Red-Brown Pigmentation of Acidipropionibacterium jensenii Is Tied to Haemolytic Activity and cyl-Like Gene Cluster

Abstract

The novel Acidipropionibacterium genus encompasses species of industrial importance but also those associated with food spoilage. In particular, Acidipropionibacterium acidipropionici, Acidipropionibacterium thoenii, and Acidipropionibacterium jensenii play an important role in food fermentation, as biopreservatives, or as potential probiotics. Notably, A. jensenii and A. thoenii can cause brown spot defects in Swiss-type cheeses, which have been tied to the rhamnolipid pigment granadaene. In the pathogenic bacterium Streptococcus agalactiae, production of granadaene depends on the presence of a cyl gene cluster, an important virulence factor linked with haemolytic activity. Here, we show that the production of granadaene in pigmented Acidipropionibacterium, including A. jensenii, A. thoenii, and Acidipropionibacterium virtanenii, is tied to haemolytic activity and the presence of a cyl-like gene cluster. Furthermore, we propose a PCR-based test, which allows pinpointing acidipropionibacteria with the cyl-like gene cluster. Finally, we present the first two whole genome sequence analyses of the A. jensenii strains as well as testing phenotypic characteristics important for industrial applications. In conclusion, the present study sheds light on potential risks associated with the presence of pigmented Acidipropionibacterium strains in food fermentation. In addition, the results presented here provide ground for development of a quick and simple diagnostic test instrumental in avoiding potential negative effects of Acidipropionibacterium strains with haemolytic activity on food quality.

The cyl Genes Reveal the Biosynthetic and Evolutionary Origins of the Group B Streptococcus Hemolytic Lipid, Granadaene

“…The latter is supported by the hemolytic and cytolytic activity of the Granadaene pigment in GBS (Whidbey et al, 2013(Whidbey et al, , 2015bBoldenow et al, 2016) and cyl-expressing L. lactis (Figures 1, 2). The presence of an identical or similar hemolytic pigment in a range of Gram-positive bacteria with cyl genes (Vanberg et al, 2007;Deptula et al, 2019), as well as our heterologous expression experiments, suggest that Granadaene can potentially function across a physiologically diverse group of organisms if they likely possess a Gram-positive-type cell wall structure. In fact, a recent study correlated pigmentation with hemolysis and cyl gene expression in Acidipropionibacterium species that have roles in cheese production and food preservation (Deptula et al, 2019).…”

“…The presence of an identical or similar hemolytic pigment in a range of Gram-positive bacteria with cyl genes (Vanberg et al, 2007;Deptula et al, 2019), as well as our heterologous expression experiments, suggest that Granadaene can potentially function across a physiologically diverse group of organisms if they likely possess a Gram-positive-type cell wall structure. In fact, a recent study correlated pigmentation with hemolysis and cyl gene expression in Acidipropionibacterium species that have roles in cheese production and food preservation (Deptula et al, 2019). Accordingly, the hemolytic and cytotoxic properties of other pigmented, cyl operon-containing microbes found in soil environments or utilized for industrial application warrant further examination.…”

Complete Genome Sequences and Methylome Analyses of Cutibacterium acnes subsp. acnes Strains DSM 16379 and DSM 1897 T

“…One methylation motif was detected for each of the strains. Annotation with the NCBI Prokaryotic Genome Annotation Pipeline (PGAP) ( 7 ) and SEQWARE methylome analysis at REBASE ( 8 ) were performed as previously described ( 9 ).…”

Propionic acid bacteria in the food industry: An update on essential traits and detection methods

“…c May turn orange to pink if kept for 3 weeks. d Corresponding to granadaene production according to Deptula et al (2019).…”

“…Piveteau et al (2000) suggested that the presence of immunoglobulins, transferrin, lactoferrin, lactoferrin-derived, or casein-derived proteins might cause inhibition of PAB. Controversially, Deptula et al (2019) observed that pigmented strains of A. thoenii and A. jensenii are somehow protected against growth inhibition caused by whey filtrates.…”