Systems solutions by lactic acid bacteria: from paradigms to practice

Lactic acid bacteria are among the powerhouses of the food industry, colonize the surfaces of plants and animals, and contribute to our health and well-being. The genomic characterization of LAB has rocketed and presently over 100 complete or nearly complete genomes are available, many of which serve as scientific paradigms. Moreover, functional and comparative metagenomic studies are taking off and provide a wealth of insight in the activity of lactic acid bacteria used in a variety of applications, ranging from starters in complex fermentations to their marketing as probiotics. In this new era of high throughput analysis, biology has become big science. Hence, there is a need to systematically store the generated information, apply this in an intelligent way, and provide modalities for constructing self-learning systems that can be used for future improvements. This review addresses these systems solutions with a state of the art overview of the present paradigms that relate to the use of lactic acid bacteria in industrial applications. Moreover, an outlook is presented of the future developments that include the transition into practice as well as the use of lactic acid bacteria in synthetic biology and other next generation applications.

[1]  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.

[2]  T. Hoover,et al.  Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge , 2009, Proceedings of the National Academy of Sciences.

[3]  Albert J R Heck,et al.  Structural basis for CRISPR RNA-guided DNA recognition by Cascade , 2011, Nature Structural &Molecular Biology.

[4]  W. D. de Vos,et al.  The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. , 2008, Microbiology.

[5]  C. Hill,et al.  Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118 , 2007, Proceedings of the National Academy of Sciences.

[6]  F. L. Davies,et al.  Plasmid encoded bacteriophage resistance in Streptococcus cremoris SK11 , 1984 .

[7]  Alexander Goesmann,et al.  Complete Genome Sequence of the Prototype Lactic Acid Bacterium Lactococcus lactis subsp. cremoris MG1363 , 2007, Journal of bacteriology.

[8]  S. Ehrlich,et al.  Low-redundancy sequencing of the entire Lactococcus lactis IL1403 genome , 1999, Antonie van Leeuwenhoek.

[9]  J. Bae,et al.  Metatranscriptome analysis of lactic acid bacteria during kimchi fermentation with genome-probing microarrays. , 2009, International journal of food microbiology.

[10]  W. D. de Vos,et al.  Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin , 1996, Applied and environmental microbiology.

[11]  J. Wells,et al.  Oral vaccination of mice against tetanus with recombinant Lactococcus lactis , 1997, Nature Biotechnology.

[12]  Trey Ideker,et al.  Boosting Signal-to-Noise in Complex Biology: Prior Knowledge Is Power , 2011, Cell.

[13]  Philippe Horvath,et al.  The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA , 2010, Nature.

[14]  G. Venemâ,et al.  Identification of a gene required for maturation of an extracellular lactococcal serine proteinase , 1989, Journal of bacteriology.

[15]  W. M. Vos,et al.  Food-grade controlled lysis of Lactococcus lactis for accelerated cheese ripening , 1997, Nature Biotechnology.

[16]  W. D. de Vos,et al.  Generation of a Membrane Potential by Lactococcus lactis through Aerobic Electron Transport , 2007, Journal of bacteriology.

[17]  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.

[18]  D. Sinderen,et al.  Sequence Analysis of the Lactococcal Plasmid pNP40: a Mobile Replicon for Coping with Environmental Hazards , 2006, Journal of bacteriology.

[19]  T. Klaenhammer,et al.  Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid , 2011, Proceedings of the National Academy of Sciences.

[20]  Bas Teusink,et al.  Modelling strategies for the industrial exploitation of lactic acid bacteria , 2006, Nature Reviews Microbiology.

[21]  P. Vandamme,et al.  Metatranscriptome Analysis for Insight into Whole-Ecosystem Gene Expression during Spontaneous Wheat and Spelt Sourdough Fermentations , 2010, Applied and Environmental Microbiology.

[22]  W. D. de Vos,et al.  Diversity, vitality and activities of intestinal lactic acid bacteria and bifidobacteria assessed by molecular approaches. , 2005, FEMS microbiology reviews.

[23]  R. Barrangou,et al.  CRISPR/Cas, the Immune System of Bacteria and Archaea , 2010, Science.

[24]  W. D. de Vos,et al.  Molecular characterization of the plasmid‐encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis , 1997, Molecular microbiology.

[25]  W. D. de Vos,et al.  Food-grade cloning and expression system for Lactococcus lactis , 1996, Applied and environmental microbiology.

[26]  W. Vos Gene cloning and expression in lactic streptococci , 1987 .

[27]  T. Klaenhammer,et al.  Engineered bacteriophage-defence systems in bioprocessing , 2006, Nature Reviews Microbiology.

[28]  M. Gasson In vivo genetic systems in lactic acid bacteria. , 1990, FEMS microbiology reviews.

[29]  Vesa,et al.  Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract , 2000, Alimentary pharmacology & therapeutics.

[30]  C. Péchoux,et al.  Cell Surface of Lactococcus lactis Is Covered by a Protective Polysaccharide Pellicle* , 2010, The Journal of Biological Chemistry.

[31]  V. Zverlov,et al.  Reconstructing the clostridial n-butanol metabolic pathway in Lactobacillus brevis , 2010, Applied Microbiology and Biotechnology.

[32]  Monya Baker Synthetic genomes: The next step for the synthetic genome , 2011, Nature.

[33]  W. D. de Vos,et al.  Functional ingredient production: application of global metabolic models. , 2005, Current opinion in biotechnology.

[34]  W. D. de Vos,et al.  Autoregulation of Nisin Biosynthesis in Lactococcus lactis by Signal Transduction (*) , 1995, The Journal of Biological Chemistry.

[35]  Maija Saxelin,et al.  Probiotic and other functional microbes: from markets to mechanisms. , 2005, Current opinion in biotechnology.

[36]  R. Evans,et al.  Applications of the bacteriocin, nisin , 1996, Antonie van Leeuwenhoek.

[37]  W. D. de Vos,et al.  Primary structure and organization of the gene for a procaryotic, cell envelope-located serine proteinase. , 1989, The Journal of biological chemistry.

[38]  L. Mckay,et al.  Functional properties of plasmids in lactic streptococci , 1983, Antonie van Leeuwenhoek.

[39]  W. D. de Vos,et al.  Physiological responses to folate overproduction in Lactobacillus plantarum WCFS1 , 2010, Microbial cell factories.

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

[41]  Harma A. Karsens,et al.  Design of thermolabile bacteriophage repressor mutants by comparative molecular modeling , 1997, Nature Biotechnology.

[42]  J. Hugenholtz,et al.  Functional genomics for food fermentation processes. , 2010, Annual review of food science and technology.

[43]  J. D. de Visser,et al.  Insertion-Sequence-Mediated Mutations Isolated During Adaptation to Growth and Starvation in Lactococcus lactis , 2004, Genetics.

[44]  T. Hartung,et al.  Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Bart Pieterse,et al.  Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. , 2005, Microbiology.

[46]  W. D. de Vos,et al.  Engineering metabolic highways in Lactococci and other lactic acid bacteria. , 2004, Trends in biotechnology.

[47]  A. Palva,et al.  Lactobacillus surface layers and their applications. , 2005, FEMS microbiology reviews.

[48]  M. Kleerebezem,et al.  A high-throughput cheese manufacturing model for effective cheese starter culture screening. , 2009, Journal of dairy science.

[49]  M. Kleerebezem,et al.  Cofactor Engineering: a Novel Approach to Metabolic Engineering in Lactococcus lactis by Controlled Expression of NADH Oxidase , 1998, Journal of bacteriology.

[50]  Douwe Molenaar,et al.  Mixed-Culture Transcriptome Analysis Reveals the Molecular Basis of Mixed-Culture Growth in Streptococcus thermophilus and Lactobacillus bulgaricus , 2010, Applied and Environmental Microbiology.

[51]  Vos,et al.  Nucleotide sequence and expression in Escherichia coli of the Lactococcus lactis citrate permease gene , 1990, Journal of bacteriology.

[52]  W. D. de Vos,et al.  Electron transport chains of lactic acid bacteria - walking on crutches is part of their lifestyle , 2009, F1000 biology reports.

[53]  R. Siezen,et al.  Prokaryotic whole‐transcriptome analysis: deep sequencing and tiling arrays , 2010, Microbial biotechnology.

[54]  D. Lechardeur,et al.  Using heme as an energy boost for lactic acid bacteria. , 2011, Current opinion in biotechnology.

[55]  W. D. de Vos,et al.  Characterization of the lactose-specific enzymes of the phosphotransferase system in Lactococcus lactis. , 1990, The Journal of biological chemistry.

[56]  M. Cronin,et al.  Progress in genomics, metabolism and biotechnology of bifidobacteria. , 2011, International journal of food microbiology.

[57]  Michiel Kleerebezem,et al.  Identification of Genetic Loci in Lactobacillus plantarum That Modulate the Immune Response of Dendritic Cells Using Comparative Genome Hybridization , 2010, PloS one.

[58]  B. Haas,et al.  A Catalog of Reference Genomes from the Human Microbiome , 2010, Science.

[59]  Venema,et al.  Engineering of the Lactococcus lactis serine proteinase by construction of hybrid enzymes. , 1991, Protein engineering.

[60]  Bas Teusink,et al.  Analysis of Growth of Lactobacillus plantarum WCFS1 on a Complex Medium Using a Genome-scale Metabolic Model* , 2006, Journal of Biological Chemistry.

[61]  W. M. Vos Advances in genomics for microbial food fermentations and safety. , 2001 .

[62]  Rudiyanto Gunawan,et al.  Parameter estimation of kinetic models from metabolic profiles: two-phase dynamic decoupling method , 2011, Bioinform..

[63]  Stan J. J. Brouns,et al.  Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes , 2008, Science.

[64]  J. Gibrat,et al.  The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[65]  B. Poolman,et al.  Genome Sequences of Lactococcus lactis MG1363 (Revised) and NZ9000 and Comparative Physiological Studies , 2010, Journal of bacteriology.

[66]  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.

[67]  David R. Riley,et al.  Comparative genomics of the genus Bifidobacterium. , 2010, Microbiology.

[68]  D. Greco,et al.  Proteomics and Transcriptomics Characterization of Bile Stress Response in Probiotic Lactobacillus rhamnosus GG* , 2010, Molecular & Cellular Proteomics.

[69]  W. D. de Vos,et al.  Comparative genomics of Lactobacillus , 2011, Microbial biotechnology.

[70]  T. Leathers,et al.  Bacterial contaminants of fuel ethanol production , 2004, Journal of Industrial Microbiology and Biotechnology.

[71]  J. Wells Mucosal vaccination and therapy with genetically modified lactic acid bacteria. , 2011, Annual review of food science and technology.

[72]  Nasib Qureshi,et al.  Functional expression of the thiolase gene thl from Clostridium beijerinckii P260 in Lactococcus lactis and Lactobacillus buchneri. , 2010, New biotechnology.

[73]  W. D. de Vos,et al.  Systems biology of the gut: the interplay of food, microbiota and host at the mucosal interface. , 2010, Current opinion in biotechnology.

[74]  P. Langella,et al.  Two plasmid-determined restriction and modification systems in Streptococcus lactis. , 1984, Plasmid.

[75]  T. Klaenhammer,et al.  Abortive Phage Resistance Mechanism AbiZ Speeds the Lysis Clock To Cause Premature Lysis of Phage-Infected Lactococcus lactis , 2006, Journal of bacteriology.

[76]  M. Kleerebezem,et al.  Cre-lox-Based System for Multiple Gene Deletions and Selectable-Marker Removal in Lactobacillus plantarum , 2006, Applied and Environmental Microbiology.

[77]  W. D. de Vos,et al.  Lactobacillus plantarum WCFS1 Electron Transport Chains , 2009, Applied and Environmental Microbiology.

[78]  M. Kleerebezem,et al.  Differential NF-κB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance , 2009, Proceedings of the National Academy of Sciences.

[79]  M. Kleerebezem,et al.  Identification of Lactobacillus plantarum Genes That Are Induced in the Gastrointestinal Tract of Mice , 2004, Journal of bacteriology.

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

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

[82]  Elaine E. Vaughan,et al.  Diversity, Dynamics, and Activity of Bacterial Communities during Production of an Artisanal Sicilian Cheese as Evaluated by 16S rRNA Analysis , 2002, Applied and Environmental Microbiology.

[83]  P. Pouwels,et al.  Interchange of the active and silent S‐layer protein genes of Lactobacillus acidophilus by inversion of the chromosomal slp segment , 1996, Molecular microbiology.

[84]  T. Klaenhammer,et al.  Bacteriophage resistance inLactococcus , 1995 .

[85]  P. R. Jensen,et al.  Artificial promoters for metabolic optimization. , 1998, Biotechnology and bioengineering.

[86]  S. Ehrlich,et al.  The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. , 2001, Genome research.

[87]  C. Hill,et al.  The gene encoded antimicrobial peptides, a template for the design of novel anti-mycobacterial drugs , 2010, Bioengineered bugs.

[88]  A. Goffeau,et al.  Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus , 2004, Nature Biotechnology.

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

[90]  M. Kleerebezem,et al.  The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. , 2004, Microbiology.

[91]  Michiel Kleerebezem,et al.  10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis , 2005, Applied Microbiology and Biotechnology.

[92]  W. D. de Vos,et al.  S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions , 2008, Proceedings of the National Academy of Sciences.

[93]  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.

[94]  M. Kleerebezem,et al.  Time-resolved genetic responses of Lactococcus lactis to a dairy environment. , 2010, Environmental microbiology.

[95]  J. Vanderleyden,et al.  Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens , 2010, Nature Reviews Microbiology.

[96]  B. Teusink,et al.  Understanding the physiology of Lactobacillus plantarum at zero growth , 2010, Molecular systems biology.

[97]  Michiel Kleerebezem,et al.  Biodiversity-Based Identification and Functional Characterization of the Mannose-Specific Adhesin of Lactobacillus plantarum , 2005, Journal of bacteriology.

[98]  S. Sieuwerts Analysis of molecular interactions between yoghurt bacteria by an integrated genomics approach , 2009 .

[99]  Petri-Jaan Lahtvee,et al.  Multi-omics approach to study the growth efficiency and amino acid metabolism in Lactococcus lactis at various specific growth rates , 2011, Microbial cell factories.

[100]  W. M. Vos,et al.  Molecular cloning, transcriptional analysis, and nucleotide sequence of lacR, a gene encoding the repressor of the lactose phosphotransferase system of Lactococcus lactis. , 1990 .

[101]  M. Kleerebezem,et al.  Lactococcus lactis as a Cell Factory for High-Level Diacetyl Production , 2000, Applied and Environmental Microbiology.

[102]  M. Kleerebezem,et al.  High-Level Acetaldehyde Production in Lactococcus lactis by Metabolic Engineering , 2005, Applied and Environmental Microbiology.

[103]  T. Klaenhammer,et al.  The impact of omic technologies on the study of food microbes. , 2011, Annual review of food science and technology.

[104]  M. Kleerebezem,et al.  Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways , 2010, Proceedings of the National Academy of Sciences.

[105]  A. Gruss,et al.  Impact of Aeration and Heme-Activated Respiration on Lactococcus lactis Gene Expression: Identification of a Heme-Responsive Operon , 2008, Journal of bacteriology.

[106]  Beat Mollet,et al.  Regulation and Adaptive Evolution of Lactose Operon Expression in Lactobacillus delbrueckii , 2002, Journal of bacteriology.

[107]  Pascal Hols,et al.  Conversion of Lactococcus lactis from homolactic to homoalanine fermentation through metabolic engineering , 1999, Nature Biotechnology.

[108]  W. D. de Vos,et al.  A maturation protein is essential for production of active forms of Lactococcus lactis SK11 serine proteinase located in or secreted from the cell envelope , 1989, Journal of bacteriology.

[109]  M. Kleerebezem,et al.  Controlled overproduction of proteins by lactic acid bacteria. , 1997, Trends in biotechnology.

[110]  G. Rook 99th Dahlem Conference on Infection, Inflammation and Chronic Inflammatory Disorders: Darwinian medicine and the ‘hygiene’ or ‘old friends’ hypothesis , 2010, Clinical and experimental immunology.

[111]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[112]  Sacha A. F. T. van Hijum,et al.  PanCGHweb: a web tool for genotype calling in pangenome CGH data , 2010, Bioinform..

[113]  Y. Le Loir,et al.  Respiration Capacity of the Fermenting BacteriumLactococcus lactis and Its Positive Effects on Growth and Survival , 2001, Journal of bacteriology.

[114]  M. Gasson,et al.  Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing , 1983, Journal of bacteriology.

[115]  Harma A. Karsens,et al.  Sequence analysis and molecular characterization of the temperate lactococcal bacteriophage r1t , 1996, Molecular microbiology.

[116]  W. D. de Vos,et al.  Characterization of the novel nisin-sucrose conjugative transposon Tn5276 and its insertion in Lactococcus lactis , 1992, Journal of bacteriology.

[117]  P. Horvath,et al.  A Novel Pheromone Quorum-Sensing System Controls the Development of Natural Competence in Streptococcus thermophilus and Streptococcus salivarius , 2009, Journal of bacteriology.

[118]  M. Kleerebezem,et al.  Indigenous and Environmental Modulation of Frequencies of Mutation in Lactobacillus plantarum , 2009, Applied and Environmental Microbiology.

[119]  G. Venema,et al.  Gene expression in Lactococcus lactis. , 1992, FEMS microbiology reviews.

[120]  M. Kleerebezem,et al.  Improvement of Lactobacillus plantarum Aerobic Growth as Directed by Comprehensive Transcriptome Analysis , 2008, Applied and Environmental Microbiology.

[121]  G. Venema,et al.  Construction of plasmid cloning vectors for lactic streptococci which also replicate in Bacillus subtilis and Escherichia coli , 1984, Applied and environmental microbiology.

[122]  R. Siezen,et al.  Molecular Description and Industrial Potential of Tn6098 Conjugative Transfer Conferring Alpha-Galactoside Metabolism in Lactococcus lactis , 2010, Applied and Environmental Microbiology.

[123]  M. I. Pastink Comparative functional genomics of amino acid metabolism of lactic acid bacteria. , 2009 .

[124]  W. D. de Vos,et al.  Role of phosphate in the central metabolism of two lactic acid bacteria – a comparative systems biology approach , 2012, The FEBS journal.

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

[126]  G. Fitzgerald,et al.  Biotechnology of lactic acid bacteria with special reference to bacteriophage resistance , 1996, Antonie van Leeuwenhoek.

[127]  Harma A. Karsens,et al.  Inducible gene expression mediated by a repressor‐operator system isolated from Lactococcus lactis bacteriophage r1t , 1996, Molecular microbiology.

[128]  M. Kleerebezem,et al.  Reconstruction of the regulatory network of Lactobacillus plantarum WCFS1 on basis of correlated gene expression and conserved regulatory motifs , 2011, Microbial biotechnology.