The Variable Regions of Lactobacillus rhamnosus Genomes Reveal the Dynamic Evolution of Metabolic and Host-Adaptation Repertoires

Corina Ceapa; Mark Davids; Jarmo Ritari; Jolanda Lambert; Michiel Wels; François P Douillard; Tamara Smokvina; Willem M de Vos; Jan Knol; Michiel Kleerebezem

doi:10.1093/gbe/evw123

The Variable Regions of Lactobacillus rhamnosus Genomes Reveal the Dynamic Evolution of Metabolic and Host-Adaptation Repertoires

Genome Biol Evol. 2016 Jul 2;8(6):1889-905. doi: 10.1093/gbe/evw123.

Authors

Affiliations

¹ Gut Biology & Microbiology Platform, Nutricia Research Centre, Utrecht, the Netherlands Laboratory of Microbiology, Wageningen University, the Netherlands corinaceapa@uchicago.edu.
² Laboratory of Systems and Synthetic Biology, Wageningen University, the Netherlands.
³ RPU Immunobiology, Department of Bacteriology and Immunology, University of Helsinki, Finland.
⁴ Gut Biology & Microbiology Platform, Nutricia Research Centre, Utrecht, the Netherlands.
⁵ NIZO Food Research, Ede, the Netherlands.
⁶ Department of Veterinary Biosciences, University of Helsinki, Finland.
⁷ Danone Research, Palaiseau, France.
⁸ Laboratory of Microbiology, Wageningen University, the Netherlands RPU Immunobiology, Department of Bacteriology and Immunology, University of Helsinki, Finland Department of Veterinary Biosciences, University of Helsinki, Finland.
⁹ Gut Biology & Microbiology Platform, Nutricia Research Centre, Utrecht, the Netherlands Laboratory of Microbiology, Wageningen University, the Netherlands.
¹⁰ Host-Microbe Interactomics Group, Department of Animal Sciences, Wageningen University and Research Centre, Wageningen, the Netherlands.

Abstract

Lactobacillus rhamnosus is a diverse Gram-positive species with strains isolated from different ecological niches. Here, we report the genome sequence analysis of 40 diverse strains of L. rhamnosus and their genomic comparison, with a focus on the variable genome. Genomic comparison of 40 L. rhamnosus strains discriminated the conserved genes (core genome) and regions of plasticity involving frequent rearrangements and horizontal transfer (variome). The L. rhamnosus core genome encompasses 2,164 genes, out of 4,711 genes in total (the pan-genome). The accessory genome is dominated by genes encoding carbohydrate transport and metabolism, extracellular polysaccharides (EPS) biosynthesis, bacteriocin production, pili production, the cas system, and the associated clustered regularly interspaced short palindromic repeat (CRISPR) loci, and more than 100 transporter functions and mobile genetic elements like phages, plasmid genes, and transposons. A clade distribution based on amino acid differences between core (shared) proteins matched with the clade distribution obtained from the presence-absence of variable genes. The phylogenetic and variome tree overlap indicated that frequent events of gene acquisition and loss dominated the evolutionary segregation of the strains within this species, which is paralleled by evolutionary diversification of core gene functions. The CRISPR-Cas system could have contributed to this evolutionary segregation. Lactobacillus rhamnosus strains contain the genetic and metabolic machinery with strain-specific gene functions required to adapt to a large range of environments. A remarkable congruency of the evolutionary relatedness of the strains' core and variome functions, possibly favoring interspecies genetic exchanges, underlines the importance of gene-acquisition and loss within the L. rhamnosus strain diversification.

Keywords: comparative genomics; core and pan-genome; diversity; niche adaptation; probiotic.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

CRISPR-Cas Systems
Carbohydrate Metabolism / genetics*
Evolution, Molecular*
Gene Transfer, Horizontal
Genome, Bacterial*
High-Throughput Nucleotide Sequencing
Lacticaseibacillus rhamnosus / genetics*
Molecular Sequence Annotation
Phylogeny

Grants and funding

250172/ERC_/European Research Council/International