title: Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii.
abstract: BACKGROUND
  Propionibacterium 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.
  
  
  RESULTS
  21 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.
  
  
  CONCLUSIONS
  These 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.
authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. valentin.loux@jouy.inra.fr.
authors.forename: Valentin
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authors.lastname: Loux
authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. mahendra.mariadassou@jouy.inra.fr.
authors.forename: Mahendra
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authors.lastname: Mariadassou
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. sintiaalmeida@gmail.com.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. sintiaalmeida@gmail.com.|Sciences, Federal University of Minas Gerais Belo Horizonte, Minas Gerais, Brazil. sintiaalmeida@gmail.com.
authors.forename: Sintia
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authors.lastname: Almeida
authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. helene.chiapello@toulouse.inra.fr.
authors.forename: Hélène
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authors.lastname: Chiapello
authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. amal.hammani@gmail.com.
authors.forename: Amal
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authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. julien.buratti@gmail.com.
authors.forename: Julien
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authors.affiliation: INRA Mathématique Informatique et Génome, France Institute of Biological, Jouy en Josas, 78352, France. annie.gendrault@jouy.inra.fr.
authors.forename: Annie
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authors.affiliation: CEA Genoscope CNRS and université d'Evry, Evry, 91006, France. vbarbe@genoscope.cns.fr.
authors.forename: Valérie
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authors.affiliation: CEA Genoscope CNRS and université d'Evry, Evry, 91006, France. jmaury@genoscope.cns.fr.
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Aury
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. stephanie-marie.deutsch@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. stephanie-marie.deutsch@rennes.inra.fr.
authors.forename: Stéphanie-Marie
authors.initials: SM
authors.lastname: Deutsch
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. sandrine.parayre@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. sandrine.parayre@rennes.inra.fr.
authors.forename: Sandrine
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authors.lastname: Parayre
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. marie-noelle.madec@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. marie-noelle.madec@rennes.inra.fr.
authors.forename: Marie-Noëlle
authors.initials: MN
authors.lastname: Madec
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. victoria.chuat@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. victoria.chuat@rennes.inra.fr.
authors.forename: Victoria
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authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. gwenael.jan@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. gwenael.jan@rennes.inra.fr.
authors.forename: Gwenaël
authors.initials: G
authors.lastname: Jan
authors.affiliation: INRIA Campus de Beaulieu- Rennes, Rennes Cedex, 35042, France. pierre.peterlongo@inria.fr.
authors.forename: Pierre
authors.initials: P
authors.lastname: Peterlongo
authors.affiliation: Sciences, Federal University of Minas Gerais Belo Horizonte, Minas Gerais, Brazil. vascoariston@gmail.com.
authors.forename: Vasco
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authors.lastname: Azevedo
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. yves.leloir@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. yves.leloir@rennes.inra.fr.
authors.forename: Yves
authors.initials: Y
authors.lastname: Le Loir
authors.affiliation: INRA, UMR 1253, Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. helene.falentin@rennes.inra.fr.|AGROCAMPUS OUEST, UMR1253, UMR Science et Technologie du Lait et de l'Oeuf, Rennes, 35000, France. helene.falentin@rennes.inra.fr.
authors.forename: Hélène
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mesh_terms: D050260:Carbohydrate Metabolism / Q000235:genetics*; D002611:Cheese / Q000382:microbiology; D004269:DNA, Bacterial / Q000032:analysis / Q000302:isolation & purification / Q000378:metabolism; D016680:Genome, Bacterial; D044404:Genomic Islands / Q000235:genetics*; D059014:High-Throughput Nucleotide Sequencing; D053858:Metabolic Networks and Pathways / Q000235:genetics; D009154:Mutation; D009566:Nitrates / Q000378:metabolism; D010641:Phenotype; D010802:Phylogeny; D011424:Propionibacterium / Q000145:classification / Q000235:genetics*; D017422:Sequence Analysis, DNA; D013045:Species Specificity
chemical_list: D004269:DNA, Bacterial; D009566:Nitrates