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

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 util...

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Published inProceedings 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
LanguageEnglish
Published United States National Academy of Sciences 22.07.2003
National Acad Sciences
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Abstract 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.
AbstractList 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.
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 Lac I 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.
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 Lac I 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.
Author Barrangou, Rodolphe
Altermann, Eric
Cano, Raul
Hutkins, Robert
Klaenhammer, Todd R.
AuthorAffiliation Genomic Sciences Program and Southeast Dairy Foods Research Center, North Carolina State University, Raleigh, NC 27695; † Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583-0919; and ‡ California Polytechnic State University, Environmental Biotechnology Institute, San Luis Obispo, CA 93407
AuthorAffiliation_xml – name: Genomic Sciences Program and Southeast Dairy Foods Research Center, North Carolina State University, Raleigh, NC 27695; † Department of Food Science and Technology, University of Nebraska, Lincoln, NE 68583-0919; and ‡ California Polytechnic State University, Environmental Biotechnology Institute, San Luis Obispo, CA 93407
Author_xml – sequence: 1
  givenname: Rodolphe
  surname: Barrangou
  fullname: Barrangou, Rodolphe
– sequence: 2
  givenname: Eric
  surname: Altermann
  fullname: Altermann, Eric
– sequence: 3
  givenname: Robert
  surname: Hutkins
  fullname: Hutkins, Robert
– sequence: 4
  givenname: Raul
  surname: Cano
  fullname: Cano, Raul
– sequence: 5
  givenname: Todd R.
  surname: Klaenhammer
  fullname: Klaenhammer, Todd R.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/12847288$$D View this record in MEDLINE/PubMed
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Abbreviations: ABC, ATP-binding cassette; cre, catabolite response element; FOS, fructooligosaccharides; MSM, multiple sugar metabolism; PTS, phosphotransferase system; LGT, lateral gene transfer; GI, gastrointestinal; NCFM, North Carolina Food Microbiology.
Contributed by Todd R. Klaenhammer, May 8, 2003
To whom correspondence should be addressed. E-mail: klaenhammer@ncsu.edu.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AY172019, AY172020, and AY177419).
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Snippet Lactobacillus acidophilus is a probiotic organism that displays the ability to use prebiotic compounds such as fructooligosaccharides (FOS), which stimulate...
Lactobacillus acidophilus is a probiotic organism that displays the ability to use prebiotic compounds such as fructooligosaccharides (FOS), which stimulate...
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SubjectTerms 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
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Genome, Bacterial
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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
Title Functional and Comparative Genomic Analyses of an Operon Involved in Fructooligosaccharide Utilization by Lactobacillus acidophilus
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