How Broad Is Enough: The Host Range of Bacteriophages and Its Impact on the Agri-Food Sector

Fong, Karen; Wong, Catherine W. Y.; Wang, Siyun; Delaquis, Pascal

doi:10.1089/phage.2020.0036

Cited by 22 publications

(11 citation statements)

References 105 publications

(134 reference statements)

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“…Collectively, phages are the main global predators of bacteria. However, individual phages tend to have narrow host ranges, often not even encompassing entire bacterial species; even when phages are found to infect taxonomically diverse bacteria, they typically do not infect broadly within those bacterial groups [ 1 , 2 , 3 , 4 , 5 ], and the diversity of bacterial anti-phage defense mechanisms virtually ensures an absence of systematically broad host ranges [ 6 ].…”

Section: Introductionmentioning

confidence: 99%

Modeling the Directed Evolution of Broad Host Range Phages

2022

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Background: The host ranges of individual phages tend to be narrow, yet many applications of phages would benefit from expanded host ranges. Empirical methods have been developed to direct the evolution of phages to attack new strains, but the methods have not been evaluated or compared for their consequences. In particular, how do different methods favor generalist (broad host range) phages over specialist phages? All methods involve exposing phages to two or more novel bacterial strains, but the methods differ in the order in which those hosts are presented through time: Parallel presentation, Sequential presentation, and Mixed presentation. Methods: We use a combination of simple analytical methods and numerical analyses to study the effect of these different protocols on the selection of generalist versus specialist phages. Results: The three presentation protocols have profoundly different consequences for the evolution of generalist versus specialist phages. Sequential presentation favors generalists almost to the exclusion of specialists, whereas Parallel presentation does the least so. However, other protocol attributes (the nature of dilution between transfers of phages to new cultures) also have effects on selection and phage maintenance. It is also noted that protocols can be designed to enhance recombination to augment evolution and to reduce stochastic loss of newly arisen mutants.

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Section: Introductionmentioning

confidence: 99%

Modeling the Directed Evolution of Broad Host Range Phages

2022

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“…The six phages displayed different host ranges, indicating that they are distinct from one another. Host range is largely dependent on the ability of phages to bind to either a single receptor (i.e., narrow host range) or multiple different receptors (i.e., broad host range; Fong et al, 2021 ). Φ206, ΦMont, and Φ13314 showed very narrow host ranges, infecting only one or two tested Salmonella strains.…”

Section: Resultsmentioning

confidence: 99%

“…Host range is critical in the selection of phage candidates for biocontrol agents and detection applications. To be considered as excellent candidates for use as biocontrol agents in foods, phages should be strictly lytic and possibly have a broad host range ( Sharma et al, 2017 ; Fong et al, 2021 ; Picozzi et al, 2021 ). Since ΦEnt exhibited the broadest and unusual host range, formed clear plaques (possibly with high lytic activity), and had higher efficiency of plating (EOP) (data not shown), it was selected for further characterization of (with respect to) its growth kinetics, restriction pattern, and lytic profiles in model food systems and for determining its thermal stability.…”

Section: Resultsmentioning

confidence: 99%

Bacteriophages Isolated From Turkeys Infecting Diverse Salmonella Serovars

Marchant

Thompson

et al. 2022

Front. Microbiol.

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Salmonella is one of the leading causes of foodborne illnesses worldwide. The rapid emergence of multidrug-resistant Salmonella strains has increased global concern for salmonellosis. Recent studies have shown that bacteriophages (phages) are novel and the most promising antibacterial agents for biocontrol in foods because phages specifically kill target bacteria without affecting other bacteria, do not alter organoleptic properties or nutritional quality of foods, and are safe and environmentally friendly. Due to the vast variation in Salmonella serotypes, large numbers of different and highly virulent Salmonella phages with broad host ranges are needed. This study isolated 14 Salmonella phages from turkey fecal and cecal samples. Six phages (Φ205, Φ206, Φ207, ΦEnt, ΦMont, and Φ13314) were selected for characterization. These phages were from all three families in the Caudovirales order. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) revealed that each phage had a unique structural protein profile. Each phage had a distinct host range. Φ207 and ΦEnt are both siphophages. They shared eight hosts, including seven different Salmonella serovars and one Shigella sonnei strain. These two phages showed different restriction banding patterns generated through EcoRI or HindIII digestion, but shared three bands from EcoRI digestion. ΦEnt displayed the broadest and very unusual host range infecting 11 Salmonella strains from nine serovars and three Shigella strains from two species, and thus was further characterized. The one-step growth curve revealed that ΦEnt had a short latent period (10 min) and relatively large burst size (100 PFU/infected cell). ΦEnt and its host showed better thermal stabilities in tryptic soy broth than in saline at 63 or 72°C. In the model food system (cucumber juice or beef broth), ΦEnt infection [regardless of the multiplicity of infections (MOIs) of 1, 10, and 100] resulted in more than 5-log10 reduction in Salmonella concentration within 4 or 5 h. Such high lytic activity combined with its remarkably broad and unusual host range and good thermal stability suggested that ΦEnt is a novel Salmonella phage with great potential to be used as an effective biocontrol agent against diverse Salmonella serovars in foods.

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“…(2019) , revealed that most of the SNPs found on Pseudomonas after exposure to DSM3 were also on membrane receptor. Additionally, different studies report that mutation in LPS genes induces phage resistance to Salmonella ( Rivera et al., 2019 ; Fong et al., 2020 ). This indicates that the most described mechanism for phage resistance in coevolution assays represent modification of protein receptors or exopolysaccharide, similar to the results found here.…”

Section: Resultsmentioning

confidence: 99%

Long-Term Interactions of Salmonella Enteritidis With a Lytic Phage for 21 Days in High Nutrients Media

Barrón-Montenegro

Rivera²,

Serrano³

et al. 2022

Front. Cell. Infect. Microbiol.

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Salmonella spp. is a relevant foodborne pathogen with worldwide distribution. To mitigate Salmonella infections, bacteriophages represent an alternative to antimicrobials and chemicals in food animals and food in general. Bacteriophages (phages) are viruses that infect bacteria, which interact constantly with their host. Importantly, the study of these interactions is crucial for the use of phages as a mitigation strategy. In this study, experimental coevolution of Salmonella Enteritidis (S. Enteritidis) and a lytic phage was conducted in tryptic soy broth for 21 days. Transfer to fresh media was conducted daily and every 24 hours, 2 mL of the sample was collected to quantify Salmonella OD600 and phage titter. Additionally, time-shift experiments were conducted on 20 colonies selected on days 1, 12, and 21 to evaluate the evolution of resistance to past (day 1), present (day 12), and future (day 21) phage populations. The behavior of the dynamics was modeled and simulated with mathematical mass-action models. Bacteria and phage from days 1 and 21 were sequenced to determine the emergence of mutations. We found that S. Enteritidis grew for 21 days in the presence and absence of the phage and developed resistance to the phage from day 1. Also, the phage was also able to survive in the media for 21 days, however, the phage titer decreased in approx. 3 logs PFU/mL. The stability of the lytic phage population was consistent with the leaky resistance model. The time-shift experiments showed resistance to phages from day 1 of at least 85% to the past, present, and future phages. Sequencing of S. Enteritidis showed mutations in genes involved in lipopolysaccharide biosynthesis genes rfbP and rfbN at day 21. The phage showed mutations in the tail phage proteins responsible for recognizing the cell surface receptors. These results suggest that interactions between bacteria and phage in a rich resource media generate a rapid resistance to the infective phage but a fraction of the population remains susceptible. Interactions between Salmonella and lytic phages are an important component for the rational use of phages to control this important foodborne pathogen.

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How Broad Is Enough: The Host Range of Bacteriophages and Its Impact on the Agri-Food Sector

Cited by 22 publications

References 105 publications

Modeling the Directed Evolution of Broad Host Range Phages

Modeling the Directed Evolution of Broad Host Range Phages

Bacteriophages Isolated From Turkeys Infecting Diverse Salmonella Serovars

Long-Term Interactions of Salmonella Enteritidis With a Lytic Phage for 21 Days in High Nutrients Media

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