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Open Access Highly Accessed Research article

Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation

Jeff R Broadbent1*, Eric C Neeno-Eckwall2, Buffy Stahl3, Kanokwan Tandee4, Hui Cai45, Wesley Morovic3, Philippe Horvath6, Jessie Heidenreich4, Nicole T Perna7, Rodolphe Barrangou3 and James L Steele4

Author affiliations

1 Utah State University Department of Nutrition, Dietetics, and Food Sciences, 8700 Old Main Hill, Logan, UT 84322-8700, USA

2 University of Wisconsin Biotechnology Center, 425 Henry Mall, Madison, WI, 53706-1580, USA

3 DuPont Nutrition and Health, 3329 Agriculture Drive, Madison, WI, 53716, USA

4 University of Wisconsin Department of Food Science, 1605 Linden Drive, Madison, WI, 53706-1565, USA

5 Present address: PPD Inc, 466 Devon Park Dr, Wayne, PA, 19087, USA

6 DuPont Nutrition and Health, BP10, F-86220, Dangé-Saint-Romain, France

7 University of Wisconsin Laboratory of Genetics, 425 Henry Mall, Madison, WI, 53706-1580, USA

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Citation and License

BMC Genomics 2012, 13:533  doi:10.1186/1471-2164-13-533

Published: 5 October 2012

Abstract

Background

The broad ecological distribution of L. casei makes it an insightful subject for research on genome evolution and lifestyle adaptation. To explore evolutionary mechanisms that determine genomic diversity of L. casei, we performed comparative analysis of 17 L. casei genomes representing strains collected from dairy, plant, and human sources.

Results

Differences in L. casei genome inventory revealed an open pan-genome comprised of 1,715 core and 4,220 accessory genes. Extrapolation of pan-genome data indicates L. casei has a supragenome approximately 3.2 times larger than the average genome of individual strains. Evidence suggests horizontal gene transfer from other bacterial species, particularly lactobacilli, has been important in adaptation of L. casei to new habitats and lifestyles, but evolution of dairy niche specialists also appears to involve gene decay.

Conclusions

Genome diversity in L. casei has evolved through gene acquisition and decay. Acquisition of foreign genomic islands likely confers a fitness benefit in specific habitats, notably plant-associated niches. Loss of unnecessary ancestral traits in strains collected from bacterial-ripened cheeses supports the hypothesis that gene decay contributes to enhanced fitness in that niche. This study gives the first evidence for a L. casei supragenome and provides valuable insights into mechanisms for genome evolution and lifestyle adaptation of this ecologically flexible and industrially important lactic acid bacterium. Additionally, our data confirm the Distributed Genome Hypothesis extends to non-pathogenic, ecologically flexible species like L. casei.

Keywords:
Lactobacillus casei; Lactic acid bacteria; Comparative genomics; Pan-genome; Supragenome; Evolution; Adaptation