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Genes but not genomes reveal bacterial domestication of Lactococcus lactis.

ABSTRACT: BACKGROUND: The population structure and diversity of Lactococcus lactis subsp. lactis, a major industrial bacterium involved in milk fermentation, was determined at both gene and genome level. Seventy-six lactococcal isolates of various origins were studied by different genotyping methods and thirty-six strains displaying unique macrorestriction fingerprints were analyzed by a new multilocus sequence typing (MLST) scheme. This gene-based analysis was compared to genomic characteristics determined by pulsed-field gel electrophoresis (PFGE). METHODOLOGY/PRINCIPAL FINDINGS: The MLST analysis revealed that L. lactis subsp. lactis is essentially clonal with infrequent intra- and intergenic recombination; also, despite its taxonomical classification as a subspecies, it displays a genetic diversity as substantial as that within several other bacterial species. Genome-based analysis revealed a genome size variability of 20%, a value typical of bacteria inhabiting different ecological niches, and that suggests a large pan-genome for this subspecies. However, the genomic characteristics (macrorestriction pattern, genome or chromosome size, plasmid content) did not correlate to the MLST-based phylogeny, with strains from the same sequence type (ST) differing by up to 230 kb in genome size. CONCLUSION/SIGNIFICANCE: The gene-based phylogeny was not fully consistent with the traditional classification into dairy and non-dairy strains but supported a new classification based on ecological separation between "environmental" strains, the main contributors to the genetic diversity within the subspecies, and "domesticated" strains, subject to recent genetic bottlenecks. Comparison between gene- and genome-based analyses revealed little relationship between core and dispensable genome phylogenies, indicating that clonal diversification and phenotypic variability of the "domesticated" strains essentially arose through substantial genomic flux within the dispensable genome.

SUBMITTER: Passerini D

PROVIDER: S-EPMC3003715 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Genes but not genomes reveal bacterial domestication of Lactococcus lactis.

Passerini Delphine D Beltramo Charlotte C Coddeville Michele M Quentin Yves Y Ritzenthaler Paul P Daveran-Mingot Marie-Line ML Le Bourgeois Pascal P

PloS one 20101217 12

<h4>Background</h4>The population structure and diversity of Lactococcus lactis subsp. lactis, a major industrial bacterium involved in milk fermentation, was determined at both gene and genome level. Seventy-six lactococcal isolates of various origins were studied by different genotyping methods and thirty-six strains displaying unique macrorestriction fingerprints were analyzed by a new multilocus sequence typing (MLST) scheme. This gene-based analysis was compared to genomic characteristics d ...[more]

PMID: 21179431

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Project description:Lactococcus lactis (L. lactis) is a well isolated and cultured lactic acid bacterium, but if utilizing the isolate genomes alone, the genome-based analysis of this taxon would be incomplete, because there are still uncultured strains in some ecological niches. In this study, we recovered 93 high-quality metagenome-assembled genomes (MAGs) of L. lactis from food and human gut metagenomes with a culture-independent method. We then constructed a unified genome catalog of L. lactis by integrating these MAGs with 70 publicly available isolated genomes. Having this comprehensive resource, we assessed the genomic diversity and phylogenetic relationships to further explore the genetic and functional properties of L. lactis. An open pangenome of L. lactis was generated using our genome catalog, consisting of 13,066 genes in total, from which 5,448 genes were not identified in the isolate genomes. The core genome-based phylogenetic analysis showed that L. lactis strains we collected were separated into two main subclades corresponding to two subspecies, with some uncultured phylogenetic lineages discovered. The species disparity was also indicated in PCA analysis based on accessory genes of our pangenome. These various analyzes shed further light on unexpectedly high diversity within the taxon at both genome and gene levels and gave clues about its population structure and evolution. Lactococcus lactis has a long history of safe use in food fermentations and is considered as one of the important probiotic microorganisms. Obtaining the complete genetic information of L. lactis is important to the food and health industry. However, it can naturally inhabit many environments other than dairy products, including drain water and human gut samples. Here we presented an open pan-genome of L. lactis constructed from 163 high-quality genomes obtained from various environments, including MAGs recovered from environmental metagenomes and isolate genomes. This study expanded the genetic information of L. lactis about one third, including more than 5,000 novel genes found in uncultured strains. This more complete gene repertoire of L. lactis is crucial to further understanding the genetic and functional properties. These properties may be harnessed to impart additional value to dairy fermentation or other industries.

Dataset Information

Genes but not genomes reveal bacterial domestication of Lactococcus lactis.

Publications

Genes but not genomes reveal bacterial domestication of Lactococcus lactis.

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