The Secreted Esterase of Propionibacterium freudenreichii Has a Major Role in Cheese Lipolysis

Mukdsi, María Claudia Abeijón; Falentin, Hélène; Maillard, Marie-Bernadette; Chuat, Victoria; Medina, Roxana Beatriz; Parayre, Sandrine; Thierry, Anne

doi:10.1128/aem.03640-13

Cited by 25 publications

(7 citation statements)

References 19 publications

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“…A mutation leading to a premature stop explained the inability of the CIRM-BIA514 and LSP108 strains to produce free fatty acids from milk fat. The genome decay of lactic acid bacteria, and particularly of Lactobacillus helveticus, has also been fully documented [ 28 , 29 ] and linked t domestication over several centuries of yoghurt fermentation.…”

Section: Discussionmentioning

confidence: 99%

Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii

et al. 2015

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BackgroundPropionibacterium freudenreichii (PF) is an actinobacterium used in cheese technology and for its probiotic properties. PF is also extremely adaptable to several ecological niches and can grow on a variety of carbon and nitrogen sources. The aim of this work was to discover the genetic basis for strain-dependent traits related to its ability to use specific carbon sources. High-throughput sequencing technologies were ideal for this purpose as they have the potential to decipher genomic diversity at a moderate cost.Results21 strains of PF were sequenced and the genomes were assembled de novo. Scaffolds were ordered by comparison with the complete reference genome CIRM-BIA1, obtained previously using traditional Sanger sequencing. Automatic functional annotation and manual curation were performed. Each gene was attributed to either the core genome or an accessory genome. The ability of the 21 strains to degrade 50 different sugars was evaluated. Thirty-three sugars were degraded by none of the sequenced strains whereas eight sugars were degraded by all of them. The corresponding genes were present in the core genome. Lactose, melibiose and xylitol were only used by some strains. In this case, the presence/absence of genes responsible for carbon uptake and degradation correlated well with the phenotypes, with the exception of xylitol. Furthermore, the simultaneous presence of these genes was in line the metabolic pathways described previously in other species. We also considered the genetic origin (transduction, rearrangement) of the corresponding genomic islands. Ribose and gluconate were degraded to a greater or lesser extent (quantitative phenotype) by some strains. For these sugars, the phenotypes could not be explained by the presence/absence of a gene but correlated with the premature appearance of a stop codon interrupting protein synthesis and preventing the catabolism of corresponding carbon sources.ConclusionThese results illustrate (i) the power of correlation studies to discover the genetic basis of binary strain-dependent traits, and (ii) the plasticity of PF chromosomes, probably resulting from horizontal transfers, duplications, transpositions and an accumulation of mutations. Knowledge of the genetic basis of nitrogen and sugar degradation opens up new strategies for the screening of PF strain collections to enable optimum cheese starter, probiotic and white biotechnology applications.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1467-7) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii

et al. 2015

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“…Similar mechanisms may explain the very diverse phenotypes observed concerning the production of aroma compounds. The different strains tested did not group together, but rather exhibited a continuum in their ability to produce aroma compounds, as previously observed for 2-methylbutanoic acid (Dherbécourt et al 2008 ) and also for free fatty acids coming from lipolysis (Abeijon Mukdsi et al 2014 ).…”

Section: Discussionmentioning

confidence: 59%

“…The four lac/nit phenotypes corresponding to the different combinations of lac/nit phenotypes were not distinguished by the production of any of the aroma compounds analysed. The aroma profile reflects the metabolic activity of the cells, since aroma compounds are synthesized via different pathways involving enzymes such as esterases and amino acid-converting enzymes (Abeijon Mukdsi et al 2014 , Thierry et al 2002 ). The pathways of synthesis of these compounds are not related to the pathways of lactose fermentation or nitrate reduction, but these different phenotypic properties may nevertheless have been found correlated.…”

Section: Discussionmentioning

confidence: 99%

“…It produces varied aroma compound in cheese from lactate fermentation, amino acid catabolism, and milk fat hydrolysis, and CO 2 . These products significantly contribute to the development of the typical flavour and the formation of eyes in Swiss-type cheeses (Thierry et al 2011 , Abeijon Mukdsi et al 2014 ). The production of aroma compounds is highly strain-dependent (Yee et al 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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New insights about phenotypic heterogeneity within Propionibacterium freudenreichii argue against its division into subspecies

Freitas

Madec

Chuat

et al. 2015

Dairy Sci. & Technol.

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Propionibacterium freudenreichii is widely used in Swiss-type cheese manufacture, where it contributes to flavour and eye development. It is currently divided into two subspecies, according to the phenotype for lactose fermentation and nitrate reduction (lac+/nit− and lac−/nit+ for P. freudenreichii subsp. shermanii and subsp. freudenreichii, respectively). However, the existence of unclassifiable strains (lac+/nit+ and lac−/nit−) has also been reported. The aim of this study was to revisit the relevance of the subdivision of P. freudenreichii into subspecies, by confirming the existence of unclassifiable strains. Relevant conditions to test the ability of P. freudenreichii for lactose fermentation and nitrate reduction were first determined, by using 10 sequenced strains, in which the presence or absence of the lactose and nitrate genomic islands were known. We also determined whether the subdivision based on lac/nit phenotype was related to other phenotypic properties of interest in cheese manufacture, in this case, the production of aroma compounds, analysed by gas chromatography-mass spectrometry, for a total of 28 strains. The results showed that a too short incubation time can lead to false negative for lactose fermentation and nitrate reduction. They confirmed the existence of four lac/nit phenotypes instead of the two expected, thus leading to 13 unclassifiable strains out of the 28 characterized (7 lac+/nit+ and 6 lac−/nit−). The production of the 15 aroma compounds detected in all cultures varied more within a lac/nit phenotype (up to 20 times) than between them. Taken together, these results demonstrate that the division of P. freudenreichii into two subspecies does not appear to be relevant.

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“…The role of autolysed LAB in lipolysis has been demonstrated in cheddar cheese [ 28 ]. Also secreted esterase was found to impact lipolysis in cheese [ 29 ]. Peptide degradation by released peptides plays a role in debittering of the ripening cheese, thereby affecting primarily the taste of the product [ 30 ].…”

Section: Introductionmentioning

confidence: 99%

Functional implications of the microbial community structure of undefined mesophilic starter cultures

et al. 2014

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This review describes the recent advances made in the studies of the microbial community of complex and undefined cheese starter cultures. We report on work related to the composition of the cultures at the level of genetic lineages, on the presence and activity of bacteriophages and on the population dynamics during cheese making and during starter culture propagation. Furthermore, the link between starter composition and starter functionality will be discussed. Finally, recent advances in predictive metabolic modelling of the multi-strain cultures will be discussed in the context of microbe-microbe interactions.

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The Secreted Esterase of Propionibacterium freudenreichii Has a Major Role in Cheese Lipolysis

Cited by 25 publications

References 19 publications

Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii

Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii

New insights about phenotypic heterogeneity within Propionibacterium freudenreichii argue against its division into subspecies

Functional implications of the microbial community structure of undefined mesophilic starter cultures

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