Biocidal Inactivation of Lactococcus lactis Bacteriophages: Efficacy and Targets of Commonly Used Sanitizers

Hayes, Stephen; Murphy, James M.; Mahony, Jennifer; Lugli, Gabriele Andrea; Ventura, Marco; Noben, Jean-Paul; Franz, Charles M. A. P.; Neve, Horst; Nauta, Arjen; Sinderen, Douwe van

doi:10.3389/fmicb.2017.00107

Cited by 28 publications

(24 citation statements)

References 48 publications

(65 reference statements)

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“…Significant effort has been invested toward understanding the adaptive responses of phages to host-encoded phage resistance systems in S. thermophilus, particularly with respect to clustered regularly interspaced palindromic repeat (CRISPR) immune systems (25)(26)(27). Studies of phage adaptive responses to thermal and chemical treatments have demonstrated the increasing insensitivity of phages of Lactococcus lactis, Lactobacillus delbrueckii, and S. thermophilus to such interventions, thus establishing the requirement for industrial strategies to overcome this issue (24,28,29).…”

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confidence: 99%

A Decade of Streptococcus thermophilus Phage Evolution in an Irish Dairy Plant

Lavelle

Murphy

Fitzgerald

et al. 2018

Appl Environ Microbiol

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Phages of present a major threat to the production of many fermented dairy products. To date, only a handful of studies have assessed the biodiversity of phages in dairy fermentations. In order to develop strategies to limit phage predation in this important industrial environment, it is imperative that such studies are undertaken and that phage-host interactions of this species are better defined. The present study investigated the biodiversity and evolution of phages within an Irish dairy fermentation facility over an eleven year period. This resulted in the isolation of 17 genetically distinct phages, all of which belong to the so-called group. Evolution of phages within the factory appears to be influenced by phages from other dairy plants introduced into the factory for whey protein powder production. Modular exchange, primarily within the regions encoding lysogeny and replication functions, was the major observation among the phages isolated between 2006 and 2016. Furthermore, the genotype of the first isolate in 2006 was observed continuously across the following decade highlighting the ability of these phages to prevail in the factory setting for extended periods of time. The proteins responsible for host recognition were analysed and carbohydrate binding domains (CBDs) were identified in the distal tail (Dit), the baseplate proteins and the Tail-associated lysin (Tal) variable regions (VR1 and VR2) of many isolates. This consolidates the notion that phages recognise a carbohydrate receptor on the cell surface of their host. Dairy fermentations are consistently threatened by the presence of bacterial viruses (bacteriophages or phages), which may lead to a reduction in acidification rates or even complete loss of the fermentate. These phages may persist in factories for long periods of time. The objective of the current study was to monitor the progression of phages infecting the dairy bacterium over a period of eleven years in an Irish dairy plant so as to understand how these phages evolve. A focused analysis of the genomic region that encodes host recognition functions highlighted that these proteins harbour a variety of carbohydrate binding domains, which corroborates the notion that phages of recognise carbohydrate receptors at the initial stages of the phage cycle.

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confidence: 99%

A Decade of Streptococcus thermophilus Phage Evolution in an Irish Dairy Plant

Lavelle

Murphy

Fitzgerald

et al. 2018

Appl Environ Microbiol

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“…To determine whether both RBP1 Phi4.2 and RBP2 Phi4.2 are expressed and incorporated into the mature phage particle, proteins of the Phi4.2 virion were analysed via ESI-MS/MS. Most of the predicted tail-associated proteins of Phi4.2, such as the major tail protein, the tail tape measure protein, the TpeX (tail protein extension) protein, and the receptor binding protein, were detected in this analysis, although phage capsid proteins were not identified (a phenomenon previously observed in a number of studies, and likely a result of covalent cross-linking of head components resulting in oligomers too large to enter the gel [44,45]). A significant number of peptide reads were obtained for both RBP1 Phi4.2 (13 unique reads covering 51% of the amino acid sequence) and RBP2 Phi4.2 (8 unique reads covering 39% of the amino acid sequence), indicating both are indeed expressed and apparently incorporated into the phage particle (Figure 3B).…”

Section: Resultsmentioning

confidence: 77%

Identification of Dual Receptor Binding Protein Systems in Lactococcal 936 Group Phages

Hayes

Duhoo

Neve

et al. 2018

Viruses

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Siphoviridae of the lactococcal 936 group are the most commonly encountered bacteriophages in the dairy processing environment. The 936 group phages possess a discrete baseplate at the tip of their tail—a complex harbouring the Receptor Binding Protein (RBP) which is responsible for host recognition and attachment. The baseplate-encoding region is highly conserved amongst 936 phages, with 112 of 115 publicly available phages exhibiting complete synteny. Here, we detail the three exceptions (Phi4.2, Phi4R15L, and Phi4R16L), which differ from this genomic architecture in possessing an apparent second RBP-encoding gene upstream of the “classical” rbp gene. The newly identified RBP possesses an elongated neck region relative to currently defined 936 phage RBPs and is genetically distinct from defined 936 group RBPs. Through detailed characterisation of the representative phage Phi4.2 using a wide range of complementary techniques, we demonstrated that the above-mentioned three phages possess a complex and atypical baseplate structure. Furthermore, the presence of both RBPs in the tail tip of the mature virion was confirmed, while the anticipated host-binding capabilities of both proteins were also verified.

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“…One of the aspects explored here is the susceptibility of phiIPLA-RODI to four disinfectants with different chemical structures. To date, most information regarding phage susceptibility to disinfectants has been gathered for phages infecting lactic acid bacteria (LAB), which are a problem in the dairy industry [ 6 , 7 ]. Conversely, information on the efficacy of commonly used biocides against phages that inactivate bacterial pathogens is scarce.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, QACs and oxidizing agents were the most effective against several LAB phages [ 6 ]. In another study, the most effective biocide against lactococcal phages was benzalkonium chloride followed by hydrogen peroxide, whereas other biocides were only active against some phages [ 7 ]. Despite the apparent trends of certain disinfectants to be more effective for the inactivation of bacteriophages, it does seem evident that this is a property that needs to be examined for each phage with antimicrobial potential.…”

Section: Discussionmentioning

confidence: 99%

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Study of the Interactions Between Bacteriophage phiIPLA-RODI and Four Chemical Disinfectants for the Elimination of Staphylococcus aureus Contamination

Agún

Fernández

González-Menéndez

et al. 2018

Viruses

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Bacteriophages are currently considered as a promising alternative to antibiotics and disinfectants. However, the use of phages in different clinical and industrial settings will involve their exposure to other disinfectants. As a result, the outcome of the phage treatment will depend on two aspects derived from such interactions. On the one hand, the susceptibility of the phage to disinfectants at the concentrations used for disinfection and at lower residual concentrations needs to be determined. Additionally, the existence of synergistic or antagonistic interactions between phages and disinfectants would also affect the potential success of phage biocontrol applications. Here, we tested these effects for the antistaphylococcal phage phiIPLA-RODI by using four different disinfectants: benzalkonium chloride, triclosan, chlorhexidine and hydrogen peroxide. Our results highlight the differences between disinfectants regarding their effect on phage survival and antimicrobial properties. For instance, our data suggests that, out of the four disinfectants used, benzalkonium chloride would be the most adequate to use in settings where phages are to be applied. Nonetheless, this preliminary analysis grants the need for further studies with a larger number of disinfectants for the development of a phiIPLA-RODI-based product.

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Biocidal Inactivation of Lactococcus lactis Bacteriophages: Efficacy and Targets of Commonly Used Sanitizers

Cited by 28 publications

References 48 publications

A Decade of Streptococcus thermophilus Phage Evolution in an Irish Dairy Plant

A Decade of Streptococcus thermophilus Phage Evolution in an Irish Dairy Plant

Identification of Dual Receptor Binding Protein Systems in Lactococcal 936 Group Phages

Study of the Interactions Between Bacteriophage phiIPLA-RODI and Four Chemical Disinfectants for the Elimination of Staphylococcus aureus Contamination

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