In silico analysis of
            <scp>AHJD</scp>
            ‐like viruses,
            <i>Staphylococcus aureus</i>
            phages S24‐1 and S13′, and study of phage S24‐1 adsorption

Uchiyama, Jumpei; Takemura‐Uchiyama, Iyo; Kato, Shin‐ichiro; Sato, M.; Ujihara, Takako; Matsui, Hidehito; Hanaki, Hideaki; Daibata, Masanori; Matsuzaki, Shigenobu

doi:10.1002/mbo3.166

Cited by 14 publications

(13 citation statements)

References 44 publications

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“…For instance, S. aureus Podoviridae phage S13′ and S24-1 have been revealed to exhibit different binding capacity to WTAs harboring different glycosidic patterns. The putative receptor-binding protein (RBP) of S13′ requires β-O-GlcNAc for binding, while that of S24-1 can bind regardless of glycosidic bonds, which makes WTA itself the receptor for S24-1 [22,23]. BLAST analysis of the CSA13 genome revealed a gene-encoding putative RBP of CSA13, and its amino acid sequence was compared with that of S13′ and S24-1 (Figure S1).…”

Section: Resultsmentioning

confidence: 99%

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Characterization and Genome Analysis of Staphylococcus aureus Podovirus CSA13 and Its Anti-Biofilm Capacity

Cha

Chun

Son

et al. 2019

Viruses

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Staphylococcus aureus is one of the notable human pathogens that can be easily encountered in both dietary and clinical surroundings. Among various countermeasures, bacteriophage therapy is recognized as an alternative method for resolving the issue of antibiotic resistance. In the current study, bacteriophage CSA13 was isolated from a chicken, and subsequently, its morphology, physiology, and genomics were characterized. This Podoviridae phage displayed an extended host inhibition effect of up to 23 h of persistence. Its broad host spectrum included methicillin susceptible S. aureus (MSSA), methicillin resistant S. aureus (MRSA), local S. aureus isolates, as well as non-aureus staphylococci strains. Moreover, phage CSA13 could successfully remove over 78% and 93% of MSSA and MRSA biofilms in an experimental setting, respectively. Genomic analysis revealed a 17,034 bp chromosome containing 18 predicted open reading frames (ORFs) without tRNAs, representing a typical chromosomal structure of the staphylococcal Podoviridae family. The results presented here suggest that phage CSA13 can be applicable as an effective biocontrol agent against S. aureus.

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Section: Resultsmentioning

confidence: 99%

“…2.7.000) [21]. The potential receptor for CSA13 was predicted based on the receptors for S13′ and S24-1 [22,23]. To verify the predicted receptor, S. aureus RN4220 [24] was used (Table 1).…”

Section: Methodsmentioning

confidence: 99%

Characterization and Genome Analysis of Staphylococcus aureus Podovirus CSA13 and Its Anti-Biofilm Capacity

Cha

Chun

Son

et al. 2019

Viruses

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“…Eleven of the phiAGO1.3 proteins are virion components, as identified by a mass spectrometry analysis of tryptic peptides of whole virions (Supplementary Table 3). Homologs of nine of them, including the major capsid protein, two tail proteins, lower and upper collar protein, RBP and tail amidase, have been identified or predicted previously as virion proteins of related phages (Vybiral et al, 2003; Takemura-Uchiyama et al, 2013; Uchiyama et al, 2014; Štveráková et al, 2018). The two additional virion proteins of phiAGO1.3 identified in this work (ORF01 and ORF07) are present in virions in a small amount as suggested by the small number of their peptides in analyzed samples (Supplementary Table 3).…”

Section: Resultsmentioning

confidence: 99%

The Ability of Lytic Staphylococcal Podovirus vB_SauP_phiAGO1.3 to Coexist in Equilibrium With Its Host Facilitates the Selection of Host Mutants of Attenuated Virulence but Does Not Preclude the Phage Antistaphylococcal Activity in a Nematode Infection Model

Głowacka-Rutkowska¹,

Gozdek²,

Empel³

et al. 2019

Front. Microbiol.

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Phage vB_SauP_phiAGO1.3 (phiAGO1.3) is a polyvalent Staphylococcus lytic podovirus with a 17.6-kb genome (Gozdek et al., 2018). It can infect most of the Staphylococcus aureus human isolates of dominant clonal complexes. We show that a major factor contributing to the wide host range of phiAGO1.3 is a lack or sparcity of target sites for certain restriction-modification systems of types I and II in its genome. Phage phiAGO1.3 requires for adsorption β-O-GlcNAcylated cell wall teichoic acid, which is also essential for the expression of methicillin resistance. Under certain conditions an exposure of S. aureus to phiAGO1.3 can lead to the establishment of a mixed population in which the bacteria and phages remain in equilibrium over multiple generations. This is reminiscent of the so called phage carrier state enabling the co-existence of phage-resistant and phage-sensitive cells supporting a continuous growth of the bacterial and phage populations. The stable co-existence of bacteria and phage favors the emergence of phage-resistant variants of the bacterium. All phiAGO1.3-resistant cells isolated from the phage-carrier-state cultures contained a mutation inactivating the two-component regulatory system ArlRS, essential for efficient expression of numerous S. aureus virulence-associated traits. Moreover, the mutants were unaffected in their susceptibility to infection with an unrelated, polyvalent S. aureus phage of the genus Kayvirus. The ability of phiAGO1.3 to establish phage-carrier-state cultures did not preclude its antistaphylococcal activity in vivo in an S. aureus nematode infection model. Taken together our results suggest that phiAGO1.3 could be suitable for the therapeutic application in humans and animals, alone or in cocktails with Kayvirus phages. It might be especially useful in the treatment of infections with the majority of methicillin-resistant S. aureus strains.

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“…Immunoelectron microscopy was conducted as described previously (23). A freshly purified phage sample (10 10 PFU/ml) was mixed with purified anti-ORF103 antibody diluted in SM buffer (1:100) and incubated at room temperature for 30 min.…”

Section: Methodsmentioning

confidence: 99%

“…To date, RBPs have been identified for Bacillus subtilis phages SPP1 and 29, Streptococcus thermophilus phages DT1 and MD4, Lactococcus lactis phages bIL67 and CHL92 of the c2 species, sk1, bIL170, and p2 of the 936 species, and TP901-1 and Tuc2009 of the P335 species, and Listeria phage A118 (13)(14)(15)(16)(17)(18)(19)(20)(21)(22). Among S. aureus phages, RBPs have also been identified in Siphoviridae phage SLT and Podoviridae AHJD-like phages S24-1 and S13= (23,24). Remarkably, Habann et al identified that the RBPs of Listeria phage A511 and staphylococcal Twort-like phages ISP and Twort (Gp108, gp40, and gp17, respectively) are located in short tail fibers (25).…”

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confidence: 99%

The Presence of Two Receptor-Binding Proteins Contributes to the Wide Host Range of Staphylococcal Twort-Like Phages

Takeuchi

Osada

Azam

et al. 2016

Appl Environ Microbiol

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Thanks to their wide host range and virulence, staphylococcal bacteriophages (phages) belonging to the genus Twortlikevirus (staphylococcal Twort-like phages) are regarded as ideal candidates for clinical application for Staphylococcus aureus infections due to the emergence of antibiotic-resistant bacteria of this species. To increase the usability of these phages, it is necessary to understand the mechanism underlying host recognition, especially the receptor-binding proteins (RBPs) that determine host range. In this study, we found that the staphylococcal Twort-like phage ⌽SA012 possesses at least two RBPs. Genomic analysis of five mutant phages of ⌽SA012 revealed point mutations in orf103, in a region unique to staphylococcal Twort-like phages. Phages harboring mutated ORF103 could not infect S. aureus strains in which wall teichoic acids (WTAs) are glycosylated with ␣-N-acetylglucosamine (␣-GlcNAc). A polyclonal antibody against ORF103 also inhibited infection by ⌽SA012 in the presence of ␣-GlcNAc, suggesting that ORF103 binds to ␣-GlcNAc. In contrast, a polyclonal antibody against ORF105, a short tail fiber component previously shown to be an RBP, inhibited phage infection irrespective of the presence of ␣-GlcNAc. Immunoelectron microscopy indicated that ORF103 is a tail fiber component localized at the bottom of the baseplate. From these results, we conclude that ORF103 binds ␣-GlcNAc in WTAs, whereas ORF105, the primary RBP, is likely to bind the WTA backbone. These findings provide insight into the infection mechanism of staphylococcal Twort-like phages. IMPORTANCE Staphylococcus phages belonging to the genus Staphylococcus aureus, a Gram-positive coccus, is a commensal and pathogenic bacterium that causes opportunistic infections in humans and animals. Currently, antibiotic resistance in this species poses a threat to public health. Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of hospital-acquired infections around the world (1). The emergence of such antibiotic-resistant bacteria requires development of alternatives to antibiotic-based therapies. One promising alternative is phage therapy, in which bacteriophages (phages) are used to treat bacterial infections (2, 3). In preclinical trials performed in mice, S. aureus infections (including MRSA infections) were successfully treated by use of phages (4). Therefore, phage therapy has attracted great interest as an alternative to antibiotics.Previously, we isolated the virulent staphylococcal phage ⌽SA012, which exerts lytic effects on a wide range of S. aureus isolates from bovine mastitis cases (5). Genomic analysis of ⌽SA012 revealed that it belongs to the genus Twortlikevirus, which contains the Staphylococcus phages Twort, K, and G, whereas the genus SPO1likevirus contains the Bacillus phage SPO1 as well as Listeria phages P100 and A511. Lactobacillus phage LP65 and Enterococcus phage ⌽EF24C were classified as orphans within the subfamily (6). Representatives of the two genera share the following features: they (i) hav...

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In silico analysis of AHJD ‐like viruses, Staphylococcus aureus phages S24‐1 and S13′, and study of phage S24‐1 adsorption

Cited by 14 publications

References 44 publications

Characterization and Genome Analysis of Staphylococcus aureus Podovirus CSA13 and Its Anti-Biofilm Capacity

Characterization and Genome Analysis of Staphylococcus aureus Podovirus CSA13 and Its Anti-Biofilm Capacity

The Ability of Lytic Staphylococcal Podovirus vB_SauP_phiAGO1.3 to Coexist in Equilibrium With Its Host Facilitates the Selection of Host Mutants of Attenuated Virulence but Does Not Preclude the Phage Antistaphylococcal Activity in a Nematode Infection Model

The Presence of Two Receptor-Binding Proteins Contributes to the Wide Host Range of Staphylococcal Twort-Like Phages

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