Analysis of the prophages carried by human infecting isolates provides new insight into the evolution of Group B Streptococcus species

Mee-Marquet, Nathalie van der; Diène, Seydina M.; Barberà, Laura; Courtier-Martinez, Luka; Lafont, L; Ouachée, A; Valentin, Anne-Sophie; Santos, Sandra Dos; Quentin, Roland; François, Patrice

doi:10.1016/j.cmi.2017.08.024

Cited by 23 publications

(59 citation statements)

References 26 publications

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“…Prophages that straddled two contigs were excluded from the phylogeny ( n = 16). Extracted prophages and 22 prophages identified by van der Mee-Marquet et al ( 2018 ) were manually inspected and curated with Geneious v2020.1.2 (Biomatters Ltd, https://www.geneious.com ). Sequences were reverse-complemented as needed to start with the integrase gene, and all integrase protein sequences were also stored separately.…”

Section: Methodsmentioning

confidence: 99%

“…In human isolates, a high prevalence of prophages has been associated with greater pathogenicity, particularly the ability to cause invasive infections (van der Mee-Marquet et al, 2006 ; Domelier et al, 2009 ; Salloum et al, 2010 , 2011 ). A number of these phages carry genes associated with virulence and host adaptation, suggesting that lysogeny (the process of integration of temperate bacteriophages into the bacterial genome as lysogenic prophages), may play an important role in the biological success of the strains (van der Mee-Marquet et al, 2018 ). Likewise, host adaptation of a cattle-associated lineage is thought to have been driven by the acquisition of mobile genetic content, including prophages (Richards et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

“…A typing scheme for prophages based on full-prophage sequence diversity and insertion sites has been proposed for GBS (van der Mee-Marquet et al, 2018 ), however, a classification scheme based on site-specific integrases had yet to be developed for this species. Such a scheme would enable the rapid screening of large batches of full and draft genome sequences for the presence of prophages (based on integrase amino-acid sequences) and would be less affected by genome fragmentation.…”

Section: Introductionmentioning

confidence: 99%

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Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus

2020

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Group B Streptococcus (GBS) is a gram-positive pathogen mainly affecting humans, cattle, and fishes. Mobile genetic elements play an important role in the evolution of GBS, its adaptation to host species and niches, and its pathogenicity. In particular, lysogenic prophages have been associated with a high virulence of certain strains and with their ability to cause invasive infections in humans. It is therefore important to be able to accurately detect and classify prophages in GBS genomes. Several bioinformatic tools for the identification of prophages in bacterial genomes are available on-line. However, genome searches for most of these programs are affected by the composition of their reference database. Lack of databases specific to GBS results in failure to recognize all prophages in the species. Additionally, performance of these programs is affected by genome fragmentation in the case of draft genomes, leading to underestimation of the number of phages. They also prove impractical when dealing with large genome datasets and they do not offer a quick way of classifying bacteriophages. We developed a GBS-specific method to screen genome assemblies for the presence of prophages and to classify them based on a reproducible typing scheme. This was achieved through an extensive search of a vast number of high-quality GBS sequences ( n = 572) originating from different host species and countries in order to build a database of phage integrase types, on which the scheme is based. The proposed typing scheme comprises 12 integration sites and sixteen prophage integrase types, including multiple subtypes per integration site and integrase genes that were not site-specific. Two putative phage-inducible chromosomal islands (PICI) and their insertion sites were also identified during the course of these analyses. Phages were common and diverse in all major clonal complexes associated with human disease and detected in isolates from every animal species and continent included in the study. This database will facilitate further work on the prevalence and role of prophages in GBS evolution, and identifies the roles of PICIs in GBS and of prophage in hypervirulent ST283 as areas for further research.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus

2020

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“…pyogenes 25,30 and S . agalactiae genomes 31 ; however, genus-wide analyses of the genomic diversity and population structure of streptococcal prophages have not yet been reported.…”

Section: Mainmentioning

confidence: 99%

Prophages and satellite prophages are widespread amongStreptococcusspecies and may play a role in pneumococcal pathogenesis

Javan

Ramos‐Sevillano

Akter

et al. 2018

Preprint

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Prophages (viral genomes integrated within a host bacterial genome) are abundant within the bacterial world and are of interest because they often confer various phenotypic traits to their hosts, such as by encoding genes that increase pathogenicity. Satellite prophages are ‘parasites of parasites’ that rely on the bacterial host and another helper prophage for survival. We analysed >1,300 genomes of 70 different Streptococcus species for evidence of prophages and identified nearly 800 prophages and satellite prophages, the majority of which are reported here for the first time. We show that prophages and satellite prophages were widely distributed among streptococci, were two clearly different entities and each possessed a structured population. There was convincing evidence that cross-species transmission of prophages is not uncommon. Furthermore, Streptococcus pneumoniae (pneumococcus) is a leading human pathogen worldwide, but the genetic basis for its pathogenicity and virulence is not yet fully understood. Here we report that over one-third of pneumococcal genomes possessed satellite prophages and demonstrate for the first time that a satellite prophage was associated with virulence in a murine model of infection. Overall, our findings demonstrate that prophages are widespread components of Streptococcus species and suggest that they play a role in pneumococcal pathogenesis.

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“…Next-Generation Sequencing (NGS) technologies have allowed sequencing and analysis Group B Streptococcus (GBS) genomes from different environments and organisms[1–6]. The presence of prophages and mobile elements in GBS was associated with the bacterial adaptation and ability to cause infections, likely enhancing their diversity and spread[7–10]. In fact, the estimates suggest that roughly 50% of Streptococcus agalactiae genome is grouped into islands of pathogenicity, where virulence genes and mobile elements are present[11].…”

Section: Introductionmentioning

confidence: 99%

Shallow MinION sequencing to assist de novo assembly of the Streptococcus agalactiae genome

Hernández-Beeftink

Rodríguez‐Pérez

Usera

et al. 2018

Preprint

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Despite the reduced read length, the so-called Next-Generation Sequencing (NGS) of second-generation has allowed rapid and complete genome characterization of many species. MinION (Oxford Nanopore Technologies), a portable third-generation NGS device, enables sequencing of long DNA fragments at low cost. Here we used a low-coverage MinION sequencing in combination with short-read NGS to improve genome assembly. We tested this possibility by using MinION R9.0 with Rapid 1D kit and MiSeq with >300X paired-end 300 bp reads (Illumina, Inc.) for the genome assembly of a Streptococcus agalactiae clinical isolate (2.2 Mb). With as few as 1,171 MinION reads that covered the genome at 2.4X (the longest read being 186 Kb long), the hybrid assembly combining MinION and Illumina reads increased the N50 by 4.9-fold compared to the assembly using Illumina data alone. Almost 50% of the genome was represented into a single contig (1.02 Mb). Besides, this allowed the full reconstruction of mobile elements, including a plasmid, and improved gene annotation. Taken together, our results support that shallow MinION sequencing combined with high-throughput second-generation NGS constitutes a cost-efficient strategy for the assembly of whole genomes.

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Analysis of the prophages carried by human infecting isolates provides new insight into the evolution of Group B Streptococcus species

Abstract: Our results suggest that prophages (possibly animal-associated) have conditioned bacterial adaptation and ability to cause infections in neonates and adults, and support a role of lysogeny with the emergence of GBS as a pathogen in human.

Cited by 23 publications

References 26 publications

Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus

Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus

Prophages and satellite prophages are widespread amongStreptococcusspecies and may play a role in pneumococcal pathogenesis

Shallow MinION sequencing to assist de novo assembly of the Streptococcus agalactiae genome

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