Numerous interactions between species can occur in cheese involving thermophilic LAB as main starters as summarized in Fig. 3. When lactococci are used for maturation, the growth and acidification by thermophilic LAB are generally stimulated during pressing. This was particularly demonstrated in Comte cheese (62); however, the mechanism is not really established. Similarly, the potential influence of the milk natural flora on the thermophilic starters growth was not really explored. Strain-specific interactions were also observed between LAB and yeasts or molds (P. roqueforti) in blue cheeses (63), the mold stimulations being attributed to the release by LAB of amino acids such as arginine and leucine. In Swiss cheeses, as well as in many cheeses involving thermophilic LAB, a significant growth of nonstarter LAB (mainly L. paracasei) has been described (>108 cfu/g at the end of the ripening). NSLAB growth, in particular of citrate positive strains, can slow down propionic cid fermentation (64). However, the most documented interactions
are those observed within thermophilic LAB, and between propionibacteria and thermo-philic LAB starters, as summarized below.
Interactions between S. thermophilus and the thermophilic lactobacilli occur frequently. The lactobacilli can influence positively the early acidification by S. thermophilus during pressing: the pH reached at the end of pressing is the same, but the kinetic of acidification is modified, leading to differences in draining and subsequently to differences in calcium salts contents, texture, and quality of cheese opening (20). Interactions during pressing were recently more precisely evidenced in Comte cheese, using a factorial experiment plan (65). Regarding mechanisms, the main hypotheses are that S. thermophilus stimulates lactobacilli by CO2, formate production and a quick release of galactose, and that lactobacilli stimulates S. thermophilus by a released growth factor, which could be a nitrogen source like peptides. Interestingly, mixed colonies of S. thermophilus and L. helveticus in Swiss cheese were observed frequently by scanning electron microscopy (Fig. 4) (45), which well supports the idea of a symbiosis between both species. By contrast, negative interactions can also occur because all these species are able to produce bacteriocins—for example, thermophilin 13 for S. thermophilus; lactacin A andB for L. delbrueckii subsp. lactis and lactocin 27; helveticin V-1829 and helveticin J for L. helveticus.
In natural starters involving growth multiplication in whey, such as in Italian cheese-making, interactions between lactobacilli themselves, species or strains—either stimulations or inhibitions—were also observed (66,67), leading to complex population dynamics (68), but the mechanisms are not elucidated.
In conclusion, as long as mechanisms of interactions would no have been better characterized, the association of thermophilic LAB strains for cheesemaking will require a validation step by cheese assays, which is time-consuming and expensive.
B. Interactions Between Thermophilic LAB and Dairy Propionibacteria
Swiss-type cheeses like Emmental are characterized by an intensive development of dairy Propionibacteria, mainly the species P. freudenreichii, during warm room ripening (69). Lactate is transformed into acetate, propionate, and CO2 leading to the characteristic eye-
opening and nutty flavor of that cheese variety. The use of propionic starters in the manufacture of Swiss cheese has increased concomitantly with the decrease of the indigenous flora in raw milk. The kinetics and intensity of lactate fermentation by propionibacteria have a key role in the final quality of the cheese. Several investigations have shown that thermophilic lactobacilli were able to stimulate the growth of propionibacteria (21,70). The effect was shown to be largely strain dependent (71), the growth of some strains of P. freudenreichii being highly influenced by the chosen thermophilic lactobacilli, whereas other were not. The mechanisms were investigated by several authors (72-74) and the main hypotheses were (a) the nature of the lactate isomer produced (D or L) (b) the amount of amino acid and peptides released by the strong peptidases activity of thermophilic LAB. Recently, the positive effect of thermophilic lactobacilli on propionibacteria was attributed to their production of stimulating peptides, possibly peptides containing aspartate.
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