Cited by 112Probiotics and Fermented FoodsFermentation and Sensory AnalysisBiochemical and biochemical processes

Production of cheese flavour compounds derived from amino acid catabolism by Propionibacterium freudenreichii

Open access
Thierry, Anne, Maillard, Marie-Bernadette·2002·Le Lait

Abstract

The catabolism of amino acids by cheese micro-organisms results in the production of various volatile flavour compounds. It was recently shown to be a rate-limiting factor in the formation of cheese flavour, leading to an increased interest in elucidating the pathways and the flora involved. This paper reviews the ability of propionibacteria (PAB) to produce flavour compounds deriving from branched-chain, aromatic and sulphur-containing amino acids. In culture media, PAB produced volatile compounds derived from Leu, Ile, Met and Phe. In cheese, the presence of PAB is positively correlated to the amount of acids, alcohols and/or aldehydes derived from Leu or Ile. The metabolic pathways of amino acid conversion to flavour compounds by PAB have been only partly elucidated. Aminotransferase(s) catalyse the first step of conversion of branched-chain, aromatic amino acids and methionine, with a higher activity for branched-chain amino acids. The -keto acids resulting from transamination are further degraded to various compounds by resting cells of PAB. So -ketoisocaproic acid, derived from Leu, is essentially converted to isovaleric acid by a ketoacid dehydrogenase complex; phenylpyruvic acid, derived from Phe, is converted to phenyllactic acid, phenylacetic acid, benzoic acid and benzaldehyde. Methionine can also be directly degraded by , -elimination, leading to methanethiol. The amino acid catabolism pathways in PAB share similarities with those of lactic acid bacteria but PAB seem to produce higher amounts of branched-chain acids, which are important flavour compounds in cheese.

Integrity signals

Registry

Crossref · 10.1051/lait:2001002

Cites

69 of 69 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

9 of 88 cited sources checked · 5 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Asp, Ala and Ser are the most degraded amino acids by both resting cells and growing cells of PAB.

    “They showed that Asp, Ala and Ser are the most degraded amino acids by both resting cells and growing cells of PAB.”
    Quote in the paperNot a substantial claim1 of 6 sources checked
    • cites [1] 1. Antila M., Der Aminosaüreabrau durch Propionsaürebakterien, Finn, J. Dairy Sci. 18/19 (1957) 1-6.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [11] 11. Brendehaug J., Langsrud T., Amino acid metab- olism in Propionibacteria: Resting cells experi- ments with four strains, J. Dairy Sci. 68 (1985) 281-289.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [15] 15. Crow V.L., Metabolism of aspartate by Propionibacterium freudenreichii subsp. shermanii: Effect on lactate fermentation, Appl. Environ. Microbiol. 52 (1986) 359-365. source
    • cites [16] 16. Crow V.L., Properties of alanine dehydrogenase and aspartase from Propionibacterium freudenreichii subsp. shermanii, Appl. Environ. Microbiol. 53 (1987) 1885-1892. source
    • cites [22] 22. Gagnaire V., Thierry A., Léonil J., Propionibacteria and facultatively heterofermentative lactobacilli weakly contribute to secondary proteolysis of Emmental cheese, Lait 81 (2001) 339-353. source

      Section 3.3 reports that PAB exhausted Asp and reduced Ser in cultures grown in Emmental juice. The Discussion identifies Asp, Ser, Gly and Glu—not Ala—as amino acids consumed in large amounts. The paper does not report results for resting cells, so it does not support the claimed ranking for both resting and growing cells. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
    • cites [32] 32. Kiuru V.J.T., Über die Propionsäuregärung in bezug auf Emmentaler Käse, Ph.D. thesis, Uni- versity of Helsinki, Finland (1949).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Findingreasoning

    Phenylpyruvic acid derived from Phe is converted to phenyllactic acid, phenylacetic acid, benzoic acid and benzaldehyde.

    “phenylpyruvic acid, derived from Phe, is converted to phenyllactic acid, phenylacetic acid, benzoic acid and benzaldehyde.”
    Quote in the paperSubstantial claim
  • Findingnone given

    α-Ketoisocaproic acid derived from Leu is essentially converted to isovaleric acid by a ketoacid dehydrogenase complex.

    “So α-ketoisocaproic acid, derived from Leu, is essentially converted to isovaleric acid by a ketoacid dehydrogenase complex;”
    Quote in the paperSubstantial claim
  • Findingnone given

    In cheese, the presence of PAB is positively correlated to the amount of acids, alcohols and/or aldehydes derived from Leu or Ile.

    “In cheese, the presence of PAB is positively correlated to the amount of acids, alcohols and/or aldehydes derived from Leu or Ile.”
    Quote in the paperNot a substantial claim
  • Findingnone given

    In culture media, PAB produced volatile compounds derived from Leu, Ile, Met and Phe.

    “In culture media, PAB produced volatile compounds derived from Leu, Ile, Met and Phe.”
    Quote in the paperSubstantial claim
  • May combine two claims. 27
  • Classified as probably not a substantial claim. 23
  • May combine two claims.

    Premisecitation

    In Swiss cheese, 2-methylbutyric acid (from Ile) appeared at a higher concentration and/or was detected in a higher number of samples than 3-methybutyric acid (from Leu), whereas it was the opposite in Parmesan cheese.

    “In Swiss cheese, 2-methylbutyric acid (from Ile) appeared at a higher concentration and/or was detected in a higher number of samples than 3-methybutyric acid (from Leu) [35,60], whereas it was the opposite in Parmesan cheese [2].”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [35] 35. Langler J.E., Day E.A., Quantitative analysis of the major free fatty acids in Swiss cheese, J. Dairy Sci. 49 (1966) 91-93. source

      In the Swiss-cheese results (page unavailable), 2-methylbutyric acid was detected in all five cheeses, while 3-methylbutyric acid was detected in only two, supporting the detection-frequency comparison. The paper identifies leucine as a precursor of 3-methylbutyric acid but does not explicitly identify isoleucine as the precursor of 2-methylbutyric acid. The Parmesan comparison is attached to a different citation and is not assessed here. (LLM, conf=0.83)

      Experimental — accuracy not yet measured
    • cites [60] 60. Tuomala T., Kallio H., Identification of free fatty acids and some other volatile flavour compounds from Swiss cheese using on line supercritical fluid extraction -gas chromatography, Z. Lebensm. Unters. Forsch. 203 (1996) 236-240. source
    • cites [2] 2. Barbieri G., Bolzoni L., Careri M., Mangia A., Parolari G., Spagnoli S., Virgili R., Study of the volatile fraction of Parmesan cheese, J. Agric. Food Chem. 42 (1994) 1170-1176. source
  • May combine two claims.

    Premisecitation

    P. freudenreichii subsp. shermanii ATCC 9617 produced ~500 μg.L-1 dimethylsulfide (DMS) in milk cultures but not in YEL medium.

    “P. freudenreichii subsp.shermanii ATCC 9617 produced ~500 µg .L -1 dimethylsulfide (DMS) in milk cultures but not in YEL medium.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [19] 19. Dykstra G.J., Drerup A., Branen A.L., Keenan T.W., Formation of dimethyl sulfide by Propionibacterium shermanii ATCC 9617, J. Dairy Sci. 54 (1971) 168-172. source

      The Results and Discussion report that P. shermanii ATCC 9617 reached approximately 0.5 ppm DMS in milk culture at 30°C, consistent with roughly 500 µg/L. They also report no DMS in broth cultures, but Experimental Procedures identify the broth as sodium lactate broth, not YEL medium. The YEL-specific part of the claim is therefore unsupported. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
  • May combine two claims.

    Premisecitation

    PAB are capable of producing volatile sulphur compounds, and this ability is strain-dependent.

    “PAB are also capable of producing volatile sulphur compounds.This ability is strain-dependent [30,51].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [30] 30. Keenan T.W., Bills D.D., Volatile compounds produced by Propionibacterium, J. Dairy Sci. 51 (1968) 797-799. source
    • cites [51] 51. Raymond, N., Biogénèse des composés soufrés à partir de la L-méthionine chez les bactéries propioniques, DEA report, Institut National Agronomique Paris-Grignon, France (2000).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The high content of isovaleric acid in Swiss cheese (~30 mg.kg-1 on average) compared to Cheddar had early been observed.

    “The high content of isovaleric acid in Swiss cheese (~30 mg .kg -1 on average, [54,61]), compared to Cheddar, had early been observed [45].”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites [54] 54. Rychlik M., Warmke R., Grosch W., Ripening of Emmental cheese wrapped in foil with and with- out addition of Lactobacillus casei subsp. casei. III. Analysis of character impact flavour com- pounds, Lebensm. Wiss. Technol. 30 (1997) 471-478. source
    • cites [61] 61. Vangtal A., Hammond E.G., Correlation of the flavor characteristics of Swiss-type cheeses with chemical parameters, J. Dairy Sci. 69 (1986) 2982-2993. source

      The Results (page unavailable) identify isovaleric acid in Swiss-type cheeses and note earlier reports of it in Swiss cheese. The paper does not establish that its concentration is higher than in Cheddar; its Cheddar references describe a flavor note in some Swiss-type samples, not a concentration comparison. The approximate 30 mg/kg figure is attached to other citations in the citing sentence. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
    • cites [45] 45. Patton S., Volatile acids of Swiss cheese, J. Dairy Sci. 47 (1964) 817-818. source
  • May combine two claims.

    Interpretationcitation

    DMS probably came from sulphur-containing amino acids in peptide linkage, but not directly from free sulphur-containing amino acids.

    “DMS probably came from sulphur-containing amino acids in peptide linkage, but not directly from sulphur-containing amino acids, since the addition of L-Met, D-Met, L-Cys or D-Cys did not enhance the production of DMS in milk culture and did not induce it in YEL culture [19].”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [19] 19. Dykstra G.J., Drerup A., Branen A.L., Keenan T.W., Formation of dimethyl sulfide by Propionibacterium shermanii ATCC 9617, J. Dairy Sci. 54 (1971) 168-172. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Several other species, such as Lactobacillus sp. and Microbacterium, are capable of producing acids from amino acids.

    “It has not yet been described in other cheese-related bacteria, but several other species are capable of producing acids from amino acids like Lactobacillus sp.[42] and Microbacterium [29].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [42] 42. Nakae T., Elliot J.A., Production of volatile fatty acids by some lactic acid bacteria. II. Selective formation of volatile fatty acids by degradation of amino acids, J. Dairy Sci. 48 (1965) 293-299. source
    • cites [29] 29. Jollivet N., Bézanger M.C., Vayssier Y., Belin J.M., Production of volatile compounds in liquid cultures by six strains of coryneform bacteria, Appl. Microbiol. Biotechnol. 36 (1992) 790-794. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The content of α-ketoacid in cheese was recently demonstrated to be the rate-limiting factor of amino acid conversion by lactococci.

    “The content of α-ketoacid in cheese was recently demonstrated to be the rate-limiting factor of amino acid conversion by lactococci [53,65,67].”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [53] 53. Rijnen L., Courtin P., Gripon J.C., Yvon M., Expression of a heterologous glutamate dehydrogenase gene in Lactococcus lactis highly improves the conversion of amino acids to aroma compounds, Appl. Environ. Microbiol. 66 (2000) 1354-1359. source
    • cites [65] 65. Yvon M., Berthelot S., Gripon J.C., Adding al- pha-ketoglutarate to semi-hard cheese curd highly enhances the conversion of amino acids to aroma compounds, Int. Dairy J. 8 (1998) 889-898. source
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
  • May combine two claims.

    Findingnone given

    Aminotransferase(s) catalyse the first step of conversion of branched-chain, aromatic amino acids and methionine, with a higher activity for branched-chain amino acids.

    “Aminotransferase(s) catalyse the first step of conversion of branched-chain, aromatic amino acids and methionine, with a higher activity for branched-chain amino acids.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    Methionine can be directly degraded by α,γ-elimination, leading to methanethiol.

    “Methionine can also be directly degraded by α, γ -elimination, leading to methanethiol.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Branched-chain acids can be produced by other flora, as observed in Morbier cheese.

    “Branched-chain acids can however be produced by other flora, as observed in Morbier cheese (Tab.III).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingcitation

    2-Methylbutanal was at a concentration close to its odour threshold in milk (0.13 mg.L-1), whereas branched-chain alcohols were at concentrations markedly lower than their odour thresholds.

    “2-Methylbutanal was at a concentration close to its odour thresh-old in milk (0.13 mg .L -1 , [57]), whereas branched-chain alcohols were at concentrations markedly lower than their odour thresholds.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [57] 57. Sheldon R.M., Lindsay R.C., Libbey L.M., Mor- gan M.E., Chemical nature of malty flavor and aroma produced by Streptococcus lactis var. maltigenes, Appl. Microbiol. 22 (1971) 263-266. source
    • Rests on an assumption: The odour threshold values used (in water, milk, or cheese) are applicable to the cheese matrix for assessing the flavour impact of the compounds.
  • May combine two claims.

    Findingcitation

    S-methylthioacetate reached a concentration around 0.03 mg.kg-1 in Morbier cheese, i.e. ~7 times higher than its odour threshold in cheese (0.005 mg.L-1).

    “S-methylthioacetate reached a concentration around 0.03 mg .kg -1 , i.e. ~7 times higher than its odour threshold in cheese (0.005 mg .L -1 , [64].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [64] 64. Weimer B., Seefeldt K., Dias B., Sulfur metabo- lism in bacteria associated with cheese, Antonie van Leeuwenhoek 76 (1999) 247-261. source
    • Rests on an assumption: The odour threshold values used (in water, milk, or cheese) are applicable to the cheese matrix for assessing the flavour impact of the compounds.
  • May combine two claims.

    Findingown data

    In mini Swiss cheeses, volatile sulphur compounds and benzaldehyde were not significantly affected by PAB, except DMTS which was found at a lower concentration in cheese containing PAB.

    “In contrast, volatile sulphur compounds and benzaldehyde were not significantly affected by PAB, except DMTS which was found at a lower concentration in cheese containing PAB.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The concentrations of 3-methylbutanol, 3-methylbutanal, 2-methylbutanol and 2-methylbutanal in mini Swiss cheeses were ~0.13, 0.02, 0.29 and 0.11 mg.kg-1, respectively, i.e. ~1% of the volatile branched-chain compounds, with isovaleric acid amounting to the remaining 99%.

    “The concentration of 3-methylbutanol, 3-methylbutanal, 2-methylbutanol and 2-methylbutanal were ~0.13, 0.02, 0.29 and 0.11 mg .kg -1 , respectively, i.e. ~1% of the volatile branched-chain compounds, isovaleric acid amounting to the remaining 99%.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The two PAB strains used as starters reached 10^8 cfu.g-1 at the end of ripening in the inoculated Morbier cheeses, whereas indigenous PAB reached 5 × 10^6 cfu.g-1 in control ones.

    “The two PAB strains used as starters reached 10 8 cfu .g -1 at the end of ripening in the inoculated cheeses, whereas indigenous PAB reached 5 × 10 6 cfu .g -1 in control ones.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingcitation

    PAB reached 6 × 10^9 cfu.g-1 in the inoculated mini Swiss cheeses, whereas indigenous PAB remained under 5 × 10^6 cfu.g-1 at the end of ripening in control ones.

    “PAB reached 6 × 10 9 cfu .g -foot_0 in the inoculated cheeses, whereas indigenous PAB remained under 5 × 10 6 cfu .g -1 at the end of ripening in control ones [25].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] 25. Hervé C., Démonstration et étude de la lysogénie de Propionibacterium freudenreichii subsp. shermanii, Ph.D. thesis, ENSAR Rennes, France (2000).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Findingown data

    In Morbier cheese, neither isovaleric acid, DMTS nor benzaldehyde were significantly affected by PAB.

    “Neither isovaleric acid, DMTS or benzaldehyde were significantly affected by PAB.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In Morbier cheese, the level of 2-methylbutanol was significantly higher in the presence of both PAB strains, and that of 2-methylbutanal with the strain ITGP20.

    “The level of 2-methylbutanol was significantly higher in the presence of both strains, and that of 2-methylbutanal with the strain ITGP20 (Tab.III).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingnone given

    The main ability demonstrated in PAB is the conversion of Ile/Leu to isovaleric acid, which was observed in medium culture and in cheese without addition of α-KG.

    “The main ability demonstrated in PAB is the conversion of Ile/Leu to isovaleric acid, which was observed in medium culture and in cheese without addition of α-KG.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    The degradation of amino acids, rather than their release, is the rate-limiting factor in the formation of cheese flavour.

    “Recent results, however, showed that the content of free amino acids in cheese could be increased, either by adding amino acids or by enhancing peptidolysis, without any concomitant increase in flavour, suggesting that the rate-limiting factor in the formation of cheese flavour is the degradation of amino acids rather than their release [67].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Many flavour compounds have structures which indicate that they could originate from branched-chain, aromatic and sulphur-containing amino acids.

    “Many flavour compounds have structures which indicate that they could originate from branched-chain, aromatic and sulphur-containing amino acids.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In general, branched-chain acids appear to be more prevalent in Swiss-type cheeses and some Italian cheeses than in semi-hard cheese like Cheddar, Edam and Gouda.

    “In general, branched-chain acids appear to be more prevalent in Swisstype cheeses and some Italian cheeses than in semi-hard cheese like Cheddar, Edam and Gouda [9,14,17,55].”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [9] 9. Bosset J.O., Collomb M., Sieber R., The aroma composition of Swiss Gruyère cheese. 4. The acidic volatile components and their changes in content during ripening, Lebensm. Wiss. Technol. 26 (1993) 581-592. source
    • cites [14] 14. Christensen J.E., Dudley E.G., Pederson J.A., Steele J.L., Peptidases and amino acid catabo- lism in lactic acid bacteria, Antonie van Leeuwenhoek 76 (1999) 217-246. source
    • cites [17] 17. Dirinck P., De Winne A., Flavour characterisa- tion and classification of cheeses by gas chro- matographic-mass spectrometric profiling, J. Chromatogr. 847 (1999) 203-208.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [55] 55. Schormüller J., The chemistry and biochemistry of cheese ripening, Adv. Food Res. 16 (1968) 231-334. source
  • May combine two claims.

    Premisecitation

    The kinetics of isovaleric acid production in YEL medium for two P. freudenreichii strains: it was produced throughout growth, concomitantly with lactate fermentation.

    “The kinetics of isovaleric acid production was determined in YEL medium for two P. freudenreichii strains: it was produced throughout growth, concomitantly with lactate fermentation [59].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [59] 59. Thierry A., Maillard M.B., Yvon M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL34 and ITGP23, Appl. Environ. Microbiol. Vol. 68 (2002) (in press).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation

    After lactate exhaustion, growth stopped while isovaleric acid further increased.

    “After lactate exhaustion, growth stopped while isovaleric acid further increased.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [59] 59. Thierry A., Maillard M.B., Yvon M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL34 and ITGP23, Appl. Environ. Microbiol. Vol. 68 (2002) (in press).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    The amino acid catabolism pathways in PAB share similarities with those of lactic acid bacteria.

    “The amino acid catabolism pathways in PAB share similarities with those of lactic acid bacteria”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    The production of branched-chain acids seems to be a common feature in PAB and was observed in different culture media.

    “The production of branchedchain acids seems to be a common feature in PAB and was observed in different culture media.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    DMDS and DMTS can be formed by auto-oxidation of methanethiol.

    “DMDS and DMTS can be formed by auto-oxidation of methanethiol [64].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [64] 64. Weimer B., Seefeldt K., Dias B., Sulfur metabo- lism in bacteria associated with cheese, Antonie van Leeuwenhoek 76 (1999) 247-261. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Amino acids can be catabolised by several reactions: deamination, decarboxylation, oxidative desamination, transamination and elimination.

    “Amino acids can be catabolised by several reactions: deamination, decarboxylation, oxidative desamination, transamination and elimination [14,55,67].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [14] 14. Christensen J.E., Dudley E.G., Pederson J.A., Steele J.L., Peptidases and amino acid catabo- lism in lactic acid bacteria, Antonie van Leeuwenhoek 76 (1999) 217-246. source
    • cites [55] 55. Schormüller J., The chemistry and biochemistry of cheese ripening, Adv. Food Res. 16 (1968) 231-334. source
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The presence of aminotransferase activities was expected in PAB, at least for the strains able to synthesise amino acids.

    “Therefore, the presence of aminotransferase activities was expected in PAB, at least for the strains able to synthesise amino acids.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Cystathionine β-lyase or cystathionine γ-lyase were found in Lactococcus lactis and several lactobacillus species: Lb. fermentum, Lb. helveticus and Lb. casei.

    “These enzymes were found in Lactococcus lactis and several lactobacillus species: Lb. fermentum, Lb. helveticus and Lb.casei [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
    • Rests on an assumption: Elimination of methionine can also be catalysed by nonspecific enzymes: cystathionine β-lyase or cystathionine γ-lyase.
  • May combine two claims.

    Interpretationcitation

    Phenylacetic acid and benzaldehyde can originate from non-enzymatic degradation of phenylpyruvic acid, whereas benzoic acid can result from further oxidisation of benzaldehyde.

    “Phenylacetic acid and benzaldehyde can originate from non-enzymatic degradation of phenylpyru-vic acid, whereas benzoic acid can result from further oxidisation of benzaldehyde [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
    • Rests on an assumption: The α-keto acids derived from amino acids can be further converted by enzymatic or non-enzymatic reactions by cheese micro-organisms.
  • May combine two claims.

    Interpretationnone given

    Branched-chain α-ketoacids appear to be mainly converted into acids by PAB, whereas higher proportions of hydroxyacids are produced by lactococci.

    “They appear, at least for those of branched-chain amino acids, to be mainly converted into acids by PAB, whereas higher proportions of hydroxyacids are produced by lactococci.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Premisenone given

    Aminotransferases are pyridoxal 5'phosphate (PLP)-dependant enzymes widely distributed in bacteria, where they are involved in the first step of catabolism of some amino acids and also in the last step of their synthesis.

    “Aminotransferases are pyridoxal 5'phosphate (PLP)-dependant enzymes widely distributed in bacteria, where they are involved in the first step of catabolism of some amino acids and also in the last step of their synthesis.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Pyruvate dehydrogenase activity has been found in PAB.

    “Pyruvate dehydrogenase activity has been found in PAB but it is not known whether this complex is active on other α-ketoacids [4].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] 4. Beck S., Schink B., Acetate oxidation through a modified citric acid cycle in Propionibacterium freudenreichii, Arch. Microbiol. 163 (1995) 182-187. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    α-ketoacid dehydrogenase complexes have been found in numerous organisms, including L. lactis.

    “α-ketoacid dehydrogenase complexes have been found in numerous organisms, including L. lactis [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Kiuru observed an odour described as 'old Emmental cheese' after 8 d incubation of resting cells of PAB.

    “The formation of an odour described as”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [32] 32. Kiuru V.J.T., Über die Propionsäuregärung in bezug auf Emmentaler Käse, Ph.D. thesis, Uni- versity of Helsinki, Finland (1949).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    Known pathways of catabolism of branched-chain amino acids and methionine in P. freudenreichii are as shown in Figure 1.

    “Known pathways of catabolism of branched-chain amino acids and methionine in P. freudenreichii (thick arrows).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Methionine γ-lyase was recently purified and characterised in Brevibacterium linens, where it is active under pH, salt and temperature conditions which exist during the ripening of Cheddar cheese.

    “Methionine γ -lyase has not been found in lactic acid bacteria, but was recently purified and characterised in Brevibacterium linens, where it is active under pH, salt and temperature conditions which exist during the ripening of Cheddar cheese [64].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [64] 64. Weimer B., Seefeldt K., Dias B., Sulfur metabo- lism in bacteria associated with cheese, Antonie van Leeuwenhoek 76 (1999) 247-261. source
    • Rests on an assumption: Elimination of methionine can be catalysed by a PLP-dependent enzyme, methionine γ-lyase.
  • May combine two claims.

    Premisecitation

    These reactions lead to the corresponding hydroxy acids, carboxylic acids with one carbon atom less, and aldehydes with one or two carbon atoms less.

    “These reactions lead to the corresponding hydroxy acids, carboxylic acids with one carbon atom less, and aldehydes with one or two carbon atoms less [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
    • Rests on an assumption: The α-keto acids derived from amino acids can be further converted by enzymatic or non-enzymatic reactions by cheese micro-organisms.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Leu aminotransferase activity of PAB is enhanced at pH 8.0.

    “Leu aminotransferase activity of PAB was enhanced at pH 8.0, as generally observed for these enzymes [67].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] 67. Yvon M., Rijnen L., Cheese flavour formation by amino acid catabolism, Int. Dairy J. 11 (2001) 185-201. source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Two enzymes have been partially purified: aspartase and alanine dehydrogenase, respectively involved in the formation of fumarate from Asp and pyruvate from Ala.

    “Two enzymes have been partially purified: aspartase and alanine dehydrogenase, respectively involved in the formation of fumarate from Asp and pyruvate from Ala [16].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] 16. Crow V.L., Properties of alanine dehydrogenase and aspartase from Propionibacterium freudenreichii subsp. shermanii, Appl. Environ. Microbiol. 53 (1987) 1885-1892. source
  • May combine two claims.

    Interpretationreasoning

    The catabolism of these amino acids could have an indirect effect on cheese flavour by modifying the ratio of acids produced from lactate fermentation and by inducing pH variations.

    “Their catabolism could therefore have an indirect effect on cheese flavour by modifying the ratio of acids produced from lactate fermentation and by inducing pH variations.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Low amounts of branched-chain alcohols (< 2 mg/L) were also produced by PAB, but branched-chain aldehydes and α-hydroxyacids were not detected under the conditions used.

    “Low amounts of branched-chain alcohols (< 2 mg .L -1 ) were also produced by PAB, but branched-chain aldehydes and α-hydroxyacids were not detected under the conditions used [59].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [59] 59. Thierry A., Maillard M.B., Yvon M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL34 and ITGP23, Appl. Environ. Microbiol. Vol. 68 (2002) (in press).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • Rests on an assumption: The α-keto acids derived from amino acids can be further converted by enzymatic or non-enzymatic reactions by cheese micro-organisms.
  • May combine two claims.

    Interpretationcitation

    It could be the same for PAB, since the addition of α-KG to YEL cultures enhanced the production of isovaleric acid by PAB.

    “It could be the same for PAB, since it was shown that the addition of α-KG to YEL cultures enhanced the production of isovaleric acid by PAB [59].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [59] 59. Thierry A., Maillard M.B., Yvon M., Conversion of L-leucine to isovaleric acid by Propionibacterium freudenreichii TL34 and ITGP23, Appl. Environ. Microbiol. Vol. 68 (2002) (in press).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The occurrence of transamination in cheese was shown early.

    “The occurrence of transamination in cheese was shown early [55].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [55] 55. Schormüller J., The chemistry and biochemistry of cheese ripening, Adv. Food Res. 16 (1968) 231-334. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Aminotransferase activity on branched-chain amino acids was found in P. jensenii.

    “Aminotransferase activity on branchedchain amino acids was also found in P. jensenii [31].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] 31. Kinney R.W., Werkman C.H., Transamination in Propionibacterium jensenii, Iowa State Coll. J. Sci. 32 (1958) 455-461.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Interpretationcitation

    Most of these compounds are found in very different cheeses, suggesting that they can be produced by various flora.

    “Most of these compounds are found in very different cheeses, suggesting that they can be produced by various flora [20,37]”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [20] 20. Engels W.J.M., Dekker R., De Jong C., Neeter R., Visser S., A comparative study of volatile compounds in the water-soluble fraction of vari- ous types of ripened cheese, Int. Dairy J. 7 (1997) 255-263. source
    • cites [37] 37. Maarse H., Visscher C.A., Willemsens L.C., Nijssen L.M., Boelens M.H., in: Volatile Com- pounds in Food: qualitative and quantitative data, TNO Nutrition and Food Research, Zeist, The Netherlands, 1994.

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

47 of 47
  • The paper relies on this without support.

    The odour threshold values used (in water, milk, or cheese) are applicable to the cheese matrix for assessing the flavour impact of the compounds.

    “These data show that isovaleric acid was the most potential branched-chain aroma in Swiss cheese, with a concentration ~600-times higher than its odour threshold in water (0.07 mg .L -1 , [12]).”
  • The paper relies on this without support.

    The PAB strains used in the cheese experiments are representative of PAB in general.

    “PAB reached 6 × 10 9 cfu .g -foot_0 in the inoculated cheeses, whereas indigenous PAB remained under 5 × 10 6 cfu .g -1 at the end of ripening in control ones [25].”
  • The paper relies on this without support.

    α,γ-elimination of methionine leads to methanethiol, ammonia and α-ketobutyric acid.

    “This one-step degradation leads to methanethiol, ammonia and α-ketobutyric acid.”
  • The paper relies on this without support.

    Elimination of methionine can be catalysed by a PLP-dependent enzyme, methionine γ-lyase.

    “Elimination of methionine can be catalysed by a PLP-dependent enzyme, methionine γ -lyase (EC.4.4.1.11,also referred to as methionine γ -demethiolase).”
  • The paper relies on this without support.

    Elimination of methionine can also be catalysed by nonspecific enzymes: cystathionine β-lyase or cystathionine γ-lyase.

    “Elimination of methionine can also be catalysed by nonspecific enzymes: cystathionine β-lyase or cystathionine γ -lyase.”
  • The paper relies on this without support.

    Two pathways can lead to the production of branched-chain acid from branched-chain α-ketoacids.

    “Two pathways can lead to the production of branched-chain acid from branchedchain α-ketoacids.”
  • The paper relies on this without support.

    The first pathway is oxidative decarboxylation via a branched-chain α-ketoacid dehydrogenase complex yielding branched-chain acyl-CoA, which can then be converted to the acid.

    “The first is oxidative decarboxylation via a branched-chain α-ketoacid dehydrogenase complex (EC 1.2.4.4), yielding branched-chain acyl-CoA, which can then be converted to the acid.”
  • The paper relies on this without support.

    The second pathway is non-oxidative decarboxylation by pyruvate decarboxylase or a pyruvate decarboxylase-like enzyme to yield aldehyde, which could be further converted to the acid.

    “The second is non-oxidative decarboxylation by pyruvate decarboxylase (EC 4.1.1.1)or a pyruvate decarboxylase-like enzyme to yield aldehyde, which could be further converted to the acid.”
  • The paper relies on this without support.

    The predominant fatty acid in P. freudenreichii is anteiso C15 (12-methyltetradecanoic acid), which is structurally related to Ile and whose synthesis is enhanced by addition of Ile to culture medium.

    “The predominant fatty acid in P. freudenreichii is anteiso C 15 (12methyltetradecanoic acid), which is structurally related to Ile and whose synthesis is enhanced by addition of Ile to culture medium.”
  • The paper relies on this without support.

    The α-keto acids derived from amino acids can be further converted by enzymatic or non-enzymatic reactions by cheese micro-organisms.

    “The α-keto acids derived from amino acids can be further converted by enzymatic or non-enzymatic reactions by cheese micro-organisms.”
10 of 10

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Morbier DMTS is described as unaffected despite a significant difference

    Minor

    The text says DMTS was not significantly affected by PAB in Morbier cheese, but Table III assigns different significance letters to the control and ITGP10 values. The table's note says values without a common letter differ significantly.

1 of 1

Cites

Flagged first, then by citations

2 of the 71 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

  1. [25]25. Hervé C., Démonstration et étude de la lysogénie de Propionibacterium freudenreichii subsp. shermanii, Ph.D. thesis, ENSAR Rennes, France (2000).
  2. [32]32. Kiuru V.J.T., Über die Propionsäuregärung in bezug auf Emmentaler Käse, Ph.D. thesis, Uni- versity of Helsinki, Finland (1949).
  3. [49]49. Preininger M., Rychlik M., Grosch W., Potent odorants of the neutral fraction of Swiss cheese (Emmentaler), in: Maarse H., van der Meij O.G., (Eds), Trends in Flavour Research, Elsevier, Amsterdam, The Netherlands, 1994, pp. 267- 270.
  4. [63]63. Webb J.L., Arsenicals, in: Enzyme and meta- bolic inhibitors, Academic Press, New York, 1966, pp. 595.

Cited by

Sorted by citations

Authors
Thierry, A., & Maillard, M.-B.
Affiliations
Institut National de la Recherche Agronomique (FR)
Venue
Le Lait
Publisher
EDP Sciences
Published
2002-01
Volume
82
Issue
1
Pages
17-32
ISSN
  • 0023-7302 (ISSN-L)
  • 1297-9694
OpenAlex
W2159813542
Cited by
110
References
71
Citations by year
2026: 2 · 2025: 4 · 2024: 4 · 2023: 7 · 2022: 3 · 2020: 5 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 2 · 2015: 8 · 2014: 4 · 2013: 1 · 2012: 8
FWCI
13.69
Type
journal article
Language
en
Open access
Locations
Le Lait (publishedVersion)
Funders
Ministère de l'Éducation Nationale
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Biochemical and biochemical processes
Keywords
cheese flavor, Propionibacterium freudenreichii, amino acid catabolism, volatile flavor compounds, branched-chain amino acids, methionine degradation, leucine, isovaleric acid, alpha-ketoisocaproate, phenylpyruvic acid, transaminases, methanethiol, cheese ripening, lactic acid bacteria

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Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-11.

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