Lactococcal 936-type phages and dairy fermentation problems: from detection to evolution and prevention

Abstract

The so-called 936-type phages are the most frequently encountered lactococcal phage species in dairy fermentations, where they cause slow or even failed fermentations with concomitant economic losses. Several dairy phage population studies, performed in different geographical locations, have detailed their dominance in dairy phage populations, while various phage-resistance mechanisms have been assessed in a bid to protect against this virulent phage group. The impact of thermal and chemical treatments on 936 phages is an important aspect for dairy technologists and has been assessed in several studies, and has indicated that these phages have adapted to better resist such treatments. The abundance of 936 phage genome sequences has permitted a focused view on genomic content and regions of variation, and the role of such variable regions in the evolution of these phages. Here, we present an overview on detection and global prevalence of the 936 phages, together with their tolerance to industrial treatments and anti-phage strategies. Furthermore, we present a comprehensive review on the comparative genomic analyses of members of this fascinating phage species.

Keywords: Lactococcus; dairy; food fermentation; lactic acid bacteria; phage.

FIGURE 1

Schematic representation of the typical genome architecture of a typical 936 phage. Genes with a predicted or proven function are assigned colors: green arrows indicate genes encoding the terminases and portal protein involved in phage DNA packaging; red arrows indicate the capsid genes; Blue arrows indicate tail structural genes; the purple arrow represents the receptor binding-encoding gene; pink arrows represent the holin and lysin of the lysis module; the black arrow represents a (subunit of) DNA polymerase. The transcriptional units as shown for sk1 are highlighted above the genomic drawing as are the functional modules of the genome. Below the genomic drawing are yellow highlighters of the dominant points of divergence in the genomes of the 936 phages: the neck passage structure, the tail tape measure, the receptor binding protein, lysin, and the origin of replication, notwithstanding that a general divergence is observed in the replication module in general. The indicated scale at the bottom of the figure represents base numbering starting at the cos site.

FIGURE 2

Phylogenetic tree of the receptor binding proteins (RBP) of representatives of the 936 phage species from several studies (Dupont et al., 2005; Mahony et al., 2006; Rousseau and Moineau, 2009a; Castro-Nallar et al., 2012). Phages that have been demonstrated to infect specifically L. lactis ssp. cremoris or ssp. lactis, are highlighted and P475 which infects both subspecies is also highlighted. *Indicates phages that have been propagated on a L. lactis ssp. cremoris strain but whose host range data is unknown. The remainder (ASCC collection) have a known host range but this data is unpublished. This phylogenetic tree highlights the divergent nature of the RBP sequences and while many of the sub-groups at the top of the tree are L. lactis ssp. cremoris-infecting phages and the lower half of the tree may be dominated by lactis-infecting phages, there are many of unknown host range.