Functional and Comparative Genomic Analyses of an Operon Involved in Fructooligosaccharide Utilization by Lactobacillus acidophilus

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 100; no. 15; pp. 8957 - 8962
• Main Authors: Barrangou, Rodolphe, Altermann, Eric, Hutkins, Robert, Cano, Raul, Klaenhammer, Todd R.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 22.07.2003; National Acad Sciences
• Subjects: ATP binding cassette transporters; ATP-Binding Cassette Transporters - genetics; ATP-Binding Cassette Transporters - metabolism; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Base Sequence; Biological Sciences; Biological Transport, Active; Chromosome Mapping; Comparative analysis; DNA, Bacterial - genetics; Enzymes; Escherichia coli Proteins - genetics; Escherichia coli Proteins - metabolism; Genes; Genetic loci; Genome, Bacterial; Genomes; Genomics; Lac Repressors; Lactobacillus acidophilus - genetics; Lactobacillus acidophilus - metabolism; Molecular Sequence Data; Multigene Family; Mutation; Oligosaccharides - metabolism; Operon; Operons; Phenotype; Phylogeny; Regulator genes; Repression; Repressor Proteins - genetics; Repressor Proteins - metabolism; RNA; Sequence Homology, Nucleic Acid; Species Specificity; Sugars
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1332765100

Lactobacillus acidophilus is a probiotic organism that displays the ability to use prebiotic compounds such as fructooligosaccharides (FOS), which stimulate the growth of beneficial commensals in the gastrointestinal tract. However, little is known about the mechanisms and genes involved in FOS utilization by Lactobacillus species. Analysis of the L. acidophilus NCFM genome revealed an msm locus composed of a transcriptional regulator of the LacI family, a four-component ATP-binding cassette (ABC) transport system, a fructosidase, and a sucrose phosphorylase. Transcriptional analysis of this operon demonstrated that gene expression was induced by sucrose and FOS but not by glucose or fructose, suggesting some specificity for nonreadily fermentable sugars. Additionally, expression was repressed by glucose but not by fructose, suggesting catabolite repression via two cre-like sequences identified in the promoter-operator region. Insertional inactivation of the genes encoding the ABC transporter substrate-binding protein and the fructosidase reduced the ability of the mutants to grow on FOS. Comparative analysis of gene architecture within this cluster revealed a high degree of synteny with operons in Streptococcus mutans and Streptococcus pneumoniae. However, the association between a fructosidase and an ABC transporter is unusual and may be specific to L. acidophilus. This is a description of a previously undescribed gene locus involved in transport and catabolism of FOS compounds, which can promote competition of beneficial microorganisms in the human gastrointestinal tract.