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

Jasmine S Ritschard,Lea Amato,Leo Meile,Markus Schuppler,Hanne Van Loon

doi:10.3390/foods11030361

Abstract

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.

Highlights

The production of cheese has a long tradition in Europe that has given rise to a majority of commercially important cheese varieties [1]
Differences in the quantity of Gram-negative bacteria might be influenced by differing production technologies, seasonal variation or the milk type applied for cheese production
This study provides valuable insights into the occurrence of Enterobacterales in cheese surface microbiota and their presumable contribution to flavor development in cheese

Summary

Introduction

The production of cheese has a long tradition in Europe that has given rise to a majority of commercially important cheese varieties [1]. About one third of the yearly cheese production of Switzerland comprises semi-hard cheeses, while the majority are surface-ripened varieties with washed rind such as Appenzeller or Raclette cheese [2]. The development of a complex microbial biocoenosis in the surface smear during the ripening process is characteristic of these semi-hard surface-ripened cheese varieties. This surface smear microbiota is responsible for the red–orange coloration of the cheese surface, it greatly determines the organoleptic properties of this type of cheese— including its intense sulfuric smell [3]. At the end of the ripening process, the surface smear microbiota consists mainly of salt-tolerant yeast and aerobic Gram-positive bacteria [3,5]. Raw milk cheeses might contain Gram-negative bacteria ab initio inside and upon the cheese matrix due to prior colonization of the milk during processing, whereas Gram-negative bacteria in cheese from pasteurized milk are rather derived from secondary contaminations during cheese manufacture [26,27]

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