Streptococcus pneumoniae: a Plethora of Temperate Bacteriophages With a Role in Host Genome Rearrangement

Abstract

Bacteriophages (phages) are viruses that infect bacteria. They are the most abundant biological entity on Earth (current estimates suggest there to be perhaps 1031 particles) and are found nearly everywhere. Temperate phages can integrate into the chromosome of their host, and prophages have been found in abundance in sequenced bacterial genomes. Prophages may modulate the virulence of their host in different ways, e.g., by the secretion of phage-encoded toxins or by mediating bacterial infectivity. Some 70% of Streptococcus pneumoniae (the pneumococcus)—a frequent cause of otitis media, pneumonia, bacteremia and meningitis—isolates harbor one or more prophages. In the present study, over 4000 S. pneumoniae genomes were examined for the presence of prophages, and nearly 90% were found to contain at least one prophage, either defective (47%) or present in full (43%). More than 7000 complete putative integrases, either of the tyrosine (6243) or serine (957) families, and 1210 full-sized endolysins (among them 1180 enzymes corresponding to 318 amino acid-long N-acetylmuramoyl-L-alanine amidases [LytAPPH]) were found. Based on their integration site, 26 different pneumococcal prophage groups were documented. Prophages coding for tRNAs, putative virulence factors and different methyltransferases were also detected. The members of one group of diverse prophages (PPH090) were found to integrate into the 3’ end of the host lytASpn gene encoding the major S. pneumoniae autolysin without disrupting it. The great similarity of the lytASpnand lytAPPH genes (85–92% identity) allowed them to recombine, via an apparent integrase-independent mechanism, to produce different DNA rearrangements within the pneumococcal chromosome. This study provides a complete dataset that can be used to further analyze pneumococcal prophages, their evolutionary relationships, and their role in the pathogenesis of pneumococcal disease.

SVep1, a temperate phage of human oral commensal Streptococcus vestibularis

“…It is estimated that 60%–70% of known bacterial genomes harbor phages, and as more phages are discovered and sequenced, this percentage is expected to increase ( Keen and Dantas, 2018 ). Although many bacterial genomes contain prophages ( Rezaei Javan et al, 2019 ; Martín-Galiano and García, 2021 ), the number of lysogenic phages currently isolated from the oral cavity is still limited. It is therefore not surprising that we isolated only one prophage from 75 oral bacterial strains.…”

PclR is a transcriptional activator of the gene that encodes the pneumococcal collagen-like protein PclA

“…DNA rearrangements and gene acquisition are natural strategies for the generation of genetic diversity in S. pneumoniae, a feature that has been recently shown to be increased by the presence of temperate bacteriophages integrated into different regions of the pneumococcal chromosome 45 www.nature.com/scientificreports/ between pairs of pneumococcal isolates can diverge by as much as 30% 46 . The sequences of the pneumococcal TIGR4 and R6 genomes were published in 2001 9,10 .…”

The role of rhizosphere phages in soil health

“…Temperate phages are widely acknowledged for their role in mediating horizontal gene transfer between bacteria via transduction and phages could hence drive bacterial evolution by promoting recombination and provision of new genes (Lwoff 1953 , Brussow et al 2004 , Bobay et al 2014 , De Paepe et al 2014 , Martin-Galiano and Garcia 2021 ). Earlier microcosm work has demonstrated high efficiency of phage transduction in soils (Zeph et al 1988 ).…”