Abstract
Despite the persistent and costly problem caused by (bacterio)phage predation of Streptococcus thermophilus in dairy plants, DNA sequence information relating to these phages remains limited. Genome sequencing is necessary to better understand the diversity and proliferative strategies of virulent phages. In this report, whole genome sequences of 40 distinct bacteriophages infecting S. thermophilus were analyzed for general characteristics, genomic structure and novel features. The bacteriophage genomes display a high degree of conservation within defined groupings, particularly across the structural modules. Supporting this observation, four novel members of a recently discovered third group of S. thermophilus phages (termed the 5093 group) were found to be conserved relative to both phage 5093 and to each other. Replication modules of S. thermophilus phages generally fall within two main groups, while such phage genomes typically encode one putative transcriptional regulator. Such features are indicative of widespread functional synteny across genetically distinct phage groups. Phage genomes also display nucleotide divergence between groups, and between individual phages of the same group (within replication modules and at the 3′ end of the lysis module)—through various insertions and/or deletions. A previously described multiplex PCR phage detection system was updated to reflect current knowledge on S. thermophilus phages. Furthermore, the structural protein complement as well as the antireceptor (responsible for the initial attachment of the phage to the host cell) of a representative of the 5093 group was defined. Our data more than triples the currently available genomic information on S. thermophilus phages, being of significant value to the dairy industry, where genetic knowledge of lytic phages is crucial for phage detection and monitoring purposes. In particular, the updated PCR detection methodology for S. thermophilus phages is highly useful in monitoring particular phage group(s) present in a given whey sample. Studies of this nature therefore not only provide information on the prevalence and associated threat of known S. thermophilus phages, but may also uncover newly emerging and genomically distinct phages infecting this dairy starter bacterium.
Highlights
The problem of phage predation of Streptococcus thermophilus in the dairy industry has been well described (Caldwell et al, 1996; Bruttin et al, 1997; Quiberoni et al, 2006; Garneau and Moineau, 2011), though the precise impact on the fermentation process can only be estimated due to logistical limitations and commercial sensitivities
The complete genomes of 20 phages infecting S. thermophilus have been published: O1205 (Stanley et al, 1997), Sfi19 and Sfi21 (Desiere et al, 1998), DT1 (Tremblay and Moineau, 1999), Sfi11 (Lucchini et al, 1999), 7201 (Stanley et al, 2000), 2972 (Levesque et al, 2005), 858 (Deveau et al, 2008), ALQ13.2 and Abc2 (Guglielmotti et al, 2009b), 5093 (Mills et al, 2011), TP-J34L and TP-778L (Ali et al, 2014), 9871, 9872, 9873, and 9874 (McDonnell et al, 2016), and CHPC577, CHPC926, and CHPC1151 (Szymczak et al, 2016). Their availability revealed that S. thermophilus phage genomes possess a modular structure, while it allowed an analysis of their evolution and relatedness (Lucchini et al, 1999; Proux et al, 2002), thereby providing insights into some unusual genetic lineages (Mills et al, 2011; McDonnell et al, 2016; Szymczak et al, 2016; discussed further below)
It is known that the S. thermophilus clustered regularly interspaced short palindromic repeats (CRISPR) (Clustered Regularly Interspaced Short Palindromic Repeats)-Cas phage-resistance system relies on the acquisition of short genomic regions from the infecting phage (Hols et al, 2005; Barrangou et al, 2007; Deveau et al, 2008), which in turn is counteracted by the accumulation of point mutations in the phage genome (Deveau et al, 2008), leading to iterative genomic alterations
Summary
The problem of phage predation of Streptococcus thermophilus in the dairy industry has been well described (Caldwell et al, 1996; Bruttin et al, 1997; Quiberoni et al, 2006; Garneau and Moineau, 2011), though the precise impact on the fermentation process can only be estimated due to logistical limitations and commercial sensitivities. The complete genomes of 20 phages infecting S. thermophilus have been published: O1205 (Stanley et al, 1997), Sfi and Sfi (Desiere et al, 1998), DT1 (Tremblay and Moineau, 1999), Sfi (Lucchini et al, 1999), 7201 (Stanley et al, 2000), 2972 (Levesque et al, 2005), 858 (Deveau et al, 2008), ALQ13.2 and Abc (Guglielmotti et al, 2009b), 5093 (Mills et al, 2011), TP-J34L and TP-778L (Ali et al, 2014), 9871, 9872, 9873, and 9874 (McDonnell et al, 2016), and (very recently) CHPC577, CHPC926, and CHPC1151 (Szymczak et al, 2016) Their availability revealed that S. thermophilus phage genomes possess a modular structure, while it allowed an analysis of their evolution and relatedness (Lucchini et al, 1999; Proux et al, 2002), thereby providing insights into some unusual genetic lineages (Mills et al, 2011; McDonnell et al, 2016; Szymczak et al, 2016; discussed further below). It is known that the S. thermophilus CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)-Cas phage-resistance system relies on the acquisition of short genomic regions from the infecting phage (Hols et al, 2005; Barrangou et al, 2007; Deveau et al, 2008), which in turn is counteracted by the accumulation of point mutations in the phage genome (Deveau et al, 2008), leading to iterative genomic alterations
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