Identification and Analysis of a Novel Group of Bacteriophages Infecting the Lactic Acid Bacterium Streptococcus thermophilus

Abstract

We present the complete genome sequences of four members of a novel group of phages infecting Streptococcus thermophilus, designated here as the 987 group. Members of this phage group appear to have resulted from genetic exchange events, as evidenced by their "hybrid" genomic architecture, exhibiting DNA sequence relatedness to the morphogenesis modules of certain P335 group Lactococcus lactis phages and to the replication modules of S. thermophilus phages. All four identified members of the 987 phage group were shown to elicit adsorption affinity to both their cognate S. thermophilus hosts and a particular L. lactis starter strain. The receptor binding protein of one of these phages (as a representative of this novel group) was defined using an adsorption inhibition assay. The emergence of a novel phage group infecting S. thermophilus highlights the continuous need for phage monitoring and development of new phage control measures. IMPORTANCEPhage predation of S. thermophilus is an important issue for the dairy industry, where viral contamination can lead to fermentation inefficiency or complete fermentation failure. Genome information and phage-host interaction studies of S. thermophilus phages, particularly those emerging in the marketplace, are an important part of limiting the detrimental impact of these viruses in the dairy environment. Streptococcus thermophilus is a globally employed dairy bacterium used in the production of a variety of cheeses and yoghurt. Having been safely consumed by humans for millennia, this bacterium is now a mainstay of the dairy industry due its favorable acidification and texturizing properties (1, 2). Despite advances in the available knowledge regarding dairy phage containment (3, 4) and S. thermophilus phage genetics and biology (5, 6), contamination of dairy production lines by S. thermophilus-infecting (bacterio)phages remains a persistent problem (for a review, see reference 7).Classification of phages of S. thermophilus (reviewed by Mahony and van Sinderen [8]) has long been based on (i) morphology, i.e., as Siphoviridae, corresponding to group B as defined by Bradley (9), and (ii) a combination of the mode of DNA packaging (i.e., cos or pac site-containing) and major structural protein content (10). A variable genomic region thought to be (at least in part) responsible for host determination (VR2 region [11]) can also be used to categorize the majority of isolated S. thermophilus phages (12). More recently, however, a morphologically distinct and genetically divergent S. thermophilus phage named 5093, containing neither cos-or pac-defining structural elements nor a confirmed antireceptor-encoding gene, was described (13), prompting the creation of a third S. thermophilus phage group (here termed the "5093 group"). The genomic content of phage 5093 (containing several genes of nondairy streptococcal phage origin) highlights the genetic plasticity of S. thermophilus phages, thus explaining the appearance of such diverse phage lineages.A total of 13 complete genom...

Phage-host interactions in Streptococcus thermophilus: Genome analysis of phages isolated in Uruguay and ectopic spacer acquisition in CRISPR array

“…Comparative genome analyses, particularly of the morphogenesis module, confirmed this previous classification6. Two other S. thermophilus phages groups, albeit rare, were recently identified78. Despite this expanding number of groups, S. thermophilus phage genomes are similarly organized into modular regions and the genes coding for DNA replication and host lysis are highly conserved.…”

A Glimpse into the World of Integrative and Mobilizable Elements in Streptococci Reveals an Unexpected Diversity and Novel Families of Mobilization Proteins

“…These proteins include homologs to: (i) ‘replisome organizers’ or ‘DnaC-related’ proteins involved in the initiation of theta replication of various phages from Firmicutes such as phi5218, phi4268, or phi9871 (Trotter et al, 2006; Tang et al, 2013; McDonnell et al, 2016), (ii) ‘ParB’ proteins involved in chromosome and plasmid partitioning (domain TIGR00180) ( Figure 4 ). Such proteins are not encoded by any other class of IMEs analyzed in this study.…”

YMC-2011, a Temperate Phage of Streptococcus salivarius 57.I

“…For instance, the virulent phages DT1 (12), 7201 (11), Sfi19 (13), and Abc2 (14), as well as the temperate phage Sfi21 (15), are cos-type phages, whereas the temperate phages O1205 (11) and TP-J34/TP-778L (16) and the virulent phages Sfi11 (17), 2972 (18), 858 (19), and ALQ13.2 (14) are pac-type phages. Additional groups, including phage 5093 (20) and the newly described 987 phage group (21), are classified independently, as both possess mosaic genomes, presumably resulting from a relatively recent horizontal gene transfer and/or recombination event. Similarly, two DNA replication modules, represented by phages Sfi21 and 7201, have been observed with S. thermophilus-infecting phages; however, most such phages possess the conserved Sfi21-like replication module (22).…”