Vol. 74, No. 1
Microbial Interactions within a Cheese Microbial Community †
Jerome Mounier,1 Christophe Monnet,1 Tatiana Vallaeys,1 Roger Arditi,2 Anne-Sophie Sarthou,1 ´ ˆ Arnaud Helias,1 and FrancoiseIrlinger1* ´ ¸
UMR782 Genie et Microbiologie des Procedes Alimentaires, INRA, AgroParisTech, 78850 Thiverval Grignon, France,1 and ´ ´ ´ Ecologie des Populations et Communautes, AgroParisTech, 75000 Paris, France2 ´
Received 15 June 2007/Accepted 25 October 2007
The interactions that occur during the ripening of smear cheeses are not well understood. Yeast-yeast interactions and yeast-bacteriuminteractions were investigated within a microbial community composed of three yeasts and six bacteria found in cheese. The growth dynamics of this community was precisely described during the ripening of a model cheese, and the Lotka-Volterra model was used to evaluate species interactions. Subsequently, the effects on ecosystem functioning of yeast omissions in the microbial community wereevaluated. It was found both in the Lotka-Volterra model and in the omission study that negative interactions occurred between yeasts. Yarrowia lipolytica inhibited mycelial expansion of Geotrichum candidum, whereas Y. lipolytica and G. candidum inhibited Debaryomyces hansenii cell viability during the stationary phase. However, the mechanisms involved in these interactions remain unclear. It was alsoshown that yeast-bacterium interactions played a signiﬁcant role in the establishment of this multispecies ecosystem on the cheese surface. Yeasts were key species in bacterial development, but their inﬂuences on the bacteria differed. It appeared that the growth of Arthrobacter arilaitensis or Hafnia alvei relied less on a speciﬁc yeast function because these species dominated the bacterial ﬂora,regardless of which yeasts were present in the ecosystem. For other bacteria, such as Leucobacter sp. or Brevibacterium aurantiacum, growth relied on a speciﬁc yeast, i.e., G. candidum. Furthermore, B. aurantiacum, Corynebacterium casei, and Staphylococcus xylosus showed reduced colonization capacities in comparison with the other bacteria in this model cheese. Bacterium-bacterium interactions couldnot be clearly identiﬁed. Little is known about yeast-bacterium interactions, and smear-ripened cheeses offer an interesting model to investigate them. Indeed, the smear cheese microbial community is composed of both yeast and bacteria, is of a known speciﬁc composition that constitutes the “inoculum,” and shows a reduced diversity and a high stability (12, 13, 23, 27, 34). The smear is ared-orange, often viscous, microbial mat which is characterized by a succession of microbial communities including both yeast and bacteria. For example, the surface microﬂora of bacterial smear-ripened cheeses, such as Reblochon, Tilsit, and Limburger, is composed of yeast, mainly Debaryomyces hansenii and Geotrichum candidum, and of grampositive catalase-positive organisms, such as coryneform bacteriaand staphylococci (2, 9, 10, 35). During the ﬁrst days of ripening, yeasts colonize the cheese surface and utilize lactate. This utilization progressively leads to the deacidiﬁcation of the cheese surface, enabling the establishment of a bacterial community that is less acid tolerant (8). These communities are relatively simple compared with other microbial communities, such as soil communities.Indeed, they are composed of a limited number, i.e., 10 to 20 species, of mostly cultivable species (12, 27). The microbial diversity of cheese was investigated using both culture and nonculture approaches, such as repetitive extragenic palindromic sequence-based PCR, Fou* Corresponding author. Mailing address: UMR782 Genie et Mi´ crobiologie des Procedes Alimentaires, INRA, AgroParisTech, 78850 ´...