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A lipopolysaccharide-dependent phage infects a pseudomonad phytopathogen and can evolve to evade phage resistance.

ABSTRACT: Bacterial pathogens are major causes of crop diseases, leading to significant production losses. For instance, kiwifruit canker, caused by the phytopathogen Pseudomonas syringae pv. actinidiae (Psa), has posed a global challenge to kiwifruit production. Treatment with copper and antibiotics, whilst initially effective, is leading to the rise of bacterial resistance, requiring new biocontrol approaches. Previously, we isolated a group of closely related Psa phages with biocontrol potential, which represent environmentally sustainable antimicrobials. However, their deployment as antimicrobials requires further insight into their properties and infection strategy. Here, we provide an in-depth examination of the genome of ΦPsa374-like phages and show that they use lipopolysaccharides (LPS) as their main receptor. Through proteomics and cryo-electron microscopy of ΦPsa374, we revealed the structural proteome and that this phage possess a T = 9 capsid triangulation, unusual for myoviruses. Furthermore, we show that ΦPsa374 phage resistance arises in planta through mutations in a glycosyltransferase involved in LPS synthesis. Lastly, through in vitro evolution experiments we showed that phage resistance is overcome by mutations in a tail fibre and structural protein of unknown function in ΦPsa374. This study provides new insight into the properties of ΦPsa374-like phages that informs their use as antimicrobials against Psa.

SUBMITTER: Warring SL

PROVIDER: S-EPMC9796965 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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A lipopolysaccharide-dependent phage infects a pseudomonad phytopathogen and can evolve to evade phage resistance.

Warring Suzanne L SL Malone Lucia M LM Jayaraman Jay J Easingwood Richard A RA Rigano Luciano A LA Frampton Rebekah A RA Visnovsky Sandra B SB Addison Shea M SM Hernandez Loreto L Pitman Andrew R AR Lopez Acedo Elena E Kleffmann Torsten T Templeton Matthew D MD Bostina Mihnea M Fineran Peter C PC

Environmental microbiology 20220801 10

Bacterial pathogens are major causes of crop diseases, leading to significant production losses. For instance, kiwifruit canker, caused by the phytopathogen Pseudomonas syringae pv. actinidiae (Psa), has posed a global challenge to kiwifruit production. Treatment with copper and antibiotics, whilst initially effective, is leading to the rise of bacterial resistance, requiring new biocontrol approaches. Previously, we isolated a group of closely related Psa phages with biocontrol potential, which ...[more]

PMID: 35912527

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Project description:The spread of multidrug resistant and hypervirulent Klebsiella pneumoniae has recently increased. Phages have been considered alternatives for treating infections caused by tenacious pathogens. Our study describes a novel lytic Klebsiella phage, hvKpP3, and we obtained spontaneous mutants, hvKpP3R and hvKpP3R15, of hvKpLS8 strain that showing strong resistance to the lytic phage hvKpP3. Sequencing analysis showed that nucleotide-deletion mutations of the glycosyltransferase gene (GT) and wcaJ genes, located in the lipopolysaccharide (LPS) gene cluster and the capsular polysaccharide (CPS) gene cluster, respectively, led to phage resistance. The wcaJ mutation confers the inhibition of phage adsorption by affecting the synthesis of hvKpP3R15 capsular polysaccharide, indicating that the capsule is the main adsorption receptor for bacteriophage hvKpP3. Interestingly, the phage-resistant mutant hvKpP3R has a loss-of-function mutation in GT, which is responsible for lipopolysaccharide biosynthesis. This results in the loss of high-molecular weight lipopolysaccharide (HMW-LPS), and alteration of the lipopolysaccharide structure of the bacterial cell wall confers resistance to phages. In conclusion, our study provides a detailed description of phage hvKpP3 and provides new insights into phage resistance in K. pneumoniae. IMPORTANCE Multidrug-resistant (MDR) Klebsiella pneumoniae strains pose a particular threat to human health. Therefore, it is very important for us to isolate phage and overcome phage resistance. In this study, we isolated a novel phage belonging to the Myoviridae family, hvKpP3, that exhibited high lytic activity against K2 hypervirulent K. pneumoniae. We demonstrated the excellent stability of phage hvKpP3 through in vitro and in vivo experiments, indicating its potential as a candidate for future clinical phage therapy. Furthermore, we identified that loss of function in the glycotransferase gene (GT) caused the failure of HMW-LPS synthesis, leading to phage resistance, which provides new insights into phage resistance in K. pneumoniae.

Project description:Juveniles are typically less resistant (more susceptible) to infectious disease than adults, and this difference in susceptibility can help fuel the spread of pathogens in age-structured populations. However, evolutionary explanations for this variation in resistance across age remain to be tested.One hypothesis is that natural selection has optimized resistance to peak at ages where disease exposure is greatest. A central assumption of this hypothesis is that hosts have the capacity to evolve resistance independently at different ages. This would mean that host populations have (a) standing genetic variation in resistance at both juvenile and adult stages, and (b) that this variation is not strongly correlated between age classes so that selection acting at one age does not produce a correlated response at the other age.Here we evaluated the capacity of three wild plant species (Silene latifolia, S. vulgaris and Dianthus pavonius) to evolve resistance to their anther-smut pathogens (Microbotryum fungi), independently at different ages. The pathogen is pollinator transmitted, and thus exposure risk is considered to be highest at the adult flowering stage.Within each species we grew families to different ages, inoculated individuals with anther smut, and evaluated the effects of age, family and their interaction on infection.In two of the plant species, S. latifolia and D. pavonius, resistance to smut at the juvenile stage was not correlated with resistance to smut at the adult stage. In all three species, we show there are significant age × family interaction effects, indicating that age specificity of resistance varies among the plant families. Synthesis. These results indicate that different mechanisms likely underlie resistance at juvenile and adult stages and support the hypothesis that resistance can evolve independently in response to differing selection pressures as hosts age. Taken together our results provide new insight into the structure of genetic variation in age-dependent resistance in three well-studied wild host-pathogen systems.

Dataset Information

A lipopolysaccharide-dependent phage infects a pseudomonad phytopathogen and can evolve to evade phage resistance.

Publications

A lipopolysaccharide-dependent phage infects a pseudomonad phytopathogen and can evolve to evade phage resistance.

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