Two novel temperate bacteriophages infecting Streptococcus pyogenes: Their genomes, morphology and stability

Harhala, Marek; Barylski, Jakub; Humińska-Lisowska, Kinga; Lecion, Dorota; Wojciechowicz, Jacek; Lahutta, Karolina; Kus, Mateja; Kropinski, Andrew M.; Nowak, Sylwia; Nowicki, Grzegorz; Hodyra-Stefaniak, Katarzyna; Dąbrowska, Krystyna

doi:10.1371/journal.pone.0205995

Cited by 14 publications

(12 citation statements)

References 40 publications

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“…Bacteriophages from groups D and G were relative to S. agalactiae phages LF2 and LF4 [ 20 ]. Group E bacteriophages were similar to S. agalactiae phage LF3 [ 20 ] and S. pyogenes phage Str03 [ 43 ] ( Figure 2 A; Table S4 ).…”

Section: Resultsmentioning

confidence: 99%

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Lichvariková

Šoltýs

Szemes

et al. 2020

Viruses

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Streptococcus agalactiae (group B Streptococcus, GBS) represents a leading cause of invasive bacterial infections in newborns and is also responsible for diseases in older and immunocompromised adults. Prophages represent an important factor contributing to the genome plasticity and evolution of new strains. In the present study, prophage content was analyzed in human GBS isolates. Thirty-seven prophages were identified in genomes of 20 representative sequenced strains. On the basis of the sequence comparison, we divided the prophages into eight groups named A–H. This division also corresponded to the clustering of phage integrase, even though several different integration sites were observed in some relative prophages. Next, PCR method was used for detection of the prophages in 123 GBS strains from adult hospitalized patients and from pregnancy screening. At least one prophage was present in 105 isolates (85%). The highest prevalence was observed for prophage group A (71%) and satellite prophage group B (62%). Other groups were detected infrequently (1–6%). Prophage distribution did not differ between clinical and screening strains, but it was unevenly distributed in MLST (multi locus sequence typing) sequence types. High content of full-length and satellite prophages detected in present study implies that prophages could be beneficial for the host bacterium and could contribute to evolution of more adapted strains.

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Section: Resultsmentioning

confidence: 99%

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Lichvariková

Šoltýs

Szemes

et al. 2020

Viruses

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“…2a . At the right of the end of prophage, there is a CDS encoding enolase (depicted as a green arrow), which is a surface-exposed adhesion protein of Streptococcus suggested to be a phage receptor or to interact with proteins of phages 33 . The aligned viral sequence in the IMG/VR v2.0 database encoded 14 CDSs, but its taxonomic classification using CAT was impossible.…”

Section: Resultsmentioning

confidence: 99%

Long-read metagenomics using PromethION uncovers oral bacteriophages and their interaction with host bacteria

et al. 2021

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Bacteriophages (phages), or bacterial viruses, are very diverse and highly abundant worldwide, including as a part of the human microbiomes. Although a few metagenomic studies have focused on oral phages, they relied on short-read sequencing. Here, we conduct a long-read metagenomic study of human saliva using PromethION. Our analyses, which integrate both PromethION and HiSeq data of >30 Gb per sample with low human DNA contamination, identify hundreds of viral contigs; 0–43.8% and 12.5–56.3% of the confidently predicted phages and prophages, respectively, do not cluster with those reported previously. Our analyses demonstrate enhanced scaffolding, and the ability to place a prophage in its host genomic context and enable its taxonomic classification. Our analyses also identify a Streptococcus phage/prophage group and nine jumbo phages/prophages. 86% of the phage/prophage group and 67% of the jumbo phages/prophages contain remote homologs of antimicrobial resistance genes. Pan-genome analysis of the phages/prophages reveals remarkable diversity, identifying 0.3% and 86.4% of the genes as core and singletons, respectively. Furthermore, our study suggests that oral phages present in human saliva are under selective pressure to escape CRISPR immunity. Our study demonstrates the power of long-read metagenomics utilizing PromethION in uncovering bacteriophages and their interaction with host bacteria.

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“…Bacteriophage Pf4, which has as a host Pseudomonas aeruginosa strain PAO1, was able to be converted into a superinfective form, producing plaques on its host’s bacterial lawn circumventing Pf4-mediated immunity (Rice et al, 2009). More recently it was reported that bacteriophages Str01 and Str03 were spontaneously released from Streptococcus pyogenes PCM 2855 and that very strain was subsequently used as their host for propagation (Harhala et al, 2018). In this case the authors examined whether the phages were prophages from the host bacteria but could not confirm their presence in the bacterial genome either by PCR or following whole genome sequencing of the host, suggesting that these were more likely environmental viruses that contaminated the original sample.…”

Section: Resultsmentioning

confidence: 99%

Characterization of a Highly Virulent Edwardsiella anguillarum Strain Isolated From Greek Aquaculture, and a Spontaneously Induced Prophage Therein

et al. 2019

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Edwardsiella-associated outbreaks are increasingly reported on both marine and freshwater aquaculture setups, accounting for severe financial and biomass losses. E. tarda, E. ictaluri, and E. hoshinae have been the traditional causative agents of edwardsiellosis in aquaculture, however, intensive studies due to the significance of the disease have just recently revealed two more species, E. piscicida and E. anguillarum. Whole genome sequencing that was conducted on the strain EA011113, isolated from farmed Diplodus puntazzo after an edwardsiellosis outbreak in Greece, confirmed it as a new clinical strain of E. anguillarum. Extensive phylogenetic analysis showed that this Greek strain is closely related to an Israeli E. piscicida-like clinical strain, isolated from diseased groupers, Epinephelus aeneus and E. marginatus in Red Sea. Bioinformatic analyses of E. anguillarum strain EA011113 unveiled a wide repertoire of potential virulence factors, the effect of which was corroborated by the mortalities that the strain induced in adult zebrafish, Danio rerio, under different levels of infection intensity (LD50 after 48 h: 1.85 × 104 cfu/fish). This strain was non-motile and according to electron microscopy lacked flagella, a fact that is not typical for E. anguillarum. Comparative genomic analysis revealed a deletion of 36 nt found in the flagellar biosynthetic gene (FlhB) that could explain that trait. Further in silico analysis revealed an intact prophage that was integrated in the bacterial genome. Following spontaneous induction, the phage was isolated, purified, characterized and independently sequenced, confirming its viability as a free, inducible virion as well. Separate genomic analysis of the prophage implies a plausible case of lysogenic conversion. Focusing on edwardsiellosis as a rapidly emerging aquaculture disease on a global scale, this work offers some insight into the virulence, fitness, and potential lysogenic conversion of a of a newly described, yet highly pathogenic, strain of E. anguillarum.

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Two novel temperate bacteriophages infecting Streptococcus pyogenes: Their genomes, morphology and stability

Cited by 14 publications

References 40 publications

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Characterization of Clinical and Carrier Streptococcus agalactiae and Prophage Contribution to the Strain Variability

Long-read metagenomics using PromethION uncovers oral bacteriophages and their interaction with host bacteria

Characterization of a Highly Virulent Edwardsiella anguillarum Strain Isolated From Greek Aquaculture, and a Spontaneously Induced Prophage Therein

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