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Psychrotolerant  Pseudomonas  species are a main cause of proteolytic spoilage of ultra-high temperature (UHT) milk products due to the secretion of the heat-resistant metallopeptidase AprX, which is encoded by the first gene of the  aprX-lipA2  operon. While the proteolytic property has been characterized for many different  Pseudomonas  isolates, the underlying  aprX-lipA2  gene organization was only described for a few strains so far. In this study, the phylogenomic analysis of 185  Pseudomonas  type strains revealed that the presence of  aprX  is strongly associated to a monophylum composed of 81 species, of which 83% carried the  aprX  locus. Furthermore, almost all type strains of known milk-relevant species were shown to be members of the three monophyletic groups  P. fluorescens ,  P. gessardii , and  P. fragi . In total, 22 different types of  aprX-lipA2  genetic organizations were identified in the genus, whereby 31% of the species tested carried the type 1 operon structure consisting of eight genes ( aprXIDEF prtAB lipA2 ). Other genetic structures differed from type 1 mainly in the presence and location of genes coding for two lipases ( lipA1  and  lipA2 ) and putative autotransporters ( prtA  and  prtB ). The peptidase activity of 129 strains, as determined on skim milk agar and in UHT-milk, correlated largely with different  aprX-lipA2  gene compositions. Particularly, isolates harboring the type 1 operon were highly proteolytic, while strains with other operon types, especially ones lacking  prtA  and  prtB , exhibited significantly lower peptidase activities. In conclusion, the phylogenomic position and the  aprX-lipA2  gene organization specify the proteolytic potential of  Pseudomonas  isolates. In addition, however, an interplay of several environmental factors and intrinsic traits influences production and activity of AprX, leading to strain-specific proteolytic phenotypes.

Genetic Organization of the aprX-lipA2 Operon Affects the Proteolytic Potential of Pseudomonas Species in Milk