Genes but Not Genomes Reveal Bacterial Domestication of Lactococcus Lactis

Abstract

BackgroundThe 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 FindingsThe 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/SignificanceThe 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.

High Genetic Diversity among Strains of the Unindustrialized Lactic Acid Bacterium Carnobacterium maltaromaticum in Dairy Products as Revealed by Multilocus Sequence Typing

“…Indeed, approximately the same nucleotide diversity () was found between the dairy strains and the strains originating from all other environments, including other food product categories, soil, and live fish. It was previously described for Lactococcus lactis that diversity of strains originating from raw milk was dramatically higher than in cheese opening the possibility for a strong bias in our study (5). However, when we removed the strains isolated from raw milk, no drastic diversity reduction was recorded, indicating that the high diversity was not biased by these strains.…”

“…Within the species Streptococcus thermophilus a low diversity was recorded compared to the closely related species of the salivarius group that share other ecological niches (4). Similarly, Lactococcus lactis strains originating from cheeses exhibit a strikingly low diversity compared to the strains isolated either from raw milk or nondairy environments (5,6). The relative low level of diversity is not restricted to starter LAB since the industrialized species Lactobacillus casei, a nonstarter LAB, exhibit a relatively low level of diversity as well (7).…”

Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution

“…Most food fermentations originate from ancient processes dating back to the introduction of agriculture and animal husbandry ;10,000 years ago (Campbell-Platt 1994). Dairy lactococci have been proposed to have evolved from typical plant isolates Siezen et al 2005;van Hylckama Vlieg et al 2006;Siezen et al 2008;Kelly et al 2010;Passerini et al 2010). The genome sequence of a L. lactis plant isolate revealed several genes that relate to the utilization of plant polymers and are absent in dairy isolates (Siezen et al 2008).…”

Optimisation of Cell Bioenergetics in Food-Associated Microorganisms

“…Milk, the proposed evolutionary environmental niche for the LAB Streptococcus thermophilus, Lactobacillus delbrueckii subsp. bulgaricus, and the "domesticated" strains of Lactococcus lactis (Bolotin et al, 2004;van de Guchte, 2006;Passerini et al, 2010), and the man-made niches, grape juice, has driven the evolution of the domesticated strains of S. cerevisiae (Martini, 1993, Fay & Benavides, 2005. These two are environments in which mono-and disaccharides resources are both large and dense.…”