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Genome Biol Evol. 2014 Jun 19;6(7):1772-89. doi: 10.1093/gbe/evu137.

From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions.

Author information

1
Texas Children's Microbiome Center, Department of Pathology, Texas Children's Hospital, Houston, TXDepartment of Pathology & Immunology, Baylor College of Medicine, Houston, TX spinler@bcm.edu.
2
Texas Children's Microbiome Center, Department of Pathology, Texas Children's Hospital, Houston, TXDepartment of Pathology & Immunology, Baylor College of Medicine, Houston, TX.
3
Department of Food Science and Technology, University of Nebraska, Lincoln.
4
Department of Molecular Virology & Microbiology, Baylor College of Medicine, Houston, TX.
5
Texas Children's Microbiome Center, Department of Pathology, Texas Children's Hospital, Houston, TXDepartment of Pathology & Immunology, Baylor College of Medicine, Houston, TXPresent address: Department of Gastrointestinal Microbiology, German Institute of Human Nutrition, Nuthetal, Germany.
6
Department of Food Science and Technology, University of Nebraska, LincolnPresent address: Departments of Agricultural, Food, & Nutritional Science and Biological Sciences, University of Alberta, Edmonton, AB, Canada.
7
Texas Children's Microbiome Center, Department of Pathology, Texas Children's Hospital, Houston, TXDepartment of Pathology & Immunology, Baylor College of Medicine, Houston, TXDepartment of Molecular Virology & Microbiology, Baylor College of Medicine, Houston, TX.
8
Department of Molecular Virology & Microbiology, Baylor College of Medicine, Houston, TXHuman Genome Sequencing Center, Baylor College of Medicine, Houston, TXPresent address: Genomic Medicine, J. Craig Venter Institute, La Jolla, CA.

Abstract

The vertebrate gut symbiont Lactobacillus reuteri has diversified into separate clades reflecting host origin. Strains show evidence of host adaptation, but how host-microbe coevolution influences microbial-derived effects on hosts is poorly understood. Emphasizing human-derived strains of L. reuteri, we combined comparative genomic analyses with functional assays to examine variations in host interaction among genetically distinct ecotypes. Within clade II or VI, the genomes of human-derived L. reuteri strains are highly conserved in gene content and at the nucleotide level. Nevertheless, they share only 70-90% of total gene content, indicating differences in functional capacity. Human-associated lineages are distinguished by genes related to bacteriophages, vitamin biosynthesis, antimicrobial production, and immunomodulation. Differential production of reuterin, histamine, and folate by 23 clade II and VI strains was demonstrated. These strains also differed with respect to their ability to modulate human cytokine production (tumor necrosis factor, monocyte chemoattractant protein-1, interleukin [IL]-1β, IL-5, IL-7, IL-12, and IL-13) by myeloid cells. Microarray analysis of representative clade II and clade VI strains revealed global regulation of genes within the reuterin, vitamin B12, folate, and arginine catabolism gene clusters by the AraC family transcriptional regulator, PocR. Thus, human-derived L. reuteri clade II and VI strains are genetically distinct and their differences affect their functional repertoires and probiotic features. These findings highlight the biological impact of microbe:host coevolution and illustrate the functional significance of subspecies differences in the human microbiome. Consideration of host origin and functional differences at the subspecies level may have major impacts on probiotic strain selection and considerations of microbial ecology in mammalian species.

KEYWORDS:

PocR transcriptional regulation; anti-inflammatory; histamine; host-based evolution; immunostimulatory; reuterin

PMID:
24951561
PMCID:
PMC4122935
DOI:
10.1093/gbe/evu137
[Indexed for MEDLINE]
Free PMC Article
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