Abstract
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.
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References
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 e71-72
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
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
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
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 10:29
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
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
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
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
Bayoumi MA, Griffiths MW (2010) Probiotics down-regulate genes in Salmonella enterica serovar typhimurium pathogenicity islands 1 and 2. J Food Prot 73:452–460
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
Berlec A, Strukelj B (2009) Novel applications of recombinant lactic acid bacteria in therapy and in metabolic engineering. Recent Pat Biotechnol 3:77–87
Bernini P et al (2009) Individual human phenotypes in metabolic space and time. J Proteome Res 8:4264–4271. doi:10.1021/pr900344m
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
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
Bottacini F et al (2010) Comparative genomics of the genus Bifidobacterium. Microbiology 156:3243–3254. doi:10.1099/mic.0.039545-0
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
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
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
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
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
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
Catalioto RM, Maggi CA, Giuliani S (2011) Intestinal epithelial barrier dysfunction in disease and possible therapeutical interventions. Curr Med Chem 18:398–426
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
Cutting SM (2011) Bacillus probiotics. Food Microbiol 28:214–220. doi:10.1016/j.fm.2010.03.007
Chrysohoou C, Stefanadis C (2013) Longevity and diet. Myth or pragmatism? Maturitas 76:303–307. doi:10.1016/j.maturitas.2013.09.014
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
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
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
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
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
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
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 58:227–231
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
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
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
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
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
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
Dimitrov DV (2011) The human gutome: nutrigenomics of the host-microbiome interactions. OMICS 15:419–430. doi:10.1089/omi.2010.0109
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
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
Eckburg PB et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638. doi:10.1126/science.1110591
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 12:996–1004
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
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
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
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
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 95:503–506
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
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
German JB, Roberts MA, Watkins SM (2003) Personal metabolomics as a next generation nutritional assessment. J Nutr 133:4260–4266
Ghishan FK, Kiela PR (2011) From probiotics to therapeutics: another step forward? J Clin Invest 121:2149–2152. doi:10.1172/JCI58025
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
Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. doi:10.1126/science.1124234
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
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
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
Gorg A, Weiss W, Dunn MJ (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics 4:3665–3685. doi:10.1002/pmic.200401031
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
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
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
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
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
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
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
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
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
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 547-548
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
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
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
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 14:3188–3194
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
Klaenhammer TR et al (2008) Functional genomics of probiotic Lactobacilli. J Clin Gastroenterol 42(3 Pt 2):S160–S162. doi:10.1097/MCG.0b013e31817da140
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
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
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
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
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
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
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
Lamiki P et al (2010) Probiotics in diverticular disease of the colon: an open label study. J Gastrointestin Liver Dis 19:31–36
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
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 Contents
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
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
Lee JH, O'Sullivan DJ (2010) Genomic insights into bifidobacteria. Microbiol Mol Biol Rev 74:378–416. doi:10.1128/MMBR.00004-10
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
Licciardi PV, Wong S-S, Tang MLK, Karagiannis TC (2010) Epigenome targeting by probiotic metabolites. Gut Pathogens 2 doi: 2410.1186/1757-4749-2-24
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)
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
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
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.v23i0
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
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
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
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
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
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
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 617
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
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
Marchesi J, Shanahan F (2007) The normal intestinal microbiota. Curr Opin Infect Dis 20:508–513. doi:10.1097/QCO.0b013e3282a56a99
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
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
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
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
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
Mayer EA (2011) Gut feelings: the emerging biology of gut–brain communication. Nat Rev Neurosci 12:453–466. doi:10.1038/nrn3071
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
Miquel S et al (2014) Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes 5:146–151
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, Madrid
Morelli L, Capurso L (2012) FAO/WHO Guidelines on probiotics 10 years later. FOREWORD. J Clin Gastroenterol 46:S1–S2
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
Mortimer SA, Kidwell MA, Doudna JA (2014) Insights into RNA structure and function from genome-wide studies. Nat Rev Genet advance online publication
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
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
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–50S
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):5769–5772
Nieuwenhuizen NE, Lopata AL (2005) Fighting food allergy: current approaches. Ann N Y Acad Sci 1056:30–45. doi:10.1196/annals.1352.003
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
O'Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693. doi:10.1038/sj.embor.7400731
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
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
Ohara T, Yoshino K, Kitajima M (2010) Possibility of preventing colorectal carcinogenesis with probiotics. Hepatogastroenterology 57:1411–1415
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
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
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
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
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
Ramos-Cormenzana A, Fuentes S, Ferrer-Cebrian R, Monteoliva-Sánchez M (2005) Probiotics and biotherapy. Recent Research Developments in Microbiology 9:97–127
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
Rescigno M (2008) The pathogenic role of intestinal flora in IBD and colon cancer. Curr Drug Targets 9:395–403
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
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
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
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
Savage M (2001) Complications with reformulated one-alpha vitamin D. BMJ 322:799
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
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
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
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
Seksik P et al (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52:237–242
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
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 36:256–275
Shenderov BA (2012) Gut indigenous microbiota and epigenetics. Microbial ecology in health and disease 23 doi:10.3402/mehd.v23i0.17195
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
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
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
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
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
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
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
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
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
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
Tannock GW (1999) Analysis of the intestinal microflora: a renaissance. Antonie Van Leeuwenhoek 76:265–278
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
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
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
Van Huynegem K, Loos M, Steidler L (2009) Immunomodulation by genetically engineered lactic acid bacteria. Front Biosci (Landmark Ed) 14:4825–4835
Vaughan EE, de Vries MC, Zoetendal EG, Ben-Amor K, Akkermans AD, de Vos WM (2002) The intestinal LABs. Antonie Van Leeuwenhoek 82:341–352
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
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/B:ANTO.0000047930.11029.ec
Verna EC, Lucak S (2010) Use of probiotics in gastrointestinal disorders: what to recommend? Therap Adv Gastroenterol 3:307–319. doi:10.1177/1756283X10373814
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
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
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
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
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
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 26:537-540
Zeisel SH et al (2005) The nutritional phenotype in the age of metabolomics. J Nutr 135:1613–1616
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
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
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
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
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
Zoetendal EG, Cheng B, Koike S, Mackie RI (2004) Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Curr Issues Intest Microbiol 5:31–47
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
Acknowledgments
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.
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Jiménez-Pranteda, M.L., Pérez-Davó, A., Monteoliva-Sánchez, M. et al. Food Omics Validation: Towards Understanding Key Features for Gut Microbiota, Probiotics and Human Health. Food Anal. Methods 8, 272–289 (2015). https://doi.org/10.1007/s12161-014-9923-6
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DOI: https://doi.org/10.1007/s12161-014-9923-6