Coevolution between Staphylococcus aureus isolated from mastitic milk and its lytic bacteriophage ΦSA012 in batch co-culture with serial transfer

Osada, Keita; Takeuchi, Ippei; Miyanaga, Kazuhiko; Tanji, Yasunori

doi:10.1016/j.bej.2017.06.022

Cited by 14 publications

(14 citation statements)

References 34 publications

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“…Hence, the mutation that we observed in this gene is 461 likely to be involved in the inhibition of phage DNA transcription. This finding is supported by a 462 previous observation (Osada et al 2017) that SA003R11 resists phage infection not only by 463…”

Section: Artificial Deletion Of Tars Gene In Sa003 Significantly Redusupporting

confidence: 65%

“…The phenotype as a result of coevolutionary adaptation of host and phage has previously 80 been observed and explained in our previous report (Takeuchi et al 2016;Osada et al 2017). In 81 this study, we focused on genetic analysis of the host cell by whole genome sequencing (WGS).…”

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confidence: 66%

“…we demonstrated the coevolution of S. aureus SA003 and phage ɸSA012 during their long-term 74 co-culture (Osada et al 2017). We observed cumulative development of phage resistance of the 75 host and corresponding infectivity of the phages during this coevolution (Osada et al 2017). The 76 coevolution of S. aureus and phage is unique and should be taken into account when considering 77 the result of clinical trials.…”

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confidence: 74%

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Analysis of phage-resistant mechanisms inStaphylococcus aureusSA003 reveals a different binding mechanism for the closely related Twort-like phages ϕSA012 and ϕSA039

Azam

Hoshiga

Takeuchi

et al. 2018

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We have previously generated strains of Staphylococcus aureus SA003 resistant to its specific phage ϕSA012 through long-term coevolution experiment. However, the DNA mutations responsible for the phenotypic change of phage resistance are unknown. Whole-genome analysis revealed six genes that acquired unique point mutations: five missense mutations and one nonsense mutation. Moreover, one deletion, 1.779-bp, resulted in the deletion of the genes encoding glycosyltransferase, TarS, and iron-sulfure repair protein, ScdA. The deletion occurred from the second round of coculture (SA003R2) and remained through the last round. The ϕSA012 infection toward SA003R2 had decreased to 79.77±7.50% according to plating efficiency. Complementation of the phage-resistant strain by the wild-type allele showed two mutated host genes were linked to the inhibition of post-adsorption, and five genes were linked to phage adsorption of ϕSA012. Unlike ϕSA012, infection by ϕSA039, a close relative of ϕSA012, onto SA003R2 was impaired drastically. Complementation of SA003R2 by wild-type tarS restores the infectivity of ϕSA039. Thus, we concluded that ϕSA039 requires β-GlcNAc in Wall Teichoic Acid (WTA) for its binding. In silico analysis of the ϕSA039 genome revealed that several proteins in the tail and baseplate region were different from ϕSA012; notably the partial deletion of orf96 of ϕSA039, a homolog of orf99 of ϕSA012. Orf100 of ϕSA039, a homolog of Orf103 of ϕSA012, a previously reported receptor binding protein (RBP), had low similarity (86%) to that of ϕSA012. The difference in tail and baseplate proteins might be the factor for specificity difference between ϕSA012 and ϕSA039.

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Section: Artificial Deletion Of Tars Gene In Sa003 Significantly Redusupporting

confidence: 65%

mentioning

confidence: 66%

mentioning

confidence: 74%

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Analysis of phage-resistant mechanisms inStaphylococcus aureusSA003 reveals a different binding mechanism for the closely related Twort-like phages ϕSA012 and ϕSA039

Azam

Hoshiga

Takeuchi

et al. 2018

Preprint

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“…A one-step growth curve was constructed to determine the phage's burst size and latent period as previously described, with modification (66). Briefly, the phage was added to refreshed overnight culture of P. aeruginosa PAO1 (OD660nm =1) at multiplicity of infection (MOI) 0.01, and incubated at 37°C for 10 minutes, with shaking at 120 rpm.…”

Section: Characterization Of Phage Growth and Determination Of Phage mentioning

confidence: 99%

Characterization of Pseudomonas lytic phages and their application as a cocktail with antibiotics in controlling Pseudomonas aeruginosa

Ong

Azam

Sasahara

et al. 2020

Journal of Bioscience and Bioengineering

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“…In addition, a previous study showed that kayviruses such as ɸSA012 and ɸK have at least two RBPs (RBP1 and RBP2), which are responsible for these phages’ broad host range (O’Flaherty et al 2004; Takeuchi et al 2016). Mutant ɸSA012 has a modified RBP2 (ORF103) that enables the phage to infect mutant S. aureus SA003R38, which has an altered WTA and overproduces capsular polysaccharide (Takeuchi et al 2016; Osada et al 2017; Azam et al 2018), indicating that mutated RBP2 may allow the phage to counter-adapt to resistant hosts by using an alternative component as a novel receptor (Takeuchi et al 2016). Like ɸSA012, ɸSA039 also has two RBPs, RBP1 (ORF100) and RBP2 (ORF102) (Azam et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Analysis host-recognition mechanism of staphylococcal kayvirus ɸSA039 reveals a novel strategy that protects Staphylococcus aureus against infection by Staphylococcus pseudintermedius Siphoviridae phages

Azam

Kadoi

Miyanaga

et al. 2019

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1 reveals a novel strategy that protects Staphylococcus aureus against infection 2 by Staphylococcus pseudintermedius Siphoviridae phages 3 4 5 6 Abstract 21Following the emergence of antibiotic resistant bacteria such as methicillin-resistant 22 Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius 23 (MRSP), phage therapy has attracted significant attention as an alternative to antibiotic 24 treatment. Bacteriophages belonging to kayvirus (previously known as Twort-like phages) have 25 broad host range and are strictly lytic in Staphylococcus spp. Previous work revealed that 26 kayvirus ɸSA039 has a host-recognition mechanism distinct from those of other known 27 kayviruses: most of kayviruses use the backbone of wall teichoic acid (WTA) as their receptor; 28 by contrast, ɸSA039 uses the β-N-acetylglucosamine (β-GlcNAc) residue in WTA. In this study, 29 we found that ɸSA039 could switch its receptor to be able to infect S. aureus lacking the β- 30 GlcNAc residue by acquiring a spontaneous mutation in open reading frame (ORF) 100 and 31 ORF102. Moreover, ɸSA039 could infect S. pseudintermedius, which has a different WTA 32 structure than S. aureus. By comparison with newly isolated S. pseudintermedius-specific phage 33 (SP phages), we determined that glycosylation in WTA of S. pseudintermedius is essential for 34 adsorption of SP phages, but not ɸSA039. Finally, we describe a novel strategy of S. aureus 35 which protects the bacteria from infection of SP phages. Notably, glycosylation of ribitol 36 phosphate (RboP) WTA by TarM or/and TarS prevents infection of S. aureus by SP phages. 37 These findings could help to establish a new strategy for treatment of S. aureus and S. 38 pseudintermedius infection, as well as provide valuable insights into the biology of phage-host 39 interactions. 40 Keyword: Kayvirus, phage therapy, host-recognition mechanism, Staphylococcus 41 pseudintermedius, Staphylococcus aureus 42 43Staphylococcus is a Gram-positive bacterium that causes many kinds of infections. Two 45 representative species, S. aureus and S. pseudintermedius, are coagulase-positive bacteria that 46 are notoriously pathogenic in humans and animals (Kloos and Bannerman 1994; Pompilio et al. 47 2015). S. aureus is a commensal found on the skin and mucosae of humans, whereas S. 48 pseudintermedius commonly inhabits dog skin. Both are common bacterial pathogens associated 49 with chronic and recurrent skin infections that require long-term systemic antimicrobial therapy. 50Infection by S. aureus and S. pseudintermedius is becoming problematic due to the emergence of 51 antibiotic-resistant strains, including methicillin-resistant (MRSA and MRSP) and vancomycin-52 resistant strains (VRSA) (Enright et al. 2002; Sakoulas et al. 2005). Virulent bacteriophages that 53 can kill a wide range of S. aureus hosts represent promising alternatives to conventional 54 antibiotic treatment (Alves et al. 2014; Iwano et al. 2018; Azam and Tanji 2019a). The success 55 of p...

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Coevolution between Staphylococcus aureus isolated from mastitic milk and its lytic bacteriophage ΦSA012 in batch co-culture with serial transfer

Cited by 14 publications

References 34 publications

Analysis of phage-resistant mechanisms inStaphylococcus aureusSA003 reveals a different binding mechanism for the closely related Twort-like phages ϕSA012 and ϕSA039

Analysis of phage-resistant mechanisms inStaphylococcus aureusSA003 reveals a different binding mechanism for the closely related Twort-like phages ϕSA012 and ϕSA039

Characterization of Pseudomonas lytic phages and their application as a cocktail with antibiotics in controlling Pseudomonas aeruginosa

Analysis host-recognition mechanism of staphylococcal kayvirus ɸSA039 reveals a novel strategy that protects Staphylococcus aureus against infection by Staphylococcus pseudintermedius Siphoviridae phages

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