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

Valentin Loux (1) , Mahendra Mariadassou (1) , Sintia Almeida (2) , Hélène Chiapello (1) , Amal Hammani (3) , Julien Buratti (1) , Annie Gendrault (1) , Valérie Barbe (4) , Jean-Marc Aury (5) , Stéphanie-Marie Deutsch (6) , Sandrine Parayre (6) , Marie-Noëlle Madec (6) , Victoria Chuat (6) , Gwénaël Jan (6) , Pierre Peterlongo (7) , Vasco Azevedo (8) , Yves Le Loir (6) , Hélène Falentin (6)

1 MIG - Unité Mathématique Informatique et Génome
2 IFSC, Curso Tecn Saneamento, BR-88020300 Florianopolis, SC, Brazil
3 IAV Hassan II - Institut Agronomique et Vétérinaire Hassan II
4 IG - Institut de Génomique d'Evry
5 LBGB - Laboratoire de Bioinformatique pour la Génomique et la Biodiversité
6 STLO - Science et Technologie du Lait et de l'Oeuf
7 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics
8 UFMG - Universidade Federal de Minas Gerais = Federal University of Minas Gerais [Belo Horizonte, Brazil]

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 duration 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 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. Conclusion 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.

Mots clés: propionibacterium freudenreichii; sucre

Mots clés: génomique; mutation; génotype; phénotype; dégradation

Domaines: Bio-Informatique, Biologie Systémique [q-bio.QM]; Génomique, Transcriptomique et Protéomique [q-bio.GN]; Recherche d'information [cs.IR]

Valentin Loux, Mahendra Mariadassou, Sintia Almeida, Hélène Chiapello, Amal Hammani, et al.. Mutations and genomic islands can explain the strain dependency of sugar utilization in 21 strains of Propionibacterium freudenreichii. BMC Genomics, 2015, 16 (1), pp.35. ⟨10.1186/s12864-015-1467-7⟩. ⟨hal-01142363⟩