Differential expression of a prophage-encoded glycocin and its immunity protein suggests a mutualistic strategy of a phage and its host

Abstract

Sublancin 168 is a highly potent and stable antimicrobial peptide secreted by the Gram-positive bacterium Bacillus subtilis . Production of sublancin gives B . subtilis a major competitive growth advantage over a range of other bacteria thriving in the same ecological niches, the soil and plant rhizosphere. B . subtilis protects itself against sublancin by producing the cognate immunity protein SunI. Previous studies have shown that both the sunA gene for sublancin and the sunI immunity gene are encoded by the prophage SPβ. The sunA gene is under control of several transcriptional regulators. Here we describe the mechanisms by which sunA is heterogeneously expressed within a population, while the sunI gene encoding the immunity protein is homogeneously expressed. The key determinants in heterogeneous sunA expression are the transcriptional regulators Spo0A, AbrB and Rok. Interestingly, these regulators have only a minor influence on sunI expression and they have no effect on the homogeneous expression of sunI within a population of growing cells. Altogether, our findings imply that the homogeneous expression of sunI allows even cells that are not producing sublancin to protect themselves at all times from the active sublancin produced at high levels by their isogenic neighbors. This suggests a mutualistic evolutionary strategy entertained by the SPβ prophage and its Bacillus host, ensuring both stable prophage maintenance and a maximal competitive advantage for the host at minimal costs.

Pervasive prophage recombination occurs during evolution of spore-forming Bacilli

“…Based on comparison of the sizes and integration sites of prophage elements within Bacillus sp., SPβ and phi3T clearly belong to a distinct prophage group. These phages appear extremely large (2-3-fold larger than average prophages), and they possess sophisticated communication systems that are potentially capable of sensing the frequency of lysogenized hosts [65,88] or biosynthetic gene clusters [89,90], and functional genes related to host dormancy [91,92]. A high level of homology between SPβ and phi3Ts offers extensive regions for homologous recombination, which can be additionally promoted by the recombination machinery involved in natural competence [93] and in non-homologous end-joining repair [94] .…”

Characterization of the Biosynthetic Gene Cluster of Enterocin F4-9, a Glycosylated Bacteriocin

“…In the same context, a single gene (asmH) has been suggested to be responsible for the immunity to ASM1 [8]. Denham et al [25] reported that sunI is responsible for encoding the immunity protein for sublancin 168. ThuI is a putative immunity protein detected in the thurandacin gene cluster [6].…”

Pervasive prophage recombination occurs during evolution of spore-formingBacilli

“…Based on comparison of the sizes and integration sites of prophage elements within Bacillus sp., SPβ and phi3T clearly belong to a distinct prophage group. These phages appear extremely large (2-3-fold larger than average prophages), and they possess sophisticated communication systems that are potentially capable of sensing the frequency of lysogenized hosts [64, 87] or biosynthetic gene clusters [88, 89], and functional genes related to host dormancy [90, 91]. A high level of homology between SPβ and phi3Ts offers extensive regions for homologous recombination, which can be additionally promoted by the recombination machinery involved in natural competence [92] and in non-homologous end-joining repair [93].…”