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Mobilome of Brevibacterium aurantiacum Sheds Light on Its Genetic Diversity and Its Adaptation to Smear-Ripened Cheeses.

ABSTRACT: Brevibacterium aurantiacum is an actinobacterium that confers key organoleptic properties to washed-rind cheeses during the ripening process. Although this industrially relevant species has been gaining an increasing attention in the past years, its genome plasticity is still understudied due to the unavailability of complete genomic sequences. To add insights on the mobilome of this group, we sequenced the complete genomes of five dairy Brevibacterium strains and one non-dairy strain using PacBio RSII. We performed phylogenetic and pan-genome analyses, including comparisons with other publicly available Brevibacterium genomic sequences. Our phylogenetic analysis revealed that these five dairy strains, previously identified as Brevibacterium linens, belong instead to the B. aurantiacum species. A high number of transposases and integrases were observed in the Brevibacterium spp. strains. In addition, we identified 14 and 12 new insertion sequences (IS) in B. aurantiacum and B. linens genomes, respectively. Several stretches of homologous DNA sequences were also found between B. aurantiacum and other cheese rind actinobacteria, suggesting horizontal gene transfer (HGT). A HGT region from an iRon Uptake/Siderophore Transport Island (RUSTI) and an iron uptake composite transposon were found in five B. aurantiacum genomes. These findings suggest that low iron availability in milk is a driving force in the adaptation of this bacterial species to this niche. Moreover, the exchange of iron uptake systems suggests cooperative evolution between cheese rind actinobacteria. We also demonstrated that the integrative and conjugative element BreLI (Brevibacterium Lanthipeptide Island) can excise from B. aurantiacum SMQ-1417 chromosome. Our comparative genomic analysis suggests that mobile genetic elements played an important role into the adaptation of B. aurantiacum to cheese ecosystems.

SUBMITTER: Levesque S

PROVIDER: S-EPMC6579920 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Corynebacterium variabile is part of the complex microflora on the surface of smear-ripened cheeses and contributes to the development of flavor and textural properties during cheese ripening. Still little is known about the metabolic processes and microbial interactions during the production of smear-ripened cheeses. Therefore, the gene repertoire contributing to the lifestyle of the cheese isolate C. variabile DSM 44702 was deduced from the complete genome sequence to get a better understanding of this industrial process. RESULTS: The chromosome of C. variabile DSM 44702 is composed of 3, 433, 007 bp and contains 3, 071 protein-coding regions. A comparative analysis of this gene repertoire with that of other corynebacteria detected 1, 534 predicted genes to be specific for the cheese isolate. These genes might contribute to distinct metabolic capabilities of C. variabile, as several of them are associated with metabolic functions in cheese habitats by playing roles in the utilization of alternative carbon and sulphur sources, in amino acid metabolism, and fatty acid degradation. Relevant C. variabile genes confer the capability to catabolize gluconate, lactate, propionate, taurine, and gamma-aminobutyric acid and to utilize external caseins. In addition, C. variabile is equipped with several siderophore biosynthesis gene clusters for iron acquisition and an exceptional repertoire of AraC-regulated iron uptake systems. Moreover, C. variabile can produce acetoin, butanediol, and methanethiol, which are important flavor compounds in smear-ripened cheeses. CONCLUSIONS: The genome sequence of C. variabile provides detailed insights into the distinct metabolic features of this bacterium, implying a strong adaption to the iron-depleted cheese surface habitat. By combining in silico data obtained from the genome annotation with previous experimental knowledge, occasional observations on genes that are involved in the complex metabolic capacity of C. variabile were integrated into a global view on the lifestyle of this species.

Project description:The complex smear microbiota colonizing the surface of red-smear cheese fundamentally impacts the ripening process, appearance and shelf life of cheese. To decipher the prokaryotic composition of the cheese smear microbiome, the surface of a semi-hard surface ripened cheese was studied post-ripening by culture-based and culture-independent molecular approaches. The aim was to detect potential bacterial alterations in the composition of the cheese smear microbiota resulting from cheese storage in vacuum film-prepackaging, which is often accompanied by the development of a surface smear defect. Next-generation sequencing of amplified 16S rRNA gene fragments revealed an unexpected high diversity of a total of 132 different genera from the domains Bacteria and Archaea on the cheese surface. Beside typical smear organisms, our study revealed the presence of several microorganisms so far not associated with cheese, but related to milk, farm and cheese dairy environments. A 16S ribosomal RNA based analysis from total RNA identified the major metabolically active populations in the cheese surface smear as Actinobacteria of the genera Corynebacterium, Brevibacterium, Brachybacterium and Agrococcus. Comparison of data on a higher phylogenetic level revealed distinct differences in the composition of the cheese smear microbiome from the different samples. While the proportions of Proteobacteria and Bacteroidetes were increased in the smear of prepacked samples and in particular in defective smear, staphylococci showed an opposite trend and turned out to be strongly decreased in defective smear. In conclusion, next-generation sequencing of amplified 16S rRNA genes and 16S rRNA from total RNA extracts provided a much deeper insight into the bacterial composition of the cheese smear microbiota. The observed shifts in the microbial composition of samples from defect surface smear suggest that certain members of the Proteobacteria contribute to the observed negative organoleptic properties of the surface smear of cheese after prepacking in plastic foil.

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Mobilome of Brevibacterium aurantiacum Sheds Light on Its Genetic Diversity and Its Adaptation to Smear-Ripened Cheeses.

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