas aeruginosa facing two phages that exploit different surface receptors, LUZ19v and PAK_P1. As confirmed in a Luria-Delbrück fluctuation test, this motivating example serves as a model for instances where bacteria are extremely unlikely to develop simultaneous resistance mutations against both phages. We then quantify therapeutic outcomes given single- or double-phage treatment models, as a function of phage traits and host immune strength. Building upon prior work showing monophage therapy efficacy in immunocompetent hosts, here we show that phage cocktails comprised of phage targeting independent bacterial receptors can improve treatment outcome in immunocompromised hosts and reduce the chance that pathogens simultaneously evolve resistance against phage combinations. The finding of phage cocktail efficacy is qualitatively robust to differences in virus-bacteria interactions and host immune dynamics. Altogether, the combined use of theory and computational analysis highlights the influence of viral life history traits and receptor complementarity when designing and deploying phage cocktails in immunocompetent and immunocompromised hosts.
噬菌体(或“噬菌体”——感染并杀死细菌的病毒)越来越被视为治疗抗生素耐药性细菌感染的一种治疗选择。然而,细菌可以进化出对噬菌体的抗性,这对噬菌体治疗近期和长期的成功构成了重大挑战。有人提出应用多种噬菌体的混合物(即“鸡尾酒”)来限制可能导致治疗失败的噬菌体抗性细菌突变体的出现。在这里,我们结合体内噬菌体治疗的理论和计算模型,以铜绿假单胞菌面对两种利用不同表面受体的噬菌体LUZ19v和PAK_P1为例,研究由两种互补噬菌体组成的噬菌体鸡尾酒的疗效。正如在卢里亚-德尔布吕克波动试验中所证实的那样,这个典型例子可作为细菌极不可能同时产生针对两种噬菌体的抗性突变的情况的模型。然后,我们根据噬菌体特征和宿主免疫强度,对单噬菌体或双噬菌体治疗模型的治疗结果进行量化。基于先前在免疫健全宿主中显示单噬菌体治疗效果的工作,我们在此表明,由靶向独立细菌受体的噬菌体组成的噬菌体鸡尾酒可以改善免疫受损宿主的治疗结果,并降低病原体同时进化出对噬菌体组合的抗性的可能性。噬菌体鸡尾酒疗效的这一发现对于病毒-细菌相互作用和宿主免疫动态的差异在定性上是稳健的。总之,理论与计算分析的结合突出了在免疫健全和免疫受损宿主中设计和部署噬菌体鸡尾酒时病毒生活史特征和受体互补性的影响。