Synthetic Biology Approaches to Engineer Probiotics and Members of the Human Microbiota for Biomedical Applications

Literature Cited

1. 1.  Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH et al. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207–14
   [Google Scholar]
2. 2.  Belizário JE, Napolitano M 2015. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front. Microbiol. 6:1050
   [Google Scholar]
3. 3.  Lau JT, Whelan FJ, Herath I, Lee CH, Collins SM et al. 2016. Capturing the diversity of the human gut microbiota through culture-enriched molecular profiling. Genome Med 8:72
   [Google Scholar]
4. 4.  Langdon A, Crook N, Dantas G 2016. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med 8:39
   [Google Scholar]
5. 5.  Didari T, Mozaffari S, Nikfar S, Abdollahi M 2015. Effectiveness of probiotics in irritable bowel syndrome: updated systematic review with meta-analysis. World J. Gastroenterol. 21:3072–84
   [Google Scholar]
6. 6.  Verna EC, Lucak S 2010. Use of probiotics in gastrointestinal disorders: what to recommend?. Ther. Adv. Gastroenterol. 3:307–19
   [Google Scholar]
7. 7.  Tsai YT, Cheng PC, Pan TM 2014. Anti-obesity effects of gut microbiota are associated with lactic acid bacteria. Appl. Microbiol. Biotechnol. 98:1–10
   [Google Scholar]
8. 8.  Brennan CA, Garrett WS 2016. Gut microbiota, inflammation, and colorectal cancer. Annu. Rev. Microbiol. 70:395–411
   [Google Scholar]
9. 9.  Moos WH, Faller DV, Harpp DN, Kanara I, Pernokas J et al. 2016. Microbiota and neurological disorders: a gut feeling. Biores. Open Access 5:137–45
   [Google Scholar]
10. 10.  Brandwein M, Steinberg D, Meshner S 2016. Microbial biofilms and the human skin microbiome. npj Biofilms Microbiomes 2:3
    [Google Scholar]
11. 11.  Egert M, Simmering R, Riedel CU 2017. The association of the skin microbiota with health, immunity, and disease. Clin. Pharmacol. Ther. 102:62–69
    [Google Scholar]
12. 12.  Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR et al. 2010. The human oral microbiome. J. Bacteriol. 192:5002–17
    [Google Scholar]
13. 13.  Kilian M, Chapple ILC, Hannig M, Marsh PD, Meuric V et al. 2016. The oral microbiome—an update for oral healthcare professionals. Br. Dent. J. 221:657–66
    [Google Scholar]
14. 14.  Gopinath S, Iwasaki A 2015. Cervicovaginal microbiota: Simple is better. Immunity 42:790–91
    [Google Scholar]
15. 15.  Sanders ME, Gibson GR, Gill HS, Guarner F 2007. Probiotics: their potential to impact human health Issue pap. 36 Counc. Agric. Sci. Technol Ames, IA:
16. 16.  Ballal SA, Veiga P, Fenn K, Michaud M, Kim JH et al. 2015. Host lysozyme-mediated lysis of Lactococcuslactis facilitates delivery of colitis-attenuating superoxide dismutase to inflamed colons. PNAS 112:7803–8
    [Google Scholar]
17. 17.  Fedorak RN 2010. Probiotics in the management of ulcerative colitis. Gastroenterol. Hepatol. 6:688–90
    [Google Scholar]
18. 18.  Prantera C 2006. Probiotics for Crohn's disease: What have we learned?. Gut 55:757–59
    [Google Scholar]
19. 19.  van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG et al. 2013. Duodenal infusion of donor feces for recurrent Clostridiumdifficile. . N. Engl. J. Med. 368:407–15
    [Google Scholar]
20. 20.  Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D et al. 2013. Stool substitute transplant therapy for the eradication of Clostridiumdifficile infection: “rePOOPulating” the gut. Microbiome 1:3
    [Google Scholar]
21. 21.  Ullah MW, Khattak WA, Ul-Islam M, Khan S, Park JK 2016. Metabolic engineering of synthetic cell-free systems: strategies and applications. Biochem. Eng. J. 105:391–405
    [Google Scholar]
22. 22.  Cameron DE, Bashor CJ, Collins JJ 2014. A brief history of synthetic biology. Nat. Rev. Microbiol. 12:381–90
    [Google Scholar]
23. 23.  Marchand N, Collins CH 2016. Synthetic quorum sensing and cell–cell communication in gram-positive Bacillusmegaterium. . ACS Synth. Biol. 5:597–606
    [Google Scholar]
24. 24.  Brophy JAN, Voigt CA 2014. Principles of genetic circuit design. Nat. Methods 11:508–20
    [Google Scholar]
25. 25.  Hsu PD, Lander ES, Zhang F 2014. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–78
    [Google Scholar]
26. 26.  Park M, Tsai SL, Chen W 2013. Microbial biosensors: engineered microorganisms as the sensing machinery. Sensors 3:5777–95
    [Google Scholar]
27. 27.  Rong G, Corrie SR, Clark HA 2017. In vivo biosensing: progress and perspectives. ACS Sens 2:327–38
    [Google Scholar]
28. 28.  Cribby S, Taylor M, Reid G 2008. Vaginal microbiota and the use of probiotics. Interdiscip. Perspect. Infect. Dis. 2008:256490
    [Google Scholar]
29. 29.  Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE et al. 2013. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214
    [Google Scholar]
30. 30.  Lagier J-C, Khelaifia S, Alou MT, Ndongo S, Dione N et al. 2016. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat. Microbiol. 1:1–8
    [Google Scholar]
31. 31.  Waller MC, Bober JR, Nair NU, Beisel CL 2017. Toward a genetic tool development pipeline for host-associated bacteria. Curr. Opin. Microbiol. 38:156–64
    [Google Scholar]
32. 32.  Spath K, Hein S, Grabherr R 2012. Direct cloning in Lactobacillusplantarum: Electroporation with non-methylated plasmid DNA enhances transformation efficiency and makes shuttle vectors obsolete. Microb. Cell Fact. 11:141
    [Google Scholar]
33. 33.  van Houte S, Buckling A, Westra ER 2016. Evolutionary ecology of prokaryotic immune mechanisms. Microbiol. Mol. Biol. Rev. 80:745–63
    [Google Scholar]
34. 34.  Roberts RJ, Vincze T, Posfai J, Macelis D 2015. REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 43:D298–99
    [Google Scholar]
35. 35.  Kok J, Van Der Vossen JMBM, Venema G 1984. Construction of plasmid cloning vectors for lactic streptococci which also replicate in Bacillussubtilis and Escherichia coli. . Appl. Environ. Microbiol. 48:726–31
    [Google Scholar]
36. 36.  De Vos WM 1987. Gene cloning and expression in lactic streptococci. FEMS Microbiol. Lett. 46:281–95
    [Google Scholar]
37. 37.  Leenhouts KJ, Kok J, Venema G 1991. Lactococcal plasmid pWVO1 as an integration vector for lactococci. Appl. Environ. Microbiol. 57:2562–67
    [Google Scholar]
38. 38.  Fang F, O'Toole PW 2009. Genetic tools for investigating the biology of commensal lactobacilli. Front. Biosci. 14:3111–27
    [Google Scholar]
39. 39.  Landete JM 2017. A review of food-grade vectors in lactic acid bacteria: from the laboratory to their application. Crit. Rev. Biotechnol. 37:296–308
    [Google Scholar]
40. 40.  Missich R, Sgorbati B, LeBlanc DJ 1994. Transformation of Bifidobacteriumlongum with pRM2, a constructed Escherichia coli–B.longum shuttle vector. Plasmid 32:208–11
    [Google Scholar]
41. 41.  Matsumura H, Takeuchi A, Kano Y 1997. Construction of Escherichia coli–Bifidobacteriumlongum shuttle vector transforming B.longum 105-A and 108-A. Biosci. Biotechnol. Biochem. 61:1211–12
    [Google Scholar]
42. 42.  Álvarez-Martín P, Flórez AB, Margolles A, Del Solar G, Mayo B 2008. Improved cloning vectors for bifidobacteria, based on the Bifidobacteriumcatenulatum pBC1 replicon. Appl. Environ. Microbiol. 74:4656–65
    [Google Scholar]
43. 43.  Garrigues-Jeanjean N, Wittmer A, Ouriet M, Duval-Iflah Y 1999. Transfer of the shuttle vector pRRI207 between Escherichia coli and Bacteroides spp. in vitro and in vivo in the digestive tract of axenic mice and in gnotoxenic mice inoculated with a human microflora. FEMS Microbiol. Ecol. 29:33–43
    [Google Scholar]
44. 44.  Tauer C, Heinl S, Egger E, Heiss S, Grabherr R 2014. Tuning constitutive recombinant gene expression in Lactobacillusplantarum. . Microb. Cell Fact. 13:150
    [Google Scholar]
45. 45.  Mimee M, Tucker AC, Voigt CA, Lu TK 2015. Programming a human commensal bacterium, Bacteroidesthetaiotaomicron, to sense and respond to stimuli in the murine gut microbiota. Cell Syst 1:62–71
    [Google Scholar]
46. 46.  Mierau I, Kleerebezem M 2005. 10 years of the nisin-controlled gene expression system (NICE) in Lactococcuslactis. . Appl. Microbiol. Biotechnol. 68:705–17
    [Google Scholar]
47. 47.  Kaswurm V, Nguyen T-T, Maischberger T, Kulbe KD, Michlmayr H 2013. Evaluation of the food grade expression systems NICE and pSIP for the production of 2,5-diketo-d-gluconic acid reductase from Corynebacteriumglutamicum. . AMB Express 3:7
    [Google Scholar]
48. 48.  Mathiesen G, Sørvig E, Blatny J, Naterstad K, Axelsson L, Eijsink VGH 2004. High-level gene expression in Lactobacillusplantarum using a pheromone-regulated bacteriocin promoter. Lett. Appl. Microbiol. 39:137–43
    [Google Scholar]
49. 49.  Heiss S, Hörmann A, Tauer C, Sonnleitner M, Egger E et al. 2016. Evaluation of novel inducible promoter/repressor systems for recombinant protein expression in Lactobacillusplantarum. . Microb. Cell Fact. 15:50
    [Google Scholar]
50. 50.  Horn N, Carvalho AL, Overweg K, Wegmann U, Carding SR, Stentz R 2016. A novel tightly regulated gene expression system for the human intestinal symbiont Bacteroidesthetaiotaomicron. . Front. Microbiol. 7:1080
    [Google Scholar]
51. 51.  Bosma EF, Forster J, Nielsen AT 2017. Lactobacilli and pediococci as versatile cell factories—evaluation of strain properties and genetic tools. Biotechnol. Adv. 35:419–42
    [Google Scholar]
52. 52.  Kushwaha M, Salis HM 2015. A portable expression resource for engineering cross-species genetic circuits and pathways. Nat. Commun. 6:7832
    [Google Scholar]
53. 53.  Allain T, Mansour NM, Bahr MMA, Martin R, Florent I et al. 2016. A new lactobacilli in vivo expression system for the production and delivery of heterologous proteins at mucosal surfaces. FEMS Microbiol. Lett. 363:fnw117
    [Google Scholar]
54. 54.  Schneewind O, Missiakas D 2014. Sec-secretion and sortase-mediated anchoring of proteins in gram-positive bacteria. Biochim. Biophys. Acta 1843:1687–97
    [Google Scholar]
55. 55.  Dieye Y, Usai S, Clier F, Gruss A, Piard J 2001. Design of a protein-targeting system for lactic acid bacteria. J. Bacteriol. 183:4157–66
    [Google Scholar]
56. 56.  Le Loir Y, Nouaille S, Commissaire J, Brétigny L, Langella P 2001. Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcuslactis. . Appl. Environ. Microbiol. 67:4119–27
    [Google Scholar]
57. 57.  Mathiesen G, Sveen A, Piard J-C, Axelsson L, Eijsink VGH 2008. Heterologous protein secretion by Lactobacillusplantarum using homologous signal peptides. J. Appl. Microbiol. 105:215–26
    [Google Scholar]
58. 58.  Zadravec P, Štrukelj B, Berlec A 2015. Heterologous surface display on lactic acid bacteria: non-GMO alternative?. Bioengineered 6:179–83
    [Google Scholar]
59. 59.  Michon C, Langella P, Eijsink VGH, Mathiesen G, Chatel JM 2016. Display of recombinant proteins at the surface of lactic acid bacteria: strategies and applications. Microb. Cell Fact. 15:70
    [Google Scholar]
60. 60.  Dalia AB, McDonough E, Camilli A 2014. Multiplex genome editing by natural transformation. PNAS 111:8937–42
    [Google Scholar]
61. 61.  van Pijkeren JP, Britton RA 2012. High efficiency recombineering in lactic acid bacteria. Nucleic Acids Res 40:e76
    [Google Scholar]
62. 62.  Lambert JM, Bongers RS, Kleerebezem M 2007. Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillusplantarum. . Appl. Environ. Microbiol. 73:1126–35
    [Google Scholar]
63. 63.  Jiang W, Bikard D, Cox D, Zhang F, Marraffin LA 2013. CRISPR-assisted editing of bacterial genomes. Nat Biotechnol 31:233–39
    [Google Scholar]
64. 64.  van Pijkeren JP, Britton RA 2014. Precision genome engineering in lactic acid bacteria. Microb. Cell Fact. 13:Suppl. 1S10
    [Google Scholar]
65. 65.  Oh JH, van Pijkeren JP 2014. CRISPR-Cas9-assisted recombineering in Lactobacillusreuteri. . Nucleic Acids Res 42:e131
    [Google Scholar]
66. 66.  Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS 2013. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8:2180–96
    [Google Scholar]
67. 67.  Danino T, Prindle A, Kwong GA, Skalak M, Li H et al. 2015. Programmable probiotics for detection of cancer in urine. Sci. Transl. Med. 7:289ra84
    [Google Scholar]
68. 68.  Ou B, Yang Y, Tham WL, Chen L, Guo J 2016. Genetic engineering of probiotic Escherichia coli Nissle 1917 for clinical application. Appl. Microbiol. Biotechnol. 100:8693–99
    [Google Scholar]
69. 69.  Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA 2007. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int. J. Med. Microbiol. 297:151–62
    [Google Scholar]
70. 70.  Gasteiger G, D'Osualdo A, Schubert DA, Weber A, Bruscia EM, Hartl D 2017. Cellular innate immunity: an old game with new players. J. Innate Immun. 9:111–25
    [Google Scholar]
71. 71.  Wyszyńska A, Kobierecka P, Bardowski J, Jagusztyn-Krynicka EK 2015. Lactic acid bacteria—20 years exploring their potential as live vectors for mucosal vaccination. Appl. Microbiol. Biotechnol. 99:2967–77
    [Google Scholar]
72. 72.  Tarahomjoo S 2012. Development of vaccine delivery vehicles based on lactic acid bacteria. Mol. Biotechnol. 51:183–99
    [Google Scholar]
73. 73.  Wells JM, Mercenier A 2008. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat. Rev. Microbiol. 6:349–62
    [Google Scholar]
74. 74.  Cronin M, Morrissey D, Rajendran S, El Mashad SM, van Sinderen D et al. 2010. Orally administered bifidobacteria as vehicles for delivery of agents to systemic tumors. Mol. Ther. 18:1397–407
    [Google Scholar]
75. 75.  Hanson ML, Hixon JA, Li W, Felber BK, Anver MR et al. 2014. Oral delivery of IL-27 recombinant bacteria attenuates immune colitis in mice. Gastroenterology 146:210–21
    [Google Scholar]
76. 76.  Meister G, Tuschi T 2004. Mechanisms of gene silencing by double-stranded RNA. Nature 431:343–49
    [Google Scholar]
77. 77.  Spisni E, Valerii MC, De Fazio L, Cavazza E, Borsetti F et al. 2015. Cyclooxygenase-2 silencing for the treatment of colitis: a combined in vivo strategy based on RNA interference and engineered Escherichia coli. . Mol. Ther. 23:278–89
    [Google Scholar]
78. 78.  Christophe M, Kuczkowska K, Langella P, Eijsink VGH, Mathiesen G, Chatel J-M 2015. Surface display of an anti-DEC-205 single chain Fv fragment in Lactobacillusplantarum increases internalization and plasmid transfer to dendritic cells in vitro and in vivo. Microb. Cell Fact. 14:95
    [Google Scholar]
79. 79.  Takei S, Omoto C, Kitagawa K, Morishita N, Katayama T et al. 2014. Oral administration of genetically modified Bifidobacterium displaying HCV-NS3 multi-epitope fusion protein could induce an HCV-NS3-specific systemic immune response in mice. Vaccine 32:3066–74
    [Google Scholar]
80. 80.  Frykberg RG, Banks J 2015. Challenges in the treatment of chronic wounds. Adv. Wound Care 4:560–82
    [Google Scholar]
81. 81.  Kim J, Amar S 2006. Periodontal disease and systemic conditions: a bidirectional relationship. Odontology 94:10–21
    [Google Scholar]
82. 82.  Bai A-P, Ouyang Q 2006. Probiotics and inflammatory bowel diseases. Postgrad. Med. J. 82:376–82
    [Google Scholar]
83. 83.  Ratjen FA 2009. Cystic fibrosis: pathogenesis and future treatment strategies. Respir. Care 54:595–605
    [Google Scholar]
84. 84.  Brogden KA 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 3:238–50
    [Google Scholar]
85. 85.  Geldart K, Borrero J, Kaznessis YN 2015. Chloride-inducible expression vector for delivery of antimicrobial peptides targeting antibiotic-resistant Enterococcusfaecium. . Appl. Environ. Microbiol. 81:3889–97
    [Google Scholar]
86. 86.  Brurberg MB, Nes IF, Eijsink VG 1997. Pheromone-induced production of antimicrobial peptides in Lactobacillus. . Mol. Microbiol. 26:347–60
    [Google Scholar]
87. 87.  Jones SE, Versalovic J 2009. Probiotic Lactobacillusreuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 9:35
    [Google Scholar]
88. 88.  Roelofs KG, Coyne MJ, Gentyala RR, Chatzidaki-Livanis M, Comstock LE 2016. Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo. mBio 7:e0155
    [Google Scholar]
89. 89.  Spinler JK, Taweechotipatr M, Rognerud CL, Ou CN, Tumwasorn S, Versalovic J 2008. Human-derived probiotic Lactobacillusreuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14:166–71
    [Google Scholar]
90. 90.  van Pijkeren J-P, Neoh KM, Sirias D, Findley AS, Britton RA 2012. Exploring optimization parameters to increase ssDNA recombineering in Lactococcuslactis and Lactobacillusreuteri. . Bioengineered 3:209–17
    [Google Scholar]
91. 91.  Borrero J, Chen Y, Dunny GM, Kaznessis YN 2015. Modified lactic acid bacteria detect and inhibit multiresistant enterococci. ACS Synth. Biol. 4:299–306
    [Google Scholar]
92. 92.  Hwang IY, Tan MH, Koh E, Ho CL, Poh CL, Chang MW 2014. Reprogramming microbes to be pathogen-seeking killers. ACS Synth. Biol. 3:228–37
    [Google Scholar]
93. 93.  Hwang IY, Koh E, Wong A, March JC, Bentley WE et al. 2017. Engineered probiotic Escherichia coli can eliminate and prevent Pseudomonasaeruginosa gut infection in animal models. Nat. Commun. 8:15028
    [Google Scholar]
94. 94.  Joyce SA, MacSharry J, Casey PG, Kinsella M, Murphy EF et al. 2014. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. PNAS 111:7421–26
    [Google Scholar]
95. 95.  Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA et al. 2009. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. PNAS 106:3698–703
    [Google Scholar]
96. 96.  Sanz Y, Olivares M, Moya-Pérez Á, Agostoni C 2015. Understanding the role of gut microbiome in metabolic disease risk. Pediatr. Res. 77:236–44
    [Google Scholar]
97. 97.  Krishnan S, Alden N, Lee K 2015. Pathways and functions of gut microbiota metabolism impacting host physiology. Curr. Opin. Biotechnol. 36:137–45
    [Google Scholar]
98. 98.  Le Barz M, Anhê FF, Varin TV, Desjardins Y, Levy E et al. 2015. Probiotics as complementary treatment for metabolic disorders. Diabetes Metab. J. 39:291–303
    [Google Scholar]
99. 99.  Rhimi M, Bermudez-Humaran LG, Huang Y, Boudebbouze S, Gaci N et al. 2015. The secreted l-arabinose isomerase displays anti-hyperglycemic effects in mice. Microb. Cell Fact. 14:204
    [Google Scholar]
100. 100.  Duan FF, Liu JH, March JC 2015. Engineered commensal bacteria reprogram intestinal cells into glucose-responsive insulin-secreting cells for the treatment of diabetes. Diabetes 64:1794–803
     [Google Scholar]
101. 101.  Mauricio MD, Serna E, Fernández-Murga ML, Portero J, Aldasoro M et al. 2017. Bifidobacteriumpseudocatenulatum CECT 7765 supplementation restores altered vascular function in an experimental model of obese mice. Int. J. Med. Sci. 14:444–51
     [Google Scholar]
102. 102.  Ojetti V, Gigante G, Gabrielli M, Ainora ME, Mannocci A et al. 2010. The effect of oral supplementation with Lactobacillusreuteri or tilactase in lactose intolerant patients: randomized trial. Eur. Rev. Med. Pharmacol. Sci. 14:163–70
     [Google Scholar]
103. 103.  Durrer KE, Allen MS, Hunt von Herbing I 2017. Genetically engineered probiotic for the treatment of phenylketonuria (PKU); assessment of a novel treatment in vitro and in the PAH^enu2 mouse model of PKU. PLOS ONE 12:e0176286
     [Google Scholar]
104. 104.  Sasikumar P, Gomathi S, Anbazhagan K, Abhishek A, Paul E et al. 2014. Recombinant Lactobacillusplantarum expressing and secreting heterologous oxalate decarboxylase prevents renal calcium oxalate stone deposition in experimental rats. J. Biomed. Sci. 21:86
     [Google Scholar]
105. 105.  Daeffler KN, Galley JD, Sheth RU, Ortiz‐Velez LC, Bibb CO et al. 2017. Engineering bacterial thiosulfate and tetrathionate sensors for detecting gut inflammation. Mol. Syst. Biol. 13:923
     [Google Scholar]
106. 106.  Benbouziane B, Ribelles P, Aubry C, Martin R, Kharrat P et al. 2013. Development of a stress-inducible controlled expression (SICE) system in Lactococcuslactis for the production and delivery of therapeutic molecules at mucosal surfaces. J. Biotechnol. 168:120–29
     [Google Scholar]
107. 107.  Landete JM, Medina M, Arqués JL 2016. Fluorescent reporter systems for tracking probiotic lactic acid bacteria and bifidobacteria. World J. Microbiol. Biotechnol. 32:119
     [Google Scholar]
108. 108.  Karimi S, Ahl D, Vågesjö E, Holm L, Phillipson M et al. 2016. In vivo and in vitro detection of luminescent and fluorescent Lactobacillusreuteri and application of red fluorescent mCherry for assessing plasmid persistence. PLOS ONE 11:e0151969
     [Google Scholar]
109. 109.  Berlec A, Završnik J, Butinar M, Turk B, Štrukelj B 2015. In vivo imaging of Lactococcuslactis, Lactobacillusplantarum and Escherichia coli expressing infrared fluorescent protein in mice. Microb. Cell Fact. 14:181
     [Google Scholar]
110. 110.  Farzadfard F, Lu TK 2014. Synthetic biology. Genomically encoded analog memory with precise in vivo DNA writing in living cell populations. Science 346:1256272
     [Google Scholar]
111. 111.  Bonnet J, Subsoontorn P, Endy D 2012. Rewritable digital data storage in live cells via engineered control of recombination directionality. PNAS 109:8884–89
     [Google Scholar]
112. 112.  Pandey KR, Naik SR, Vakil BV 2015. Probiotics, prebiotics and synbiotics—a review. J. Food Sci. Technol. 52:7577–87
     [Google Scholar]
113. 113.  Beisel CL, Gomaa AA, Barrangou R 2014. A CRISPR design for next-generation antimicrobials. Genome Biol 15:516
     [Google Scholar]
114. 114.  Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW et al. 2014. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32:1146–50
     [Google Scholar]
115. 115.  Gomaa AA, Klumpe HE, Luo ML, Selle K, Barrangou R, Beisel CL 2014. Programmable removal of bacterial strains by use of genome-targeting CRISPR-Cas systems. mBio 5:e00928
     [Google Scholar]
116. 116.  Citorik RJ, Mimee M, Lu TK 2014. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32:1141–45
     [Google Scholar]
117. 117.  Park JY, Moon BY, Park JW, Thornton JA, Park YH, Seo KS 2017. Genetic engineering of a temperate phage-based delivery system for CRISPR/Cas9 antimicrobials against Staphylococcusaureus. . Sci. Rep. 7:1–13
     [Google Scholar]
118. 118.  Goren M, Yosef I, Qimron U 2017. Sensitizing pathogens to antibiotics using the CRISPR-Cas system. Drug Resist. Update 30:1–6
     [Google Scholar]
119. 119.  Brito IL, Yilmaz S, Huang K, Xu L, Jupiter SD et al. 2016. Mobile genes in the human microbiome are structured from global to individual scales. Nature 535:435–39
     [Google Scholar]
120. 120.  Sheth RU, Cabral V, Chen SP, Wang HH 2016. Manipulating bacterial communities by in situ microbiome engineering. Trends Genet 32:189–200
     [Google Scholar]
121. 121.  Tannock GW 1987. Conjugal transfer of plasmid pAMβ1 in Lactobacillusreuteri and between lactobacilli and Enterococcusfaecalis. . Appl. Environ. Microbiol. 53:2693–95
     [Google Scholar]
122. 122.  McConnell MA, Mercer AA, Tannock GW 1991. Transfer of plasmid pAMβl between members of the normal microflora inhabiting the murine digestive tract and modification of the plasmid in a Lactobacillusreuteri host. Microb. Ecol. Health Dis. 4:343–55
     [Google Scholar]
123. 123.  Netherwood T, Bowden R, Harrison P, O'Donnell G, Parker DS, Gilbert HJ 1999. Gene transfer in the gastrointestinal tract. Appl. Environ. Microbiol. 65:5139–41
     [Google Scholar]
124. 124.  Shintani M, Sanchez ZK, Kimbara K 2015. Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front. Microbiol. 6:242
     [Google Scholar]
125. 125.  Chen Y, Lin Y, Davis KM, Wang Q, Rnjak-Kovacina J et al. 2015. Robust bioengineered 3D functional human intestinal epithelium. Sci. Rep. 5:13708
     [Google Scholar]
126. 126.  Arnold JW, Roach J, Azcarate-Peril MA 2016. Emerging technologies for gut microbiome research. Trends Microbiol 24:887–901
     [Google Scholar]
127. 127.  Yaung SJ, Church GM, Wang HH 2014. Recent progress in engineering human-associated microbiomes. Methods Mol. Biol. 1151:3–25
     [Google Scholar]
128. 128.  Hazebrouck S, Oozeer R, Adel-Patient K, Langella P, Rabot S et al. 2006. Constitutive delivery of bovine β-lactoglobulin to the digestive tracts of gnotobiotic mice by engineered Lactobacilluscasei. . Appl. Environ. Microbiol. 72:7460–67
     [Google Scholar]
129. 129.  Rooks MG, Garrett WS 2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16:341–52
     [Google Scholar]
130. 130.  Fiebiger U, Bereswill S, Heimesaat MM 2016. Dissecting the interplay between intestinal microbiota and host immunity in health and disease: lessons learned from germfree and gnotobiotic animal models. Eur. J. Microbiol. Immunol. 6:253–71
     [Google Scholar]
131. 131.  MacKenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ et al. 2010. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillusreuteri. . Microbiology 156:3368–78
     [Google Scholar]
132. 132.  Jourová L, Anzenbacher P, Lišková B, Matušková Z, Hermanová P et al. 2017. Colonization by non-pathogenic bacteria alters mRNA expression of cytochromes P450 in originally germ-free mice. Folia Microbiol 62:463–69
     [Google Scholar]
133. 133.  Ito R, Takahashi T, Katano I, Ito M 2012. Current advances in humanized mouse models. Cell. Mol. Immunol. 9:208–14
     [Google Scholar]
134. 134.  Nguyen TLA, Vieira-Silva S, Liston A, Raes J 2015. How informative is the mouse for human gut microbiota research?. Dis. Model. Mech. 8:1–16
     [Google Scholar]
135. 135.  Arrieta M, Walter J, Finlay BB 2016. Forum human microbiota–associated mice: a model with challenges. Cell Host Microbe 19:575–78
     [Google Scholar]
136. 136.  Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermeire A et al. 2003. Biological containment of genetically modified Lactococcuslactis for intestinal delivery of human interleukin 10. Nat. Biotechnol. 21:785–89
     [Google Scholar]
137. 137.  Mandell DJ, Lajoie MJ, Mee MT, Takeuchi R, Kuznetsov G et al. 2015. Biocontainment of genetically modified organisms by synthetic protein design. Nature 518:55–60
     [Google Scholar]
138. 138.  Chan CTY, Lee JW, Cameron DE, Bashor CJ, Collins JJ 2015. “Deadman” and “Passcode” microbial kill switches for bacterial containment. Nat. Chem. Biol. 12:82–86
     [Google Scholar]
139. 139.  Penders J, Thijs C, Vink C, Stelma FF, Snijders B et al. 2006. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–21
     [Google Scholar]
140. 140.  O'Connor EM 2013. The role of gut microbiota in nutritional status. Curr. Opin. Clin. Nutr. Metab. Care 16:509–16
     [Google Scholar]
141. 141.  Kali A 2015. Human microbiome engineering: the future and beyond. J. Clin. Diagn. Res. 9:1–4
     [Google Scholar]
142. 142.  Krumbeck JA, Marsteller NL, Frese SA, Peterson DA, Ramer-Tait AE et al. 2016. Characterization of the ecological role of genes mediating acid resistance in Lactobacillusreuteri during colonization of the gastrointestinal tract. Environ. Microbiol. 18:2172–84
     [Google Scholar]
143. 143.  Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK 2013. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501:426–29
     [Google Scholar]
144. 144.  Etzold S, Kober OI, Mackenzie DA, Tailford LE, Gunning AP et al. 2014. Structural basis for adaptation of lactobacilli to gastrointestinal mucus. Environ. Microbiol. 16:888–903
     [Google Scholar]
145. 145.  Coyne MJ, Chatzidaki-Livanis M, Paoletti LC, Comstock LE 2008. Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroidesfragilis. . PNAS 105:13099–104
     [Google Scholar]
146. 146.  Etzold S, Mackenzie DA, Jeffers F, Walshaw J, Roos S et al. 2014. Structural and molecular insights into novel surface-exposed mucus adhesins from Lactobacillusreuteri human strains. Mol. Microbiol. 92:543–56
     [Google Scholar]
147. 147.  Angelakis E, Armougom F, Carrière F, Bachar D, Laugier R et al. 2015. A metagenomic investigation of the duodenal microbiota reveals links with obesity. PLOS ONE 10:e0137784
     [Google Scholar]
148. 148.  Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA et al. 2006. Molecular analysis of the bacterial microbiota in the human stomach. PNAS 103:732–37
     [Google Scholar]
149. 149.  Shin NR, Whon TW, Bae JW 2015. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503
     [Google Scholar]
150. 150.  Sankar SA, Lagier J-C, Pontarotti P, Raoult D, Fournier P-E 2015. The human gut microbiome, a taxonomic conundrum. Syst. Appl. Microbiol. 38:276–86
     [Google Scholar]