Food Analytical Methods

, Volume 8, Issue 2, pp 272–289 | Cite as

Food Omics Validation: Towards Understanding Key Features for Gut Microbiota, Probiotics and Human Health

  • María Luján Jiménez-Pranteda
  • Azahara Pérez-Davó
  • Mercedes Monteoliva-Sánchez
  • Alberto Ramos-Cormenzana
  • Margarita AguileraEmail author


Probiotics are constituents of functional foods, which when administered in appropriate amounts confer a benefit to the host. Research studies performed on probiotics and gut microbiota along recent years have been focused on investigating the correlation between their molecular features and their impacts on individual health status. Consequently, many present and future challenges are being raised to elucidate the molecular bases of their interaction-mediated systemic effects, along with the ability to manipulate them for preventive and therapeutic interventions. Moreover, insights derived from the parallel evolution of “omics” technologies, with applications in different fields of biomedicine, are being efficiently transferred to this area of molecular microbiology. Thus, the present work compiles a summary of the general and useful omics applications: genomics, metagenomics, transcriptomics, proteomics, metabolomics, phenomics, and recently, integromics and interactomics and their putative use for validating models of interactions of the better-known probiotic microorganisms administered Lactobacillus and Bifidobacterium species. The impact on molecular resistance features, formula preparation, and route administration are also discussed. Omics tools will generate large amounts of data that, once correctly interpreted, are expected to rapidly validate the knowledge of probiotic molecular fundaments that trigger important positive human biological processes.


Probiotic Genomics Transcriptomics Proteomics Metabolomics Integromics 



The funding that supports this research field has been a Project GREIB under CEI-BIOTIC, University of Granada.

Conflict of Interest

All authors belong to the University of Granada, which partially has founding the research that supports the review manuscript. However, they declare that they have no conflict of interest. Maria Lujan Jiménez-Pranteda declares that she has no conflict of interest. Azahara Pérez-Davó declares that she has no conflict of interest. Mercedes Monteoliva-Sánchez declares that she has no conflict of interest. Alberto Ramos Cormenzana declares that he has no conflict of interest. Margarita Aguilera Gómez declares that she has no conflict of interest. Maria Lujan Jiménez-Pranteda has received research grants from Science Ministry in Spain. Azahara Pérez-Davó has received research grants from University of Granada. This article does not contain any studies with human or animal subjects.


  1. Aaltonen J, Ojala T, Laitinen K, Piirainen TJ, Poussa TA, Isolauri E (2008) Evidence of infant blood pressure programming by maternal nutrition during pregnancy: a prospective randomized controlled intervention study. J Pediatr 152:79–84. doi: 10.1016/j.jpeds.2007.05.048, 84 e71-72Google Scholar
  2. Aaltonen J, Ojala T, Laitinen K, Poussa T, Ozanne S, Isolauri E (2011) Impact of maternal diet during pregnancy and breastfeeding on infant metabolic programming: a prospective randomized controlled study. Eur J Clin Nutr 65:10–19. doi: 10.1038/ejcn.2010.225 Google Scholar
  3. Abu-Asab MS et al (2011) Biomarkers in the age of omics: time for a systems biology approach. OMICS 15:105–112. doi: 10.1089/omi.2010.0023 Google Scholar
  4. Aguilera M, Rakotoarivonina H, Brutus A, Giardina T, Simon G, Fons M (2012) Aga1, the first alpha-Galactosidase from the human bacteria Ruminococcus gnavus E1, efficiently transcribed in gut conditions. Res Microbiol 163:14–21. doi: 10.1016/j.resmic.2011.10.005 Google Scholar
  5. Aires J, Anglade P, Baraige F, Zagorec M, Champomier-Verges MC, Butel MJ (2010) Proteomic comparison of the cytosolic proteins of three Bifidobacterium longum human isolates and B. longum NCC2705. BMC Microbiol 10:29Google Scholar
  6. AlFaleh K, Anabrees J (2014) Probiotics for prevention of necrotizing enterocolitis in preterm infants. The Cochrane database of systematic reviews 4:CD005496–CD005496. doi: 10.1002/14651858.CD005496.pub4 Google Scholar
  7. Avalos JL, Bever KM, Wolberger C (2005) Mechanism of sirtuin inhibition by nicotinamide: altering the NAD(+) cosubstrate specificity of a Sir2 enzyme. Mol Cell 17:855–868. doi: 10.1016/j.molcel.2005.02.022 Google Scholar
  8. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920. doi: 10.1126/science.1104816 Google Scholar
  9. Baugher JL, Klaenhammer TR (2011) Invited review: application of omics tools to understanding probiotic functionality. J Dairy Sci 94:4753–4765. doi: 10.3168/jds.2011-4384 Google Scholar
  10. Bayoumi MA, Griffiths MW (2010) Probiotics down-regulate genes in Salmonella enterica serovar typhimurium pathogenicity islands 1 and 2. J Food Prot 73:452–460Google Scholar
  11. Benson AK et al (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A 107:18933–18938. doi: 10.1073/pnas.1007028107 Google Scholar
  12. Berlec A, Strukelj B (2009) Novel applications of recombinant lactic acid bacteria in therapy and in metabolic engineering. Recent Pat Biotechnol 3:77–87Google Scholar
  13. Bernini P et al (2009) Individual human phenotypes in metabolic space and time. J Proteome Res 8:4264–4271. doi: 10.1021/pr900344m Google Scholar
  14. Boesten RJ, de Vos WM (2008) Interactomics in the human intestine: Lactobacilli and Bifidobacteria make a difference. J Clin Gastroenterol 42(Suppl 3 Pt 2):S163–S167. doi: 10.1097/MCG.0b013e31817dbd62 Google Scholar
  15. Booijink CC, Boekhorst J, Zoetendal EG, Smidt H, Kleerebezem M, de Vos WM (2010) Metatranscriptome analysis of the human fecal microbiota reveals subject-specific expression profiles, with genes encoding proteins involved in carbohydrate metabolism being dominantly expressed. Appl Environ Microbiol 76:5533–5540. doi: 10.1128/AEM.00502-10 Google Scholar
  16. Bottacini F et al (2010) Comparative genomics of the genus Bifidobacterium. Microbiology 156:3243–3254. doi: 10.1099/mic.0.039545-0 Google Scholar
  17. Briczinski EP, Loquasto JR, Barrangou R, Dudley EG, Roberts AM, Roberts RF (2009) Strain-specific genotyping of Bifidobacterium animalis subsp. lactis by using single-nucleotide polymorphisms, insertions, and deletions. Appl Environ Microbiol 75:7501–7508. doi: 10.1128/AEM.01430-09 Google Scholar
  18. Bron PA, Kleerebezem M (2011) Engineering lactic acid bacteria for increased industrial functionality. Bioeng Bugs 2:80–87. doi: 10.4161/bbug.2.2.13910 Google Scholar
  19. Budin-Verneuil A, Pichereau V, Auffray Y, Ehrlich D, Maguin E (2007) Proteome phenotyping of acid stress-resistant mutants of Lactococcus lactis MG1363. Proteomics 7:2038–2046. doi: 10.1002/pmic.200600773 Google Scholar
  20. Candela M, Guidotti M, Fabbri A, Brigidi P, Franceschi C, Fiorentini C (2011) Human intestinal microbiota: cross-talk with the host and its potential role in colorectal cancer. Crit Rev Microbiol 37:1–14. doi: 10.3109/1040841X.2010.501760 Google Scholar
  21. Cangemi de Gutierrez R, Santos VM, Nader-Macias ME (2004) Colonization capability of lactobacilli and pathogens in the respiratory tract of mice: microbiological, cytological, structural, and ultrastructural studies. Methods Mol Biol 268:373–385. doi: 10.1385/1-59259-766-1:373 Google Scholar
  22. Carrington LJ, Langley-Evans SC (2006) Wheezing and eczema in relation to infant anthropometry: evidence of developmental programming of disease in childhood. Maternal and Child Nutrition 2:51–61. doi: 10.1111/j.1740-8709.2006.00036.x Google Scholar
  23. Catalioto RM, Maggi CA, Giuliani S (2011) Intestinal epithelial barrier dysfunction in disease and possible therapeutical interventions. Curr Med Chem 18:398–426Google Scholar
  24. Claesson MJ et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 108(Suppl 1):4586–4591. doi: 10.1073/pnas.1000097107 Google Scholar
  25. Cutting SM (2011) Bacillus probiotics. Food Microbiol 28:214–220. doi: 10.1016/ Google Scholar
  26. Chrysohoou C, Stefanadis C (2013) Longevity and diet. Myth or pragmatism? Maturitas 76:303–307. doi: 10.1016/j.maturitas.2013.09.014 Google Scholar
  27. de Klerk E, den Dunnen J, 't Hoen PC (2014) RNA sequencing: from tag-based profiling to resolving complete transcript structure. Cellular and Molecular Life Sciences:1-15 doi: 10.1007/s00018-014-1637-9
  28. De Preter V, Ghebretinsae AH, Abrahantes JC, Windey K, Rutgeerts P, Verbeke K (2011a) Impact of the symbiotic combination of Lactobacillus casei shirota and oligofructose-enriched inulin on the fecal volatile metabolite profile in healthy subjects. Mol Nutr Food Res 55:714–722. doi: 10.1002/mnfr.201000442 Google Scholar
  29. De Preter V, Hamer HM, Windey K, Verbeke K (2011b) The impact of pre- and/or probiotics on human colonic metabolism: does it affect human health? Mol Nutr Food Res 55:46–57. doi: 10.1002/mnfr.201000451 Google Scholar
  30. de Vos WM, Hugenholtz J (2004) Engineering metabolic highways in Lactococci and other lactic acid bacteria. Trends Biotechnol 22:72–79. doi: 10.1016/j.tibtech.2003.11.011 Google Scholar
  31. Del Piano M et al (2006) Probiotics: from research to consumer. Dig Liver Dis 38(Suppl 2):S248–S255. doi: 10.1016/S1590-8658(07)60004-8 Google Scholar
  32. Del Piano M, Carmagnola S, Anderloni A, Andorno S, Ballarè M, Balzarini M, Montino F, Orsello M, Pagliarulo M, Sartori M, Tari R, Sforza F, Capurso L (2010) The use of probiotics in healthy volunteers with evacuation disorders and hard stools: a double-blind, randomized, placebo-controlled study. J Clin Gastroenterol 44(Suppl 1):S30–S34. doi: 10.1097/MCG.0b013e3181ee31c3
  33. Delia A, Morgante G, Rago G, Musacchio MC, Petraglia F, De Leo V (2006) Effectiveness of oral administration of Lactobacillus paracasei subsp. paracasei F19 in association with vaginal suppositories of Lactobacillus acidofilus in the treatment of vaginosis and in the prevention of recurrent vaginitis. Minerva Ginecol 58:227–231Google Scholar
  34. Deshpande G, Rao S, Patole S (2011) Progress in the field of probiotics: year 2011. Curr Opin Gastroenterol 27:13–18. doi: 10.1097/MOG.0b013e328341373e Google Scholar
  35. Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818. doi: 10.1038/nature06245 Google Scholar
  36. Di Cagno R, De Angelis M, Calasso M, Gobbetti M (2011) Proteomics of the bacterial cross-talk by quorum sensing. J Proteomics 74:19–34. doi: 10.1016/j.jprot.2010.09.003 Google Scholar
  37. Di Cagno R et al (2010) Quorum sensing in sourdough Lactobacillus plantarum DC400: induction of plantaricin A (PlnA) under co-cultivation with other lactic acid bacteria and effect of PlnA on bacterial and Caco-2 cells. Proteomics 10:2175–2190. doi: 10.1002/pmic.200900565 Google Scholar
  38. Diaz-Torres ML et al (2006) Determining the antibiotic resistance potential of the indigenous oral microbiota of humans using a metagenomic approach. Fems Microbiology Letters 258:257–262. doi: 10.1111/j.1574-6968.2006.00221.x Google Scholar
  39. Diaz Heijtz R et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108:3047–3052. doi: 10.1073/pnas.1010529108 Google Scholar
  40. Dimitrov DV (2011) The human gutome: nutrigenomics of the host-microbiome interactions. OMICS 15:419–430. doi: 10.1089/omi.2010.0109 Google Scholar
  41. Dumas ME, Kinross J, Nicholson JK (2014) Metabolic phenotyping and systems biology approaches to understanding metabolic syndrome and fatty liver disease. Gastroenterology 146:46–62. doi: 10.1053/j.gastro.2013.11.001 Google Scholar
  42. Dusko Ehrlich S, Meta HIT (2010) Metagenomics of the intestinal microbiota: potential applications. Gastroenterol Clin Biol 34(1):S23–S28. doi: 10.1016/S0399-8320(10)70017-8 Google Scholar
  43. Eckburg PB et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638. doi: 10.1126/science.1110591 Google Scholar
  44. Eliasson M, Rannar S, Trygg J (2011) From data processing to multivariate validation—essential steps in extracting interpretable information from metabolomics data. Curr Pharm Biotechnol 12:996–1004Google Scholar
  45. Fakhry S, Manzo N, D'Apuzzo E, Pietrini L, Sorrentini I, Ricca E, De Felice M, Baccigalupi L (2009) Characterization of intestinal bacteria tightly bound to the human ileal epithelium. Res Microbiol 160(10):817–823. doi: 10.1016/j.resmic.2009.09.009
  46. Fenech M et al (2011) Nutrigenetics and nutrigenomics: viewpoints on the current status and applications in nutrition research and practice. J Nutrigenet Nutrigenomics 4:69–89. doi: 10.1159/000327772 Google Scholar
  47. Ferguson LR, Shelling AN, Lauren D, Heyes JA, McNabb WC, Nutrigenomics New Z (2007) Nutrigenomics and gut health. Mutat Res 622:1–6. doi: 10.1016/j.mrfmmm.2007.05.001 Google Scholar
  48. Fredslund F, Hachem MA, Larsen RJ, Sorensen PG, Coutinho PM, Lo Leggio L, Svensson B (2011) Crystal structure of alpha-galactosidase from Lactobacillus acidophilus NCFM: insight into tetramer formation and substrate binding. J Mol Biol 412:466–480. doi: 10.1016/j.jmb.2011.07.057 Google Scholar
  49. Freitas M, Tavan E, Cayuela C, Diop L, Sapin C, Trugnan G (2003) Host-pathogens cross-talk. Indigenous bacteria and probiotics also play the game. Biol Cell 95:503–506Google Scholar
  50. Gerasimidis K et al (2014a) Decline in presumptively protective gut bacterial species and metabolites are paradoxically associated with disease improvement in pediatric Crohn's disease during enteral nutrition. Inflamm Bowel Dis 20:861–871. doi: 10.1097/mib.0000000000000023 Google Scholar
  51. Gerasimidis K et al. (2014b) Reply to Sokol and Langella: Role of Faecalibacterium prausnitzii in Crohn's disease: friend, foe, or does not really matter? Inflammatory bowel diseases Publish Ahead of Print: 10.1097/MIB.0000000000000079
  52. German JB, Roberts MA, Watkins SM (2003) Personal metabolomics as a next generation nutritional assessment. J Nutr 133:4260–4266Google Scholar
  53. Ghishan FK, Kiela PR (2011) From probiotics to therapeutics: another step forward? J Clin Invest 121:2149–2152. doi: 10.1172/JCI58025 Google Scholar
  54. Gilad O, Svensson B, Viborg AH, Stuer-Lauridsen B, Jacobsen S (2011) The extracellular proteome of Bifidobacterium animalis subsp. lactis BB-12 reveals proteins with putative roles in probiotic effects. Proteomics 11:2503–2514. doi: 10.1002/pmic.201000716 Google Scholar
  55. Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. doi: 10.1126/science.1124234 Google Scholar
  56. Gloux K et al (2007) Development of high-throughput phenotyping of metagenomic clones from the human gut microbiome for modulation of eukaryotic cell growth. Appl Environ Microbiol 73:3734–3737. doi: 10.1128/AEM.02204-06 Google Scholar
  57. Golowczyc MA, Silva J, Abraham AG, De Antoni GL, Teixeira P (2010) Preservation of probiotic strains isolated from kefir by spray drying. Lett Appl Microbiol 50(1):7–12. doi: 10.1111/j.1472-765X.2009.02759.x
  58. Gomez-Llorente C et al (2013) Three main factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr 57:461–466. doi: 10.1097/MPG.0b013e31829d519a Google Scholar
  59. Gorg A, Weiss W, Dunn MJ (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics 4:3665–3685. doi: 10.1002/pmic.200401031 Google Scholar
  60. Grangette C et al (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A 102:10321–10326. doi: 10.1073/pnas.0504084102 Google Scholar
  61. Grindberg RV et al (2013) RNA-sequencing from single nuclei. Proc Natl Acad Sci U S A 110:19802–19807. doi: 10.1073/pnas.1319700110 Google Scholar
  62. Gueniche A et al (2010) Bifidobacterium longum lysate, a new ingredient for reactive skin. Exp Dermatol 19:e1–e8. doi: 10.1111/j.1600-0625.2009.00932.x Google Scholar
  63. Hisbergues M et al (2007) In vivo and in vitro immunomodulation of Der p 1 allergen-specific response by Lactobacillus plantarum bacteria. Clin Exp Allergy 37:1286–1295. doi: 10.1111/j.1365-2222.2007.02792.x Google Scholar
  64. Hong YS et al (2011) Metabonomic understanding of probiotic effects in humans with irritable bowel syndrome. J Clin Gastroenterol 45:415–425. doi: 10.1097/MCG.0b013e318207f76c Google Scholar
  65. Huang CH, Lee FL (2011) The dnaK gene as a molecular marker for the classification and discrimination of the Lactobacillus casei group. Antonie Van Leeuwenhoek 99(2):319–327. doi: 10.1007/s10482-010-9493-6
  66. Iannitti T, Palmieri B (2010) Therapeutical use of probiotic formulations in clinical practice. Clin Nutr 29:701–725. doi: 10.1016/j.clnu.2010.05.004 Google Scholar
  67. Iguchi A, Umekawa N, Maegawa T, Tsuruta H, Odamaki T, Xiao JZ, Osawa R (2011) Polymorphism and distribution of putative cell-surface adhesin-encoding ORFs among human fecal isolates of Bifidobacterium longum subsp. longum. Antonie Van Leeuwenhoek 99(3):457–471. doi: 10.1007/s10482-010-9506-5
  68. Izquierdo E, Medina M, Ennahar S, Marchioni E, Sanz Y (2008) Resistance to simulated gastrointestinal conditions and adhesion to mucus as probiotic criteria for Bifidobacterium longum strains. Curr Microbiol 56(6):613–618. doi: 10.1007/s00284-008-9135-7
  69. Jackson EL, Hamlin PJ, Ford AC (2011) VSL#3 and remission in active ulcerative colitis: larger studies required. Am J Gastroenterol 106:547, author reply 547-548Google Scholar
  70. Jimenez-Pranteda ML, Poncelet D, Nader-Macias ME, Arcos A, Aguilera M, Monteoliva-Sanchez M, Ramos-Cormenzana A (2012) Stability of lactobacilli encapsulated in various microbial polymers. J Biosci Bioeng 113:179–184. doi: 10.1016/j.jbiosc.2011.10.010 Google Scholar
  71. Kant R, Blom J, Palva A, Siezen RJ, de Vos WM (2011) Comparative genomics of Lactobacillus. Microb Biotechnol 4:323–332. doi: 10.1111/j.1751-7915.2010.00215.x Google Scholar
  72. Kawase M, He F, Kubota A, Harata G, Hiramatsu M (2010) Oral administration of lactobacilli from human intestinal tract protects mice against influenza virus infection. Lett Appl Microbiol 51:6–10. doi: 10.1111/j.1472-765X.2010.02849.x Google Scholar
  73. Kekkonen RA, Sysi-Aho M, Seppanen-Laakso T, Julkunen I, Vapaatalo H, Oresic M, Korpela R (2008) Effect of probiotic Lactobacillus rhamnosus GG intervention on global serum lipidomic profiles in healthy adults. World J Gastroenterol 14:3188–3194Google Scholar
  74. Klaassens ES, de Vos WM, Vaughan EE (2007) Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl Environ Microbiol 73:1388–1392. doi: 10.1128/AEM.01921-06 Google Scholar
  75. Klaenhammer TR et al (2008) Functional genomics of probiotic Lactobacilli. J Clin Gastroenterol 42(3 Pt 2):S160–S162. doi: 10.1097/MCG.0b013e31817da140 Google Scholar
  76. Klaenhammer TR, Barrangou R, Buck BL, Azcarate-Peril MA, Altermann E (2005) Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29:393–409. doi: 10.1016/j.femsre.2005.04.007 Google Scholar
  77. Kleerebezem M et al (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990–1995. doi: 10.1073/pnas.0337704100 Google Scholar
  78. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, Bron PA (2010) The extracellular biology of the lactobacilli. FEMS Microbiol Rev 34:199–230. doi: 10.1111/j.1574-6976.2010.00208.x Google Scholar
  79. Koeth RA et al (2013) Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19:576–585. doi: 10.1038/nm.3145 Google Scholar
  80. Koyama T, Kirjavainen PV, Fisher C, Anukam K, Summers K, Hekmat S, Reid G (2010) Development and pilot evaluation of a novel probiotic mixture for the management of seasonal allergic rhinitis. Can J Microbiol 56(9):730–738. doi: 10.1139/w10-061
  81. Kurokawa K et al (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14:169–181. doi: 10.1093/dnares/dsm018 Google Scholar
  82. Kussmann M, Raymond F, Affolter M (2006) OMICS-driven biomarker discovery in nutrition and health. J Biotechnol 124:758–787. doi: 10.1016/j.jbiotec.2006.02.014 Google Scholar
  83. Lamiki P et al (2010) Probiotics in diverticular disease of the colon: an open label study. J Gastrointestin Liver Dis 19:31–36Google Scholar
  84. Le Cao KA, Gonzalez I, Dejean S (2009) integrOmics: an R package to unravel relationships between two omics datasets. Bioinformatics 25:2855–2856. doi: 10.1093/bioinformatics/btp515 Google Scholar
  85. Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764. doi: 10.1128/MMBR.00017-08, Table of ContentsGoogle Scholar
  86. Lebeer S, Vanderleyden J, De Keersmaecker SC (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8:171–184. doi: 10.1038/nrmicro2297 Google Scholar
  87. LeBlanc JG, Sybesma W, Starrenburg M, Sesma F, de Vos WM, de Giori GS, Hugenholtz J (2010) Supplementation with engineered Lactococcus lactis improves the folate status in deficient rats. Nutrition 26:835–841. doi: 10.1016/j.nut.2009.06.023 Google Scholar
  88. Lee JH, O'Sullivan DJ (2010) Genomic insights into bifidobacteria. Microbiol Mol Biol Rev 74:378–416. doi: 10.1128/MMBR.00004-10 Google Scholar
  89. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848. doi: 10.1016/j.cell.2006.02.017 Google Scholar
  90. Licciardi PV, Wong S-S, Tang MLK, Karagiannis TC (2010) Epigenome targeting by probiotic metabolites. Gut Pathogens 2 doi: 2410.1186/1757-4749-2-24Google Scholar
  91. Lim EM, Ehrlich SD, Maguin E (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus. Electrophoresis 21:2557–2561. doi: 10.1002/1522-2683(20000701) Google Scholar
  92. Luoto R, Laitinen K, Nermes M, Isolauri E (2010) Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr 103:1792–1799. doi: 10.1017/S0007114509993898 Google Scholar
  93. Ly NP, Litonjua A, Gold DR, Celedon JC (2011) Gut microbiota, probiotics, and vitamin D: interrelated exposures influencing allergy, asthma, and obesity? J Allergy Clin Immunol 127:1087–1094. doi: 10.1016/j.jaci.2011.02.015 Google Scholar
  94. MacFabe DF (2012) Short-chain fatty acid fermentation products of the gut microbiome: implications in autism spectrum disorders. Microbial ecology in health and disease 23:19260 doi:10.3402/mehd.v23i0Google Scholar
  95. Macho Fernandez E, Pot B, Grangette C (2011) Beneficial effect of probiotics in IBD: are peptidogycan and NOD2 the molecular key effectors? Gut Microbes 2(5):280–286. doi: 10.4161/gmic.2.5.18255
  96. Macías-Rodríguez ME, Zagorec M, Ascencio F, Vázquez-Juárez R, Rojas M (2009) Lactobacillus fermentum BCS87 expresses mucus- and mucin-binding proteins on the cell surface. J Appl Microbiol 107(6):1866–1874. doi: 10.1111/j.1365-2672.2009.04368.x
  97. MacPhee RA, Hummelen R, Bisanz JE, Miller WL, Reid G (2010) Probiotic strategies for the treatment and prevention of bacterial vaginosis. Expert Opin Pharmacother 11:2985–2995. doi: 10.1517/14656566.2010.512004 Google Scholar
  98. Madsen K (2011) Using metabolomics to decipher probiotic effects in patients with irritable bowel syndrome. J Clin Gastroenterol 45(5):389–390. doi: 10.1097/MCG.0b013e31821377cf
  99. Madsen R, Lundstedt T, Trygg J (2010) Chemometrics in metabolomics—a review in human disease diagnosis. Anal Chim Acta 659:23–33. doi: 10.1016/j.aca.2009.11.042 Google Scholar
  100. Makarova K et al (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103:15611–15616. doi: 10.1073/pnas.0607117103 Google Scholar
  101. Mangian HF, Tappenden KA (2009) Butyrate increases GLUT2 mRNA abundance by initiating transcription in Caco2-BBe cells. JPEN J Parenter Enteral Nutr 33:607–617. doi: 10.1177/0148607109336599, discussion 617Google Scholar
  102. Manichanh C et al (2006) Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55:205–211. doi: 10.1136/gut.2005.073817 Google Scholar
  103. Marco ML et al (2010) Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J 4:1481–1484. doi: 10.1038/ismej.2010.61 Google Scholar
  104. Marchesi J, Shanahan F (2007) The normal intestinal microbiota. Curr Opin Infect Dis 20:508–513. doi: 10.1097/QCO.0b013e3282a56a99 Google Scholar
  105. Marques SCF, Oliveira CR, Pereira CMF, Outeiro TF (2011) Epigenetics in neurodegeneration: A new layer of complexity. Prog Neuropsychopharmacol Biol Psychiatry 35:348–355. doi: 10.1016/j.pnpbp.2010.08.008 Google Scholar
  106. Martin FP et al (2007) A top-down systems biology view of microbiome–mammalian metabolic interactions in a mouse model. Mol Syst Biol 3:112. doi: 10.1038/msb4100153 Google Scholar
  107. Martin FP, Sprenger N, Montoliu I, Rezzi S, Kochhar S, Nicholson JK (2010) Dietary modulation of gut functional ecology studied by fecal metabonomics. J Proteome Res 9:5284–5295. doi: 10.1021/pr100554m Google Scholar
  108. Martins FS et al (2010) Interaction of Saccharomyces boulardii with Salmonella enterica serovar Typhimurium protects mice and modifies T84 cell response to the infection. PLoS One 5:8925. doi: 10.1371/journal.pone.0008925 Google Scholar
  109. Matsuyama A et al (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24:841–847. doi: 10.1038/nbt1222 Google Scholar
  110. Mayer EA (2011) Gut feelings: the emerging biology of gut–brain communication. Nat Rev Neurosci 12:453–466. doi: 10.1038/nrn3071 Google Scholar
  111. McCartney AL (2002) Application of molecular biological methods for studying probiotics and the gut flora. Br J Nutr 88(1):S29–S37. doi: 10.1079/BJN2002627 Google Scholar
  112. Miquel S et al (2014) Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes 5:146–151Google Scholar
  113. Monteoliva-Sánchez M, Aguilera M, Jiménez-Pranteda ML, Ramos-Cormenzana A (2010) Probióticos en las distintas etapas de la vida. In: Ramos-Cormenzana A, Nader-Macías F, Monteoliva-Sánchez M (eds) Probióticos y salud. Díaz de Santos, MadridGoogle Scholar
  114. Morelli L, Capurso L (2012) FAO/WHO Guidelines on probiotics 10 years later. FOREWORD. J Clin Gastroenterol 46:S1–S2Google Scholar
  115. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, Relman DA, Banfield JF (2011) Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci U S A 108:1128–1133. doi: 10.1073/pnas.1010992108 Google Scholar
  116. Mortimer SA, Kidwell MA, Doudna JA (2014) Insights into RNA structure and function from genome-wide studies. Nat Rev Genet advance online publicationGoogle Scholar
  117. Muegge BD et al (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974. doi: 10.1126/science.1198719 Google Scholar
  118. Nakanishi Y, Fukuda S, Chikayama E, Kimura Y, Ohno H, Kikuchi J (2011) Dynamic omics approach identifies nutrition-mediated microbial interactions. J Proteome Res 10:824–836. doi: 10.1021/pr100989c Google Scholar
  119. Nanno M, Kato I, Kobayashi T, Shida K (2011) Biological effects of probiotics: what impact does Lactobacillus casei shirota have on us? Int J Immunopathol Pharmacol 24:45S–50SGoogle Scholar
  120. Nielsen VR MK, Paerregaard A (2002) Lactic bacteria and other probiotics in infections and inflammatory diseases in children. What do we believe?—What do we know? Ugeskr Laeger 2(164):5769–5772Google Scholar
  121. Nieuwenhuizen NE, Lopata AL (2005) Fighting food allergy: current approaches. Ann N Y Acad Sci 1056:30–45. doi: 10.1196/annals.1352.003 Google Scholar
  122. O'Connell Motherway M et al (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 108:11217–11222. doi: 10.1073/pnas.1105380108 Google Scholar
  123. O'Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693. doi: 10.1038/sj.embor.7400731 Google Scholar
  124. O'Hara AM, Shanahan F (2007) Gut microbiota: mining for therapeutic potential. Clin Gastroenterol Hepatol 5:274–284. doi: 10.1016/j.cgh.2006.12.009 Google Scholar
  125. O'Sullivan O et al (2009) Comparative genomics of lactic acid bacteria reveals a niche-specific gene set. BMC Microbiol 9:50. doi: 10.1186/1471-2180-9-50 Google Scholar
  126. Ohara T, Yoshino K, Kitajima M (2010) Possibility of preventing colorectal carcinogenesis with probiotics. Hepatogastroenterology 57:1411–1415Google Scholar
  127. Ohigashi S, Hoshino Y, Ohde S, Onodera H (2011) Functional outcome, quality of life, and efficacy of probiotics in postoperative patients with colorectal cancer. Surg Today 41:1200–1206. doi: 10.1007/s00595-010-4450-6 Google Scholar
  128. Ozdemir V, Suarez-Kurtz G, Stenne R, Somogyi AA, Someya T, Kayaalp SO, Kolker E (2009) Risk assessment and communication tools for genotype associations with multifactorial phenotypes: the concept of "edge effect" and cultivating an ethical bridge between omics innovations and society. OMICS 13:43–61. doi: 10.1089/omi.2009.0011 Google Scholar
  129. Panduru M, Panduru NM, Sălăvăstru CM, Tiplica GS (2014) Probiotics and primary prevention of atopic dermatitis: a meta-analysis of randomized controlled studies. J Eur Acad Dermatol Venereol. doi: 10.1111/jdv.12496 Google Scholar
  130. Ponnusamy K, Choi JN, Kim J, Lee SY, Lee CH (2011) Microbial community and metabolomic comparison of irritable bowel syndrome faeces. J Med Microbiol 60:817–827. doi: 10.1099/jmm.0.028126-0 Google Scholar
  131. Rajilic-Stojanovic M, Smidt H, de Vos WM (2007) Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 9:2125–2136. doi: 10.1111/j.1462-2920.2007.01369 Google Scholar
  132. Ramos-Cormenzana A, Fuentes S, Ferrer-Cebrian R, Monteoliva-Sánchez M (2005) Probiotics and biotherapy. Recent Research Developments in Microbiology 9:97–127Google Scholar
  133. Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ (2011) Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 9:27–38. doi: 10.1038/nrmicro2473 Google Scholar
  134. Rescigno M (2008) The pathogenic role of intestinal flora in IBD and colon cancer. Curr Drug Targets 9:395–403Google Scholar
  135. Ruiz L, Gueimonde M, Couté Y, Salminen S, Sanchez JC, de los Reyes-Gavilán CG, Margolles A (2011) Evaluation of the ability of Bifidobacterium longum to metabolize human intestinal mucus. FEMS Microbiol Lett 314(2):125–130. doi: 10.1111/j.1574-6968.2010.02159.x
  136. Saleh M, Trinchieri G (2011) Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol 11:9–20. doi: 10.1038/nri2891 Google Scholar
  137. Sato T et al (2011) Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141:1762–1772. doi: 10.1053/j.gastro.2011.07.050 Google Scholar
  138. Saulnier DM et al (2011) Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PLoS One 6:e18783. doi: 10.1371/journal.pone.0018783 Google Scholar
  139. Savage M (2001) Complications with reformulated one-alpha vitamin D. BMJ 322:799Google Scholar
  140. Savijoki K, Lietzén N, Kankainen M, Alatossava T, Koskenniemi K, Varmanen P, Nyman TA (2011) Comparative proteome cataloging of Lactobacillus rhamnosus strains GG and Lc705. J Proteome Res 10(8):3460–3473. doi: 10.1021/pr2000896
  141. Saxelin M et al (2010) Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. Int J Food Microbiol 144:293–300. doi: 10.1016/j.ijfoodmicro.2010.10.009 Google Scholar
  142. Schell MA et al (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99:14422–14427. doi: 10.1073/pnas.212527599 Google Scholar
  143. Secher T, Gaillot O, Ryffel B, Chamaillard M (2010) Remote control of intestinal tumorigenesis by innate immunity. Cancer Res 70:1749–1752. doi: 10.1158/0008-5472.CAN-09-3401 Google Scholar
  144. Seksik P et al (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52:237–242Google Scholar
  145. Shanahan F (2005) Physiological basis for novel drug therapies used to treat the inflammatory bowel diseases I. Pathophysiological basis and prospects for probiotic therapy in inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 288:G417–G421. doi: 10.1152/ajpgi.00421.2004 Google Scholar
  146. Shen S, Qu Y, Zhang J (2014) The application of next generation sequencing on epigenetic study. Yi chuan =. Hereditas / Zhongguo yi chuan xue hui bian ji 36:256–275Google Scholar
  147. Shenderov BA (2012) Gut indigenous microbiota and epigenetics. Microbial ecology in health and disease 23 doi:10.3402/mehd.v23i0.17195Google Scholar
  148. Shima T et al (2008) Differential effects of two probiotic strains with different bacteriological properties on intestinal gene expression, with special reference to indigenous bacteria. FEMS Immunol Med Microbiol 52:69–77. doi: 10.1111/j.1574-695X.2007.00344.x Google Scholar
  149. Skoog EC, Lindberg M, Lindén SK (2011) Strain-dependent proliferation in response to human gastric mucin and adhesion properties of Helicobacter pylori are not affected by co-isolated Lactobacillus sp. Helicobacter 16(1):9–19. doi: 10.1111/j.1523-5378.2010.00810.x
  150. Sokol H, Langella P (2014) Beneficial effects of exclusive enteral nutrition in Crohn's disease are not mediated by Faecalibacterium prausnitzii. Inflammatory bowel diseases Publish Ahead of Print: 10.1097/MIB.0000000000000071
  151. Sonnenburg JL, Chen CT, Gordon JI (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4:e413. doi: 10.1371/journal.pbio.0040413 Google Scholar
  152. Spear GT, Gilbert D, Landay AL, Zariffard R, French AL, Patel P, Gillevet PM (2011) Pyrosequencing of the genital microbiotas of HIV-seropositive and -seronegative women reveals Lactobacillus iners as the predominant Lactobacillus species. Appl Environ Microbiol 77:378–381. doi: 10.1128/AEM.00973-10 Google Scholar
  153. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290. doi: 10.1038/nrmicro2540 Google Scholar
  154. Stanghellini V et al (2010) Gut microbiota and related diseases: clinical features. Intern Emerg Med 5(Suppl 1):S57–S63. doi: 10.1007/s11739-010-0451-0 Google Scholar
  155. Stecher B et al (2010) Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6:e1000711. doi: 10.1371/journal.ppat.1000711 Google Scholar
  156. Stewart JA, Chadwick VS, Murray A (2005) Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children. J Med Microbiol 54:1239–1242. doi: 10.1099/jmm.0.46189-0 Google Scholar
  157. Stover PJ, Caudill MA (2008) Genetic and epigenetic contributions to human nutrition and health: managing genome–diet interactions. J Am Diet Assoc 108:1480–1487. doi: 10.1016/j.jada.2008.06.430 Google Scholar
  158. Tannock GW (1999) Analysis of the intestinal microflora: a renaissance. Antonie Van Leeuwenhoek 76:265–278Google Scholar
  159. Thierry AC, Bernasconi E, Mercenier A, Corthésy B (2009) Conditioned polarized Caco-2 cell monolayers allow to discriminate for the ability of gut-derived microorganisms to modulate permeability and antigen-induced basophil degranulation. Clin Exp Allergy 39(4):527–536. doi: 10.1111/j.1365-2222.2008.03185.x
  160. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031. doi: 10.1038/nature05414 Google Scholar
  161. Turnbaugh PJ et al (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci U S A 107:7503–7508. doi: 10.1073/pnas.1002355107 Google Scholar
  162. Van Huynegem K, Loos M, Steidler L (2009) Immunomodulation by genetically engineered lactic acid bacteria. Front Biosci (Landmark Ed) 14:4825–4835Google Scholar
  163. Vaughan EE, de Vries MC, Zoetendal EG, Ben-Amor K, Akkermans AD, de Vos WM (2002) The intestinal LABs. Antonie Van Leeuwenhoek 82:341–352Google Scholar
  164. Veltman K, Hummel S, Cichon C, Sonnenborn U, Schmidt MA (2012) Identification of specific miRNAs targeting proteins of the apical junctional complex that simulate the probiotic effect of E. coli Nissle 1917 on T84 epithelial cells. International Journal of Biochemistry & Cell Biology 44:341–349. doi: 10.1016/j.biocel.2011.11.006 Google Scholar
  165. Ventura M, van Sinderen D, Fitzgerald GF, Zink R (2004) Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86:205–223. doi: 10.1023/ Google Scholar
  166. Verna EC, Lucak S (2010) Use of probiotics in gastrointestinal disorders: what to recommend? Therap Adv Gastroenterol 3:307–319. doi: 10.1177/1756283X10373814 Google Scholar
  167. Vitali B, Wasinger V, Brigidi P, Guilhaus M (2005) A proteomic view of Bifidobacterium infantis generated by multi-dimensional chromatography coupled with tandem mass spectrometry. Proteomics 5:1859–1867. doi: 10.1002/pmic.200401080 Google Scholar
  168. Vrieze A, Holleman F, Zoetendal EG, de Vos WM, Hoekstra JB, Nieuwdorp M (2010) The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia 53:606–613. doi: 10.1007/s00125-010-1662-7 Google Scholar
  169. Waddington L, Cyr T, Hefford M, Hansen LT, Kalmokoff M (2010) Understanding the acid tolerance response of bifidobacteria. J Appl Microbiol 108:1408–1420. doi: 10.1111/j.1365-2672.2009.04540.x Google Scholar
  170. Washburn MP, Wolters D, Yates JR 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19:242–247. doi: 10.1038/85686 Google Scholar
  171. Worthley DL et al (2009) A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. Am J Clin Nutr 90:578–586. doi: 10.3945/ajcn.2009.28106 Google Scholar
  172. Xiong P, Zhou J-l, Xiao L-y, Kong X-l, Li J-y, Jia X-m, Li W (2008) Initial study on the discrimination of oral microorganisms with a metabonomics method. Hua xi kou qiang yi xue za zhi = Huaxi kouqiang yixue zazhi = West China journal of stomatology 26:537-540Google Scholar
  173. Zeisel SH et al (2005) The nutritional phenotype in the age of metabolomics. J Nutr 135:1613–1616Google Scholar
  174. Zhang C et al (2010) Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4:232–241. doi: 10.1038/ismej.2009.112 Google Scholar
  175. Zhou M, Theunissen D, Wels M, Siezen RJ (2010) LAB-Secretome: a genome-scale comparative analysis of the predicted extracellular and surface-associated proteins of lactic acid bacteria. BMC Genomics 11:651. doi: 10.1186/1471-2164-11-651 Google Scholar
  176. Zhu B, Wang X, Li L (2010) Human gut microbiome: the second genome of human body. Protein Cell 1:718–725. doi: 10.1007/s13238-010-0093-z Google Scholar
  177. Zhu Y, Michelle Luo T, Jobin C, Young HA (2011) Gut microbiota and probiotics in colon tumorigenesis. Cancer Lett 309:119–127. doi: 10.1016/j.canlet.2011.06.004 Google Scholar
  178. Zoetendal EG, Ben-Amor K, Akkermans AD, Abee T, de Vos WM (2001) DNA isolation protocols affect the detection limit of PCR approaches of bacteria in samples from the human gastrointestinal tract. Syst Appl Microbiol 24:405–410. doi: 10.1078/0723-2020-00060 Google Scholar
  179. Zoetendal EG, Cheng B, Koike S, Mackie RI (2004) Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Curr Issues Intest Microbiol 5:31–47Google Scholar
  180. Zoetendal EG, Vaughan EE, de Vos WM (2006) A microbial world within us. Mol Microbiol 59:1639–1650. doi: 10.1111/j.1365-2958.2006.05056.x Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • María Luján Jiménez-Pranteda
    • 1
    • 2
  • Azahara Pérez-Davó
    • 1
  • Mercedes Monteoliva-Sánchez
    • 1
  • Alberto Ramos-Cormenzana
    • 1
  • Margarita Aguilera
    • 1
    • 2
    Email author
  1. 1.Department of Microbiology, School of PharmacyUniversity of GranadaGranadaSpain
  2. 2.INYTA, Institute of Nutrition and Food TechnologyCIBMGranadaSpain

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