The Microbial Diversity on the Surface of Smear-Ripened Cheeses and Its Impact on Cheese Quality and Safety.

Smear-ripened cheeses are characterized by a viscous, red-orange surface smear on their rind. It is the complex surface microbiota on the cheese rind that is responsible for the characteristic appearance of this cheese type, but also for the wide range of flavors and textures of the many varieties of smear-ripened cheeses. The surface smear microbiota also represents an important line of defense against the colonization with undesirable microorganisms through various types of interaction, such as competitive exclusion or production of antimicrobial substances. Predominant members of the surface smear microbiota are salt-tolerant yeast and bacteria of the phyla Actinobacteria, Firmicutes, and Proteobacteria. In the past, classical culture-based approaches already shed light on the composition and succession of microorganisms and their individual contribution to the typicity of this cheese type. However, during the last decade, the introduction and application of novel molecular approaches with high-resolution power provided further in-depth analysis and, thus, a much more detailed view of the composition, structure, and diversity of the cheese smear microbiota. This led to abundant novel knowledge, such as the identification of so far unknown community members. Hence, this review is summarizing the current knowledge of the diversity of the surface smear microbiota and its contribution to the quality and safety of smear-ripened cheese. If the succession or composition of the surface-smear microbiota is disturbed, cheese smear defects might occur, which may promote food safety issues. Hence, the discussion of cheese smear defects in the context of an increased understanding of the intricate surface smear ecosystem in this review may not only help in troubleshooting and quality control but also paves the way for innovations that can lead to safer, more consistent, and higher-quality smear-ripened cheeses.

High Prevalence of Enterobacterales in the Smear of Surface-Ripened Cheese with Contribution to Organoleptic Properties.

The smear of surface-ripened cheese harbors complex microbiota mainly composed of typical Gram-positive aerobic bacteria and yeast. Gram-negative bacteria are usually classified as un-wanted contaminants. In order to investigate the abundance and impact of Gram-negative bacte-ria naturally occurring in the smear of surface-ripened cheese, we performed a culture-based analysis of smear samples from 15 semi-hard surface-ripened cheese varieties. The quantity, di-versity and species distribution of Proteobacteria in the surface smear of the analyzed cheese vari-eties were unexpectedly high, and comprised a total of 22 different species. Proteus and Morganella predominated most of the analyzed cheese varieties, while Enterobacter, Citrobacter, Hafnia and Serratia were also found frequently. Further physiological characterization of Proteus isolates re-vealed strong proteolytic activity, and the analysis of volatiles in the smear cheese surface head-space suggested that Enterobacterales produce volatile organic flavor compounds that contribute to the organoleptic properties of surface-ripened cheese. Autochthonous members of Enterobac-terales were found in 12 of the 15 smear samples from surface-ripened cheeses, suggesting that they are part of the typical house microbiota that shape the organoleptic properties of the cheese rather than represent unwanted contaminants. However, further investigation on safety issues of the individual species should be performed in order to manage the health risk for consumers.

The role of the surface smear microbiome in the development of defective smear on surface-ripened red-smear cheese.

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.