Comparative genomic analysis of Brevibacterium strains: insights into key genetic determinants involved in adaptation to the cheese habitat

Abstract

Background Brevibacterium strains are widely used for the manufacturing of surface-ripened cheeses, contributing to the breakdown of lipids and proteins and producing volatile sulfur compounds and red-orange pigments. The objective of the present study was to perform comparative genomic analyses in order to better understand the mechanisms involved in their ability to grow on the cheese surface and the differences between the strains.ResultsThe genomes of 23 Brevibacterium strains, including twelve strains isolated from cheeses, were compared for their gene repertoire involved in salt tolerance, iron acquisition, bacteriocin production and the ability to use the energy compounds present in cheeses. All or almost all the genomes encode the enzymes involved in ethanol, acetate, lactate, 4-aminobutyrate and glycerol catabolism, and in the synthesis of the osmoprotectants ectoine, glycine-betaine and trehalose. Most of the genomes contain two contiguous genes encoding extracellular proteases, one of which was previously characterized for its activity on caseins. Genes encoding a secreted triacylglycerol lipase or involved in the catabolism of galactose and D-galactonate or in the synthesis of a hydroxamate-type siderophore are present in part of the genomes. Numerous Fe3+/siderophore ABC transport components are present, part of them resulting from horizontal gene transfers. Two cheese-associated strains have also acquired catecholate-type siderophore biosynthesis gene clusters by horizontal gene transfer. Predicted bacteriocin biosynthesis genes are present in most of the strains, and one of the corresponding gene clusters is located in a probable conjugative transposon that was only found in cheese-associated strains.Conclusions Brevibacterium strains show differences in their gene repertoire potentially involved in the ability to grow on the cheese surface. Part of these differences can be explained by different phylogenetic positions or by horizontal gene transfer events. Some of the distinguishing features concern biotic interactions with other strains such as the secretion of proteases and triacylglycerol lipases, and competition for iron or bacteriocin production. In the future, it would be interesting to take the properties deduced from genomic analyses into account in order to improve the screening and selection of Brevibacterium strains, and their association with other ripening culture components.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4322-1) contains supplementary material, which is available to authorized users.

The Internal, External and Extended Microbiomes of Hominins

“…In other cases, they were microbes associated with human or other mammal bodies. Modern examples of the latter include the use of salivary microbial communities to initiate the fermenting process in chicha production in Peru, and similar fermented beverages around the world (Freire et al, 2016), the use of skin microbes to produce bodily aromas in some semi-soft cheeses (Pham et al, 2017), the use of body associated Lactobacillus species in sourdough breads (Gänzle and Ripari, 2016) or the use of the ancestrally mouth-associated bacteria species, Streptococcus thermophilus, in the production of yogurt (Goh et al, 2011). Once they began using body and other microbes to ferment foods, our ancestors extended their genomes and ultimately their phenotypes in much the way that beavers do in building a dam that yields a pond (Carthey et al, 2018).…”

Gluconacin fromGluconacetobacter diazotrophicusPAL5 is an active bacteriocin against phytopathogenic and beneficial sugarcane bacteria

“…Another class of bacteriocin is represented by Linocin M18, initially characterized in Brevibacterium linens (Valdés‐Stauber and Scherer ) and recently detected in 15 of the 23 investigated B. linens genomes belonging to different phylogenetic groups and isolated from different habitats (Pham et al . ). The authors also concluded that the main function of Linocin M18 in cheese is to inhibit other microbial groups that share the same ecological niche, therefore conferring a selective advantage on themselves.…”

Brevibacterium from Austrian hard cheese harbor a putative histamine catabolism pathway and a plasmid for adaptation to the cheese environment

“…The taxonomy of the genus Brevibacterium is under reorganization with Brevibacterium genomes varying greatly in both size and functional content 7,14,15 . It should be noted that the genus Brevibacterium also contains opportunistic pathogens and other biotechnologically important species 16–19 .…”

“…It should be noted that the genus Brevibacterium also contains opportunistic pathogens and other biotechnologically important species 16–19 . Cheese-associated subtypes of Brevibacterium can be found in several species of the genus, suggesting that adaptation to cheese environments might have been acquired independently through horizontal gene transfer (HGT) events 15,20 . Two recent studies have analyzed the genetic content of Brevibacterium focusing on their putative genetic functions in cheese production.…”

“…The second study analyzed 23 Brevibacterium isolate genomes, 12 of which were isolated from cheese, and found many putative genes involved in iron acquisition and bacteriocin production. Notably, they found a 96 kbp insertion element in a number of Brevibacterium genomes containing lanthipeptide bacteriocin genes, which they designated Brevibacterium Lanthipeptide Island (BreLI) 15 . These BreLI islands thus potentially provide a competitive advantage to their host strains against other bacteria.…”