The extracellular phage-host interactions involved in the bacteriophage LL-H infection of Lactobacillus delbrueckii ssp. lactis ATCC 15808

Abstract

The complete genome sequence of Lactobacillus bacteriophage LL-H was determined in 1996. Accordingly, LL-H has been used as a model phage for the infection of dairy Lactobacillus, specifically for thermophilic Lactobacillus delbrueckii ssp. lactis host strains, such as ATCC 15808. One of the major goals of phage LL-H research consisted of the characterization of the first phage-host interactions at the level of phage adsorption and phage DNA injection steps to determine effective and practical methods to minimize the risks associated with the appearance and attack of phages in the manufacture of yogurt, and Swiss or Italian hard type cheeses, which typically use thermophilic lactic acid bacteria starter cultures containing L. delbrueckii strains among others. This mini review article summarizes the present data concerning (i) the special features, particle structure, and components of phage LL-H and (ii) the structure and properties of lipoteichoic acids (LTAs), which are the phage LL-H receptor components of L. delbrueckii ssp. lactis host strains. Moreover, a model of the first, extracellular, phage-host interactions for the infection of L. delbrueckii ssp. lactis ATCC 15808 by phage LL-H is presented and further discussed.

Keywords: Lactobacillus delbrueckii; antireceptor; bacteriophage LL-H; lactic acid bacteria; lipoteichoic acid; phage adsorption; phage receptor; phage–host interaction.

FIGURE 1

Schematic diagram of phage LL-H particle. Genes encoding capsid and tail proteins are indicated as green and blue, respectively. Gene g71 (red) encodes the antireceptor protein SP58. The proteins coded by genes orf351 and orf546 (yellow) are considered as tape measure protein (TMP) homologs, likely localized to the core of the tail. The base plate is indicated as gray.

FIGURE 2

A model of phage LL-H antireceptor-Lactobacillus delbrueckii ssp. lactis ATCC 15808 lipoteichoic acid (LTA) interactions during the extracellular phase of phage infection [steps (A–E)]. (A) The LL-H tail fiber (red) is suggested to comprise six antireceptor protein (SP58) subunits. (B,C) Each antireceptor subunit initially interacts (reversible adsorption) with the top glucose moiety (green), followed by one of the negatively charged top phosphate groups (black) of LTA (irreversible adsorption) to facilitate the tail fiber attachment to the ends of up to six LTA molecules outside the peptidoglycan (PG) layer. (D) SP58 subunits-LTA interactions promote the tail fiber rearrangement into a ring structure attached to the end of the tail base for the release of the TMP homologs ORF546 (SP54?) and ORF351 from the tail core into the space restricted by the SP58-bound LTA molecules and further stabilized with calcium (Ca) bridges. (E) The PG-degrading activity of ORF546 proteins (yellow triangle) produces additional space for the formation of the stable Ca-LTA channel between the end of the tail base and the cytoplasmic membrane (CM). The Ca-LTA channel provides a gateway for ORF351 proteins (yellow square) to interact with the CM, and to further guide the transfer of the linear phage LL-H DNA complexed with calcium, through the CM into the cytoplasm of the infected host bacterial cell.