Catabolic flexibility of mammalian-associated lactobacilli

Metabolic flexibility may be generally defined as “the capacity for the organism to adapt fuel oxidation to fuel availability”. The metabolic diversification strategies used by individual bacteria vary greatly from the use of novel or acquired enzymes to the use of plasmid-localised genes and transporters. In this review, we describe the ability of lactobacilli to utilise a variety of carbon sources from their current or new environments in order to grow and survive. The genus Lactobacillus now includes more than 150 species, many with adaptive capabilities, broad metabolic capacity and species/strain variance. They are therefore, an informative example of a cell factory capable of adapting to new niches with differing nutritional landscapes. Indeed, lactobacilli naturally colonise and grow in a wide variety of environmental niches which include the roots and foliage of plants, silage, various fermented foods and beverages, the human vagina and the mammalian gastrointestinal tract (GIT; including the mouth, stomach, small intestine and large intestine). Here we primarily describe the metabolic flexibility of some lactobacilli isolated from the mammalian gastrointestinal tract, and we also describe some of the food-associated species with a proven ability to adapt to the GIT. As examples this review concentrates on the following species - Lb. plantarum, Lb. acidophilus, Lb. ruminis, Lb. salivarius, Lb. reuteri and Lb. sakei, to highlight the diversity and inter-relationships between the catabolic nature of species within the genus.

[1]  W. Hammes,et al.  Structural similarity and distribution of small cryptic plasmids of Lactobacillus curvatus and L. sake. , 1991, FEMS microbiology letters.

[2]  B. Svensson,et al.  Proteome reference map of Lactobacillus acidophilus NCFM and quantitative proteomics towards understanding the prebiotic action of lactitol , 2011, Proteomics.

[3]  Can V. Tran,et al.  Phylogeny as a guide to structure and function of membrane transport proteins (Review) , 2004, Molecular membrane biology.

[4]  Michael E. Stiles,et al.  Biopreservation by lactic acid bacteria , 1996, Antonie van Leeuwenhoek.

[5]  J. Lengeler Carbohydrate transport in bacteria under environmental conditions, a black box? , 2004, Antonie van Leeuwenhoek.

[6]  B. Görke,et al.  Carbon catabolite repression in bacteria: many ways to make the most out of nutrients , 2008, Nature Reviews Microbiology.

[7]  R. Barrangou,et al.  Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus , 2011, Proceedings of the National Academy of Sciences.

[8]  W. Hammes,et al.  The genus Lactobacillus , 1995 .

[9]  Min Zhang,et al.  The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteri , 2011, PLoS genetics.

[10]  B. Chassy,et al.  Cloning and expression of the beta-D-phosphogalactoside galactohydrolase gene of Lactobacillus casei in Escherichia coli K-12 , 1982, Journal of bacteriology.

[11]  M. Kleerebezem,et al.  Complete genome sequence of Lactobacillus plantarum WCFS1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  B Henrissat,et al.  A classification of glycosyl hydrolases based on amino acid sequence similarities. , 1991, The Biochemical journal.

[13]  S. Vollenweider,et al.  Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives. , 2003, Journal of agricultural and food chemistry.

[14]  A. Coghlan,et al.  Genome sequences and comparative genomics of two Lactobacillus ruminis strains from the bovine and human intestinal tracts , 2011, Microbial cell factories.

[15]  Milton H. Saier,et al.  TCDB: the Transporter Classification Database for membrane transport protein analyses and information , 2005, Nucleic Acids Res..

[16]  A Bairoch,et al.  Updating the sequence-based classification of glycosyl hydrolases. , 1996, The Biochemical journal.

[17]  M. De Felice,et al.  Expression of the bglH Gene ofLactobacillus plantarum Is Controlled by Carbon Catabolite Repression , 1998, Journal of bacteriology.

[18]  A. Sangrador-Vegas,et al.  Genome Sequence of Lactobacillus helveticus, an Organism Distinguished by Selective Gene Loss and Insertion Sequence Element Expansion , 2007, Journal of bacteriology.

[19]  W. Konings Microbial transport: Adaptations to natural environments , 2006, Antonie van Leeuwenhoek.

[20]  Sam P. Brown,et al.  What traits are carried on mobile genetic elements, and why? , 2011, Heredity.

[21]  B. Neville,et al.  Carbohydrate catabolic flexibility in the mammalian intestinal commensal Lactobacillus ruminis revealed by fermentation studies aligned to genome annotations , 2011, Microbial cell factories.

[22]  V. Loux,et al.  The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K , 2005, Nature Biotechnology.

[23]  J. Deutscher,et al.  The mechanisms of carbon catabolite repression in bacteria. , 2008, Current opinion in microbiology.

[24]  M. Gänzle,et al.  Levansucrase and sucrose phoshorylase contribute to raffinose, stachyose, and verbascose metabolism by lactobacilli. , 2012, Food microbiology.

[25]  P. Langella,et al.  Analysis of Lactobacillus sakei Mutants Selected after Adaptation to the Gastrointestinal Tracts of Axenic Mice , 2010, Applied and Environmental Microbiology.

[26]  R. Barrangou,et al.  Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  E. W. V. van Niel,et al.  Phosphoketolase Pathway Dominates in Lactobacillus reuteri ATCC 55730 Containing Dual Pathways for Glycolysis , 2007, Journal of bacteriology.

[28]  G. Holtrop,et al.  Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach , 2011, The ISME Journal.

[29]  Reinhold Brückner,et al.  Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. , 2002, FEMS microbiology letters.

[30]  P. Brigidi,et al.  Effect of a synbiotic food consumption on human gut metabolic profiles evaluated by (1)H Nuclear Magnetic Resonance spectroscopy. , 2009, International journal of food microbiology.

[31]  Bas Teusink,et al.  Understanding the Adaptive Growth Strategy of Lactobacillus plantarum by In Silico Optimisation , 2009, PLoS Comput. Biol..

[32]  Yin Li,et al.  Distribution of Megaplasmids in Lactobacillus salivarius and Other Lactobacilli , 2007, Journal of bacteriology.

[33]  T. S. Manning,et al.  Microbial-gut interactions in health and disease. Prebiotics. , 2004, Best practice & research. Clinical gastroenterology.

[34]  W. Wood,et al.  Pathways of carbohydrate metabolism in microorganisms. , 1955, Bacteriological reviews.

[35]  R. Barrangou,et al.  Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  B. Berger,et al.  Identification of Genes Associated with the Long-Gut-Persistence Phenotype of the Probiotic Lactobacillus johnsonii Strain NCC533 Using a Combination of Genomics and Transcriptome Analysis , 2008, Journal of bacteriology.

[37]  M. Inui,et al.  Sugar transporters in efficient utilization of mixed sugar substrates: current knowledge and outlook , 2009, Applied Microbiology and Biotechnology.

[38]  R. Schoenfeld,et al.  Comparative Genomics of Listeria Species , 1976 .

[39]  M. Kleerebezem,et al.  Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. , 2010, Environmental microbiology.

[40]  M. Saier,et al.  Carbohydrate transport in bacteria. , 1980, Microbiological reviews.

[41]  Shengyue Wang,et al.  Complete Sequencing and Pan-Genomic Analysis of Lactobacillus delbrueckii subsp. bulgaricus Reveal Its Genetic Basis for Industrial Yogurt Production , 2011, PloS one.

[42]  R. Siezen,et al.  Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer , 2011, Microbial cell factories.

[43]  L. Axelsson,et al.  Characterisation of the gap Operon from Lactobacillus plantarum and Lactobacillus sakei , 2007, Current Microbiology.

[44]  B. Poolman Transporters and their roles in LAB cell physiology , 2004, Antonie van Leeuwenhoek.

[45]  Philippe Sansonetti,et al.  Microbial-gut interactions in health and disease. Epithelial cell responses. , 2004, Best practice & research. Clinical gastroenterology.

[46]  A. Goesmann,et al.  Complete Genome Sequence of Lactobacillus johnsonii FI9785, a Competitive Exclusion Agent against Pathogens in Poultry , 2009, Journal of bacteriology.

[47]  Philippe Bessières,et al.  Extensive horizontal transfer of core genome genes between two Lactobacillus species found in the gastrointestinal tract , 2007, BMC Evolutionary Biology.

[48]  M. Roberfroid,et al.  Dietary modulation of the human colonic microbiota: updating the concept of prebiotics , 2004, Nutrition Research Reviews.

[49]  B. Lee,et al.  Plasmids in Lactobacillus. , 1997, Critical reviews in biotechnology.

[50]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.

[51]  Katherine H. Huang,et al.  Comparative genomics of the lactic acid bacteria , 2006, Proceedings of the National Academy of Sciences.

[52]  A. Jeanes,et al.  Physiological Effects of Food Carbohydrates , 1975 .

[53]  Enrique Galindo,et al.  Oxygen transfer rate during the production of alginate by Azotobacter vinelandii under oxygen-limited and non oxygen-limited conditions , 2011, Microbial cell factories.

[54]  W. D. de Vos,et al.  Identification of Prebiotic Fructooligosaccharide Metabolism in Lactobacillus plantarum WCFS1 through Microarrays , 2007, Applied and Environmental Microbiology.

[55]  P. Auvinen,et al.  Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein , 2009, Proceedings of the National Academy of Sciences.

[56]  T. Hansen Bergey's Manual of Systematic Bacteriology , 2005 .

[57]  M. Kleerebezem,et al.  Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice , 2010, The ISME Journal.

[58]  W. Holzapfel,et al.  The Genera of Lactic Acid Bacteria , 1999 .

[59]  M. Kleerebezem,et al.  Lifestyle of Lactobacillus plantarum in the mouse caecum. , 2009, Environmental microbiology.

[60]  J. M. Rodríguez,et al.  Complete Genome Sequence of Lactobacillus salivarius CECT 5713, a Probiotic Strain Isolated from Human Milk and Infant Feces , 2010, Journal of bacteriology.

[61]  E. Zoetendal,et al.  The Intestinal LABs , 2002, Antonie van Leeuwenhoek.

[62]  G. Reuter The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. , 2001, Current issues in intestinal microbiology.

[63]  Complete nucleotide sequence of plasmid plca36 isolated from Lactobacillus casei Zhang. , 2008, Plasmid.

[64]  J. Walter,et al.  Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm , 2010, Proceedings of the National Academy of Sciences.

[65]  Franco Dellaglio,et al.  Taxonomy of Lactobacilli and Bifidobacteria. , 2007, Current issues in intestinal microbiology.

[66]  R. Tauxe,et al.  Interspecies gene transfer in vivo producing an outbreak of multiply resistant shigellosis. , 1989, The Journal of infectious diseases.

[67]  G R Jacobson,et al.  Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. , 1993, Microbiological reviews.

[68]  M. Hecker,et al.  Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon , 2001, Molecular microbiology.

[69]  W. Hillen,et al.  Global control of sugar metabolism: a Gram-positive solution , 2004, Antonie van Leeuwenhoek.

[70]  S. Shoemaker,et al.  Relaxed control of sugar utilization in Lactobacillus brevis. , 2009, Microbiology.

[71]  R. Leer,et al.  Complementation of the inability of Lactobacillus strains to utilize D-xylose with D-xylose catabolism-encoding genes of Lactobacillus pentosus , 1991, Applied and environmental microbiology.

[72]  Pawel Kaleta,et al.  Comparative genomics of lactic acid bacteria reveals a niche-specific gene set , 2009, BMC Microbiology.

[73]  Rodolphe Barrangou,et al.  The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[74]  F. González-Candelas,et al.  Horizontal gene transfer in the molecular evolution of mannose PTS transporters. , 2005, Molecular biology and evolution.

[75]  J. Steele,et al.  Genotypic and phenotypic characterization of Lactobacillus casei strains isolated from different ecological niches suggests frequent recombination and niche specificity. , 2007, Microbiology.

[76]  Rodolphe Barrangou,et al.  Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  W. D. de Vos,et al.  Genome Sequence of Lactobacillus amylovorus GRL1112 , 2010, Journal of bacteriology.

[78]  W. Hillen,et al.  Carbon catabolite repression in bacteria. , 1999, Current opinion in microbiology.

[79]  Guo-Ping Zhao,et al.  Complete Genome Sequence of Lactobacillus plantarum JDM1 , 2009, Journal of bacteriology.

[80]  Michiel Kleerebezem,et al.  Exploring Lactobacillus plantarum Genome Diversity by Using Microarrays , 2005, Journal of bacteriology.

[81]  L. Gautier,et al.  Comparative Genomics of Listeria Species , 2001, Science.

[82]  O. Kandler,et al.  Carbohydrate metabolism in lactic acid bacteria , 1983, Antonie van Leeuwenhoek.

[83]  J. M. Rodríguez,et al.  Complete Genome Sequence of Lactobacillus fermentum CECT 5716, a Probiotic Strain Isolated from Human Milk , 2010, Journal of bacteriology.

[84]  I. Paulsen,et al.  Catabolite repression and inducer control in Gram-positive bacteria. , 1996, Microbiology.

[85]  W. Holzapfel,et al.  Lactic acid bacteria of foods and their current taxonomy. , 1997, International journal of food microbiology.

[86]  M. Hattori,et al.  Comparative Genome Analysis of Lactobacillus reuteri and Lactobacillus fermentum Reveal a Genomic Island for Reuterin and Cobalamin Production , 2008, DNA research : an international journal for rapid publication of reports on genes and genomes.

[87]  P. Dürre,et al.  Differential Expression of Genes Within the gap Operon of Clostridium acetobutylicum , 2000 .

[88]  J. Parkhill,et al.  Multireplicon genome architecture of Lactobacillus salivarius. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[89]  Michael J. Miller,et al.  Analysis of the Genome Sequence of Lactobacillus gasseri ATCC 33323 Reveals the Molecular Basis of an Autochthonous Intestinal Organism , 2008, Applied and Environmental Microbiology.

[90]  D. Block,et al.  Atypical ethanol production by carbon catabolite derepressed lactobacilli. , 2010, Bioresource technology.

[91]  G. Garrity Bergey’s Manual® of Systematic Bacteriology , 2012, Springer New York.

[92]  A. Guillot,et al.  Proteomic analysis of Lactococcus lactis, a lactic acid bacterium , 2003, Proteomics.

[93]  S. Fukui Carbohydrate Metabolism in Lactic Acid Bacteria , 1960 .

[94]  M. Hattori,et al.  Complete Genome Sequence of the Probiotic Lactobacillus rhamnosus ATCC 53103 , 2009, Journal of Bacteriology.

[95]  G. Vinderola,et al.  Inside the adaptation process of Lactobacillus delbrueckii subsp. lactis to bile. , 2010, International journal of food microbiology.

[96]  J. J. Rackis Oligosaccharides of Food Legumes: Alpha-Galactosidase Activity and the Flatus Problem , 1975 .

[97]  M. Morange,et al.  Microbial Cell Factories , 2006 .