Safety of novel microbes for human consumption: Practical examples of assessment in the European Union

Frontiers in Microbiology

Volumn 8, Issue SEP, 2017, Pages

  Brodmann, Theodor ^a   Endo, Akihito ^b   Gueimonde, Miguel ^c   Vinderola, Gabriel ^d   Kneifel, Wolfgang ^a   de Vos, Willem M ^e,f   Salminen, Seppo ^g   Gómez Gallego, Carlos ^g  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^c DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^d UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f UNIVERSITY OF HELSINKI   (Finland)

^g UNIVERSITY OF TURKU   (Finland)

Author keywords

Akkermansia muciniphila; Bacteroides xylanisolvens; Fructophilic lactic acid bacteria, Faecalibacterium prausnitzii; Novel microbes; Safety

Indexed keywords

BIOLOGICAL PRODUCT; FARNOQUINONE; PROBIOTIC AGENT;

AKKERMANSIA MUCINIPHILA; ANTIBIOTIC RESISTANCE; BACILLUS SUBTILIS NATTO; BACTERIAL STRAIN; BACTEROIDES XYLANISOLVENS; CLOSTRIDIUM BUTYRICUM; COLORECTAL CANCER; DRUG EFFICACY; DRUG SAFETY; EUROPEAN UNION; FAECALIBACTERIUM PRAUSNITZII; FERMENTATION; FOOD CONTROL; FOOD INDUSTRY; FOOD SAFETY; FRUCTOPHILIC LACTIC ACID BACTERIA; HUMAN; IMMUNOMODULATION; INTESTINE FLORA; LACTIC ACID BACTERIUM; LAW; LEUCONOSTOC MESENTEROIDES; METAGENOMICS; NEW SPECIES; NONHUMAN; OBESITY; PARABIOSIS; PATHOGENICITY; QUALIFIED PRESUMPTION OF SAFETY; REVIEW; RISK ASSESSMENT; TAXONOMIC RANK;

EID: 85029688885     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01725     Document Type: Review

References (110)

1. Alcantara-Hernandez, R. J., Rodriguez-Alvarez, J. A., Valenzuela-Encinas, C., Gutierrez-Miceli, F. A., Castanon-Gonzalez, H., Marsch, R., et al. (2010). The bacterial community in 'taberna' a traditional beverage of Southern Mexico. Lett. Appl. Microbiol. 51, 558-563. doi: 10.1111/j.1472-765X.2010.02934.x
2. Asama, T., Arima, T. H., Gomi, T., Keishi, T., Tani, H., Kimura, Y., et al. (2015). Lactobacillus kunkeei YB38 from honeybee products enhances IgA production in healthy adults. J. Appl. Microbiol. 119, 818-826. doi: 10.1111/jam.12889
3. Asama, T., Kimura, Y., Kono, T., Tatefuji, T., Hashimoto, K., and Benno, Y. (2016). Effects of heat-killed Lactobacillus kunkeei YB38 on human intestinal environment and bowel movement: a pilot study. Benef. Microbes 7, 337-344. doi: 10.3920/BM2015.0132
4. Aureli, P., Capurso, L., Castellazzi, A. M., Clerici, M., Giovannini, M., Morelli, L., et al. (2011). Probiotics and health: an evidence-based review. Pharmacol. Res. 63, 366-376. doi: 10.1016/j.phrs.2011.02.006
5. BAuA (2011). Begründungspapier zur Einstufung von Bacteroides xylanisolvens in Risikogruppe 1 nach BioStoffV. Bundesanstalt für Arbeitsschutz und Arbeitsmedizin, BAuA
6. Belzer, C., and De Vos, W. M. (2012). Microbes insidefrom diversity to function: the case of Akkermansia. ISME J. 6, 1449-1458. doi: 10.1038/ismej.2012.6
7. Borresen, E. C., Henderson, A. J., Kumar, A., Weir, T. L., and Ryan, E. P. (2012). Fermented foods: patented approaches and formulations for nutritional supplementation and health promotion. Recent Pat. Food Nutr. Agric. 4, 134-140. doi: 10.2174/2212798411204020134
8. Breyner, N. M., Michon, C., de Sousa, C. S., Vilas Boas, P. B., Chain, F., Azevedo, V., et al. (2017). Microbial Anti-Inflammatory Molecule (MAM) from Faecalibacterium prausnitzii shows a protective effect on DNBS and DSS-induced colitis model in mice through inhibition of NF-kappaB pathway. Front. Microbiol. 8:114. doi: 10.3389/fmicb.2017.00114
9. Cammarota, G., Ianiro, G., Bibbo, S., and Gasbarrini, A. (2014). Gut microbiota modulation: probiotics, antibiotics or fecal microbiota transplantation? Intern. Emerg. Med. 9, 365-373. doi: 10.1007/s11739-014-1069-4
10. Cani, P. D., and Everard, A. (2014). Akkermansia muciniphila: a novel target controlling obesity, type 2 diabetes and inflammation? Med. Sci. 30, 125-127. doi: 10.1051/medsci/20143002003
11. Chassard, C., Delmas, E., Lawson, P. A., and Bernalier-Donadille, A. (2008). Bacteroides xylanisolvens sp. nov., a xylan-degrading bacterium isolated from human faeces. Int. J. Syst. Evol. Microbiol. 58(Pt 4), 1008-1013. doi: 10.1099/ijs.0.65504-0
12. Cibik, R., Lepage, E., and Talliez, P. (2000). Molecular diversity of leuconostoc mesenteroides and leuconostoc citreum isolated from traditional french cheeses as revealed by RAPD fingerprinting, 16S rDNA sequencing and 16S rDNA fragment amplification. Syst. Appl. Microbiol. 23, 267-278. doi: 10.1016/S0723-2020(00)80014-4
13. Collado, M. C., Laitinen, K., Salminen, S., and Isolauri, E. (2012). Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr. Res. 72, 77-85. doi: 10.1038/pr.2012.42
14. Costello, E. K., Gordon, J. I., Secor, S. M., and Knight, R. (2010). Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J. 4, 1375-1385. doi: 10.1038/ismej.2010.71
15. D'Angelo, L., Cicotello, J., Zago, M., Guglielmotti, D., Quiberoni, A., and Suarez, V. (2017). Leuconostoc strains isolated from dairy products: response against food stress conditions. Food Microbiol. 66, 28-39. doi: 10.1016/j.fm.2017.04.001
16. de Almada, C. N., Almada, C. N., Martinez, R. C. R., and Sant'Ana, A. S. (2016). Paraprobiotics: evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends Food Sci. Technol. 98, 56-114. doi: 10.1016/j.tifs.2016.09.011
17. de Paula, A. T., Jeronymo-Ceneviva, A. B., Todorov, S. D., and Penna, A. L. B. (2015). The two faces of Leuconostoc mesenteroides in food systems. Food Rev. Int. 31, 147-171. doi: 10.1080/87559129.2014.981825
18. Derrien, M., Collado, M. C., Ben-Amor, K., Salminen, S., and De Vos, W. M. (2008). The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl. Environ. Microbiol. 74, 1646-1648. doi: 10.1128/AEM.01226-07
19. Derrien, M., van Passel, M. W. J., van de Bovenkamp, J. H. B., Schipper, R. G., de Vos, W. M., and Dekker, J. (2010). Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1, 254-268. doi: 10.4161/gmic.1.4.12778
20. Derrien, M., Vaughan, E. E., Plugge, C. M., and de Vos, W. M. (2004). Akkermansia municiphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54, 1469-1476. doi: 10.1099/ijs.0.02873-0
21. Donohue, D., and Salminen, S. (1996). Safety of probiotic bacteria. Asia Pac. J. Clin. Nutr. 5, 25-28
22. Dostal, A., Lacroix, C., Bircher, L., Pham, V. T., Follador, R., Zimmermann, M. B., et al. (2015). Iron modulates butyrate production by a child gut microbiota in vitro. MBio 6, e01453-e01415. doi: 10.1128/mBio.01453-15
23. EFSA (2007). Introduction of a Qualified Presumption of Safety (QPS) Approach for Assessment of Selected Microorganisms Referred to EFSA-Opinion of the Scientific Committee
24. EFSA Panel on Biological Hazards (2014). Statement on the update of the list of QPS-recommended biological agents intentionally added to food or feed as notified to EFSA 1: Suitability of taxonomic units notified to EFSA until October 2014. EFSA J. 12, 1-42. doi: 10.2903/j.efsa.2014.3938
25. EFSA Panel on Biological Hazards (2010). Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2010 update). EFSA J. 8, 1-56. doi: 10.2903/j.efsa.2010.1944
26. EFSA Panel on Dietetic Products (2016). Guidance on the preparation and presentation of an application for authorisation of a novel food in the context of Regulation (EU) 2015/2283. EFSA J. 14, 1-24. doi: 10.2903/j.efsa.2016.4594
27. EFSA Panel on Dietetic Products, Nutrition and Allergies. (2014). Scientific Opinion on the evaluation of allergenic foods and food ingredients for labelling purposes. EFSA J. 12, 1-286. doi: 10.2903/j.efsa.2014.3894
28. EFSA Panel on Dietetic Products, Nutrition and Allergies. (2015). Scientific Opinion on the safety of 'heat-treated milk products fermented with Bacteroides xylanisolvens DSM 23964' as a novel food. EFSA J. 13, 1-18. doi: 10.2903/j.efsa.2015.3956
29. Endo, A. (2012). Fructophilic lactic acid bacteria inhabit fructose-rich niches in nature. Microb. Ecol. Health Dis. 23, 6-12 doi: 10.3402/mehd.v23i0.18563
30. Endo, A., Futagawa-Endo, Y., and Dicks, L. M. (2009). Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst. Appl. Microbiol. 32, 593-600. doi: 10.1016/j.syapm.2009.08.002
31. Endo, A., Futagawa-Endo, Y., Sakamoto, M., Kitahara, M., and Dicks, L. M. T. (2010). Lactobacillus florum sp. nov., a fructophilic species isolated from flowers. Int. J. Syst. Evol. Microbiol. 60, 2478-2482. doi: 10.1099/ijs.0.019067-0
32. Endo, A., Irisawa, T., Futagawa-Endo, Y., Takano, K., du Toit, M., Okada, S., et al. (2012). Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium. Int. J. Syst. Evol. Microbiol. 62, 500-504. doi: 10.1099/ijs.0.031054-0
33. Endo, A., and Okada, S. (2008). Reclassification of the genus Leuconostoc and proposals of Fructobacillus fructosus gen. nov., comb. nov., Fructobacillus durionis comb. nov., Fructobacillus ficulneus comb. nov. and Fructobacillus pseudoficulneus comb. nov. Int. J. Syst. Evol. Microbiol. 58(Pt 9), 2195-2205. doi: 10.1099/ijs.0.65609-0
34. Endo, A., and Salminen, S. (2013). Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Syst. Appl. Microbiol. 36, 444-448. doi: 10.1016/j.syapm.2013.06.002
35. Endo, A., Tanizawa, Y., Tanaka, N., Maeno, S., Kumar, H., Shiwa, Y., et al. (2015). Comparative genomics of Fructobacillus spp. and Leuconostoc spp. reveals niche-specific evolution of Fructobacillus spp. BMC Genomics 16:1117. doi: 10.1186/s12864-015-2339-x
36. European Commission (1997a). 97/618/EC. Commission Recommendation of 29 July 1997 Concerning the Scientific Aspects and the Presentation of Information Necessary to Support Applications for the Placing on the Market of Novel Foods and Novel Food Ingredients and the Preparation of Initial Assessment Reports Under Regulation (EC) No 258/97 of the European Parliament and of the Council
37. European Commission (1997b). R. 285/97/ERegulation, C. (EC) No. 258/97 of the European Parliament and of the Council of 27 January 1997 Concerning Novel Foods and Novel Food Ingredients
38. European Commission (2001). E. Commission: 2001/122/EC. Commission Decision of 30 January 2001 on Authorising the Placing on the Market of a Dextran Preparation Produced by Leuconostoc mesenteroides as a Novel Food Ingredient in Bakery Products under Regulation (EC) No 258/97 of the European Parliament and of the Council (Notified Under Document Number C(2001) 174)
39. European Commission (2009). E. Commission: 2009/345/EC. Commission Decision of 22 April 2009 Authorising the Placing on the Market of Vitamin K2 (Menaquinone) from Bacillus subtilis natto as a Novel Food Ingredient under Regulation (EC) No 258/97 of the European Parliament and of the Council (Notified Under Document Number C(2009) 2935)
40. European Commission (2014). E. Commission: 2014/907/EU. Commission Implementing Decision of 11 December 2014 Authorising the Placing on the Market of Clostridium butyricum (CBM 588) as a Novel Food Ingredient under Regulation (EC) No 258/97 of the European Parliament and of the Council (Notified Under Document C(2014) 9345)
41. European Commission (2015). R. E. 2015/2283. Regulation (EU) 2015/2283 of the European Parliament and of the Council of 25 November 2015 on Novel Foods, Amending Regulation (EU) No 1169/2011 of the European Parliament and of the Council and Repealing Regulation (EC) No 258/97 of the European Parliament and of the Council and Commission Regulation (EC) No, 1852/2001
42. Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J. P., Druart, C., Bindels, L. B., et al. (2013). Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 110, 9066-9071. doi: 10.1073/pnas.1219451110
43. Foditsch, C., Santos, T. M., Teixeira, A. G., Pereira, R. V., Dias, J. M., Gaeta, N., et al. (2014). Isolation and characterization of Faecalibacterium prausnitzii from calves and piglets. PLoS ONE 9:e116465. doi: 10.1371/journal.pone.0116465
44. Gomez-Gallego, C., Pohl, S., Salminen, S., De Vos, W. M., and Kneifel, W. (2016). Akkermansia muciniphila: a novel functional microbe with probiotic properties. Benef. Microbes 7, 571-584. doi: 10.3920/BM2016.0009
45. Gómez-Gallego, C., and Salminen, S. (2016). Novel probiotics and prebiotics: how can they help in human gut microbiota dysbiosis? Appl. Food Biotechnol. 3, 72-81. doi: 10.22037/afb.v3i2.11276
46. Gregory, K. E., LaPlante, R. D., Shan, G., Kumar, D. V., and Gregas, M. (2015). Mode of birth influences preterm infant intestinal colonization with bacteroides over the early neonatal period. Adv. Neonatal Care 15, 386-393. doi: 10.1097/ANC.0000000000000237
47. H. C. P. Directorate-General (2003). Working Document on a Generic Approach to the Safety Assessment of Micro-Organisms Used in Feed/Food and Feed/Food Production. Available online at: https://ec.europa.eu/food/sites/food/files/safety/docs/sci-com_scf_out178_en.pdf
48. Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., et al. (2014). The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506-514. doi: 10.1038/nrgastro.2014.66
49. Hooper, L. V., Midtvedt, T., and Gordon, J. I. (2002). How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22, 283-307. doi: 10.1146/annurev.nutr.22.011602.092259
50. Hosseini, E., Grootaert, C., Verstraete, W., and Van de Wiele, T. (2011). Propionate as a health-promoting microbial metabolite in the human gut. Nutr. Rev. 69, 245-258. doi: 10.1111/j.1753-4887.2011.00388.x
51. Isa, K., Oka, K., Beauchamp, N., Sato, M., Wada, K., Ohtani, K., et al. (2016). Safety assessment of the Clostridium butyricum MIYAIRI 588(R) probiotic strain including evaluation of antimicrobial sensitivity and presence of Clostridium toxin genes in vitro and teratogenicity in vivo. Hum. Exp. Toxicol. 35, 818-832. doi: 10.1177/0960327115607372
52. Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., et al. (2015). Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 48, 186-194. doi: 10.1016/j.bbi.2015.03.016
53. Karlsson, C. L., önnerfält, J., Xu, J., Molin, G., Ahrné, S., and Thorngren-Jerneck, K. (2012). The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20, 2257-2261. doi: 10.1038/oby.2012.110
54. Korpela, K., Salonen, A., Virta, L. J., Kekkonen, R. A., Forslund, K., Bork, P., et al. (2016). Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat. Commun. 7:10410. doi: 10.1038/ncomms10410
55. Lagier, J. C., Hugon, P., Khelaifia, S., Fournier, P. E., La Scola, B., and Raoult, D. (2015). The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin. Microbiol. Rev. 28, 237-264. doi: 10.1128/CMR.00014-14
56. Laval, L., Martin, R., Natividad, J. N., Chain, F., Miquel, S., Desclee de Maredsous, C., et al. (2015). Lactobacillus rhamnosus CNCM I-3690 and the commensal bacterium Faecalibacterium prausnitzii A2-165 exhibit similar protective effects to induced barrier hyper-permeability in mice. Gut Microbes 6, 1-9. doi: 10.4161/19490976.2014.990784
57. Lefeber, T., Gobert, W., Vrancken, G., Camu, N., and De Vuyst, L. (2011). Dynamics and species diversity of communities of lactic acid bacteria and acetic acid bacteria during spontaneous cocoa bean fermentation in vessels. Food Microbiol. 28, 457-464. doi: 10.1016/j.fm.2010.10.010
58. Leuschner, R. G. K., Robinson, T. P., Hugas, M., Cocconcelli, P. S., Richard-Forget, F., Klein, G., et al. (2010). Qualified presumption of safety (QPS): a generic risk assessment approach for biological agents notified to the European Food Safety Authority (EFSA). Trends Food Sci. Technol. 21, 425-435. doi: 10.1016/j.tifs.2010.07.003
59. Li, M., Li, G., Shang, Q., Chen, X., Liu, W., Pi, X. E., et al. (2016). In vitro fermentation of alginate and its derivatives by human gut microbiota. Anaerobe 39, 19-25. doi: 10.1016/j.anaerobe.2016.02.003
60. Maeno, S., Dicks, L., Nakagawa, J., and Endo, A. (2017). Lactobacillus apinorum belongs to the fructophilic lactic acid bacteria. Biosci. Microb. Food Health. doi: 10.12938/bmfh.17-008
61. Maeno, S., Tanizawa, Y., Kanesaki, Y., Kubota, E., Kumar, H., Dicks, L., et al. (2016). Genomic characterization of a fructophilic bee symbiont Lactobacillus kunkeei reveals its niche-specific adaptation. Syst. Appl. Microbiol. 39, 516-526. doi: 10.1016/j.syapm.2016.09.006
62. Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D., Hirschfield, G. M., Hold, G., et al. (2016). The gut microbiota and host health: a new clinical frontier. Gut 65, 330-339. doi: 10.1136/gutjnl-2015-309990
63. Miquel, S., Beaumont, M., Martín, R., Langella, P., Braesco, V., and Thomas, M. (2015). A proposed framework for an appropriate evaluation scheme for microorganisms as novel foods with a health claim in Europe. Microb. Cell Fact. 9, 14-48. doi: 10.1186/s12934-015-0229-1
64. Miquel, S., Martin, R., Rossi, O., Bermudez-Humaran, L. G., Chatel, J. M., Sokol, H., et al. (2013). Faecalibacterium prausnitzii and human intestinal health. Curr. Opin. Microbiol. 16, 255-261. doi: 10.1016/j.mib.2013.06.003
65. Mirande, C., Kadlecikova, E., Matulova, M., Capek, P., Bernalier-Donadille, A., Forano, E., et al. (2010). Dietary fibre degradation and fermentation by two xylanolytic bacteria Bacteroides xylanisolvens XB1AT and Roseburia intestinalis XB6B4 from the human intestine. J. Appl. Microbiol. 109, 451-460. doi: 10.1111/j.1365-2672.2010.04671.x
66. Mtshali, P. S., Divol, B., and du Toit, M. (2012). Identification and characterization of Lactobacillus florum strains isolated from South African grape and wine samples. Int. J. Food Microbiol. 153, 106-113. doi: 10.1016/j.ijfoodmicro.2011.10.023
67. Nakanishi, S., Kataoka, K., Kuwahara, T., and Ohnishi, Y. (2003). Effects of high amylose maize starch and Clostridium butyricum on microbiota and formation metabolism in colonic of azoxymethane-induced aberrant crypt foci in the rat colon. Microbiol. Immunol. 47, 951-958. doi: 10.1111/j.1348-0421.2003.tb03469.x
68. Neveling, D. P., Endo, A., and Dicks, L. M. (2012). Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives. Curr. Microbiol. 65, 507-515. doi: 10.1007/s00284-012-0186-4
69. Ouwerkerk, J. P., Aalvink, S., Belzer, C., and de Vos, W. M. (2016a). Akkermansia glycaniphila sp. nov., an anaerobic mucin-degrading bacterium isolated from reticulated python faeces. Int. J. Syst. Evol. Microbiol. 66, 4614-4620. doi: 10.1099/ijsem.0.001399
70. Ouwerkerk, J. P., Koehorst, J. J., Schaap, P. J., Ritari, J., Paulin, L., Belzer, C., et al. (2017). Complete genome sequence of Akkermansia glycaniphila strain PytT, a mducin-degrading specialist of the reticulated python gut. Genome Announc. 5:e01098-16. doi: 10.1128/genomeA.01098-16
71. Ouwerkerk, J. P., van der Ark, K. C., Davids, M., Claassens, N. J., Robert Finestra, T., de Vos, W., et al. (2016b). Adaptation of Akkermansia muciniphila to the oxic-anoxic interface of the mucus layer. Appl. Environ. Microbiol. 82, 6983-6993. doi: 10.1128/AEM.01641-16
72. Papalexandratou, Z., Vrancken, G., De Bruyne, K., Vandamme, P., and De Vuyst, L. (2011). Spontaneous organic cocoa bean box fermentations in Brazil are characterized by a restricted species diversity of lactic acid bacteria and acetic acid bacteria. Food Microbiol. 28, 1326-1338. doi: 10.1016/j.fm.2011.06.003
73. Pham, V. T., Lacroix, C., Braegger, C. P., and Chassard, C. (2016). Early colonization of functional groups of microbes in the infant gut. Environ. Microbiol. 18, 2246-2258. doi: 10.1111/1462-2920.13316
74. Plovier, H., Everard, A., Druart, C., Depommier, C., Van Hul, M., Geurts, L., et al. (2017). A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat. Med. 23, 107-113. doi: 10.1038/nm.4236
75. Png, C. W., Lindén, S. K., Gilshenan, K. S., Zoetendal, E. G., McSweeney, C. S., Sly, L., et al. (2010). Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am. J. Gastroenterol. 105, 2420-2428. doi: 10.1038/ajg.2010.281
76. Quevrain, E., Maubert, M. A., Sokol, H., Devreese, B., and Seksik, P. (2016). The presence of the anti-inflammatory protein MAM, from Faecalibacterium prausnitzii, in the intestinal ecosystem. Gut. 65:882. doi: 10.1136/gutjnl-2015-311094
77. Remely, M., Hippe, B., Geretschlaeger, I., Stegmayer, S., Hoefinger, I., and Haslberger, A. (2015). Increased gut microbiota diversity and abundance of Faecalibacterium prausnitzii and Akkermansia after fasting: a pilot study. Wien. Klin. Wochenschr. 127, 394-398. doi: 10.1007/s00508-015-0755-1
78. Reunanen, J., Kainulainen, V., Huuskonen, L., Ottman, N., Belzer, C., Huhtinen, H., et al. (2015). Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer. Appl. Environ. Microbiol. 81, 3655-3662. doi: 10.1128/AEM.04050-14
79. Roeselers, G., Mittge, E. K., Stephens, W. Z., Parichy, D. M., Cavanaugh, C. M., Guillemin, K., et al. (2011). Evidence for a core gut microbiota in the zebrafish. ISME J. 5, 1595-1608. doi: 10.1038/ismej.2011.38
80. Schneeberger, M., Everard, A., Gomez-Valades, A. G., Matamoros, S., Ramirez, S., Delzenne, N. M., et al. (2015). Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 5:16643. doi: 10.1038/srep16643
81. Scott, K. P., Antoine, J. M., Midtvedt, T., and van Hemert, S. (2015). Manipulating the gut microbiota to maintain health and treat disease. Microb. Ecol. Health Dis. 26:25877. doi: 10.3402/mehd.v26.25877
82. Sears, C. L. (2005). A dynamic partnership: celebrating our gut flora. Anaerobe 11, 247-251. doi: 10.1016/j.anaerobe.2005.05.001
83. Selhub, E. M., Logan, A. C., and Bested, A. C. (2014). Fermented foods, microbiota, and mental health: ancient practice meets nutritional psychiatry. J. Physiol. Anthropol. 33:2 doi: 10.1186/1880-6805-33-2
84. Shang, H., Sun, J., and Chen, Y. Q. (2016). Clostridium butyricum CGMCC0313.1 modulates lipid profile, insulin resistance and colon homeostasis in obese mice. PLoS ONE 11:e0154373. doi: 10.1371/journal.pone.0154373
85. Shimbo, I., Yamaguchi, T., Odaka, T., Nakajima, K., Koide, A., Koyama, H., et al. (2005). Effect of Clostridium butyricum on fecal flora in Helicobacter pylori eradication therapy. World J. Gastroenterol. 11, 7520-7524. doi: 10.3748/wjg.v11.i47.7520
86. Shinnoh, M., Horinaka, M., Yasuda, T., Yoshikawa, S., Morita, M., Yamada, T., et al. (2013). Clostridium butyricum MIYAIRI 588 shows antitumor effects by enhancing the release of TRAIL from neutrophils through MMP-8. Int. J. Oncol. 42, 903-911. doi: 10.3892/ijo.2013.1790
87. Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermudez-Humaran, L. G., Gratadoux, J. J., et al. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U.S.A. 105, 16731-16736. doi: 10.1073/pnas.0804812105
88. Tamanai-Shacoori, Z., Smida, I., Bousarghin, L., Loreal, O., Meuric, V., Fong, S. B., et al. (2017). Roseburia spp.: a marker of health? Future Microbiol. 12, 157-170. doi: 10.2217/fmb-2016-0130
89. Taverniti, V., and Guglielmetti, S. (2011). The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 6, 261-274. doi: 10.1007/s12263-011-0218-x
90. Thomas, L. V., Suzuki, K., and Zhao, J. (2015). Probiotics: a proactive approach to health. A symposium report. Br. J. Nutr. 114(Suppl. 1), S1-S15. doi: 10.1017/S0007114515004043
91. Thorning, T. K., Raben, A., Tholstrup, T., Soedamah-Muthu, S. S., Givens, I., and Astrup, A. (2016). Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food Nutr. Res. 60:32527. doi: 10.3402/fnr.v60.32527
92. Tsilingiri, K., and Rescigno, M. (2012). Postbiotics: what else? Benef. Microbes 4, 101-107. doi: 10.3920/BM2012.0046
93. Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., and Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031. doi: 10.1038/nature05414
94. Udayappan, S., Manneras-Holm, L., Chaplin-Scott, A., Belzer, C., Herrema, H., Dallinga-Thie, G. M., et al. (2016). Oral treatment with. Npj Biofilms Microb. 2, 1-10. doi: 10.1038/npjbiofilms.2016.9
95. Ulluwishewa, D., Anderson, R. C., Young, W., McNabb, W. C., van Baarlen, P., Moughan, P. J., et al. (2015). Live Faecalibacterium prausnitzii in an apical anaerobic model of the intestinal epithelial barrier. Cell. Microbiol. 17, 226-240. doi: 10.1111/cmi.12360
96. Ulsemer, P., Toutounian, K., Kressel, G., Goletz, C., Schmidt, J., Karsten, U., et al. (2016). Impact of oral consumption of heat-treated Bacteroides xylanisolvens DSM 23964 on the level of natural TFa-specific antibodies in human adults. Benef. Microbes 6:16. doi: 10.3920/BM2015.0143
97. Ulsemer, P., Toutounian, K., Kressel, G., Schmidt, J., Karsten, U., Hahn, A., et al. (2012a). Safety and tolerance of Bacteroides xylanisolvens DSM 23964 in healthy adults. Benef. Microbes 3, 99-111. doi: 10.3920/BM2011.0051
98. Ulsemer, P., Toutounian, K., Schmidt, J., Karsten, U., and Goletz, S. (2012b). Preliminary safety evaluation of a new Bacteroides xylanisolvens isolate. Appl. Environ. Microbiol. 78, 528-535. doi: 10.1128/AEM.06641-11
99. Ulsemer, P., Toutounian, K., Schmidt, J., Leuschner, J., Karsten, U., and Goletz, S. (2012c). Safety assessment of the commensal strain Bacteroides xylanisolvens DSM 23964. Regul. Toxicol. Pharmacol. 62, 336-346. doi: 10.1016/j.yrtph.2011.10.014
100. Urbaniak, C., Cummins, J., Brackstone, M., MacKlaim, J. M., Gloor, G. B., Baban, C. K., et al. (2014). Microbiota of human breast tissue. Appl. Environ. Microbiol. 80, 3007-3014. doi: 10.1128/AEM.00242-14
101. van Passel, M. W. J., Kant, R., Zoetendal, E. G., Plugge, C. M., Derrien, M., Malfatti, S., et al. (2011). The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS ONE 6:e16876. doi: 10.1371/journal.pone.0016876
102. von Wright, A. (2012). Microbes for human and animal consumption. Benef. Microorg. Agric. Food Environ. 27-40 doi: 10.1079/9781845938109.0027
103. Wang, F.-Y., Liu, J.-M., Luo, H.-H., Liu, A.-H., and Jiang, Y. (2015). Potential protective effects of Clostridium butyricum on experimental gastric ulcers in mice. World J. Gastroenterol. 21, 8340-8351. doi: 10.3748/wjg.v21.i27.8340
104. Weir, T. L., Manter, D. K., Sheflin, A. M., Barnett, B. A., Heuberger, A. L., and Ryan, E. P. (2013). Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS ONE 8:e70803. doi: 10.1371/journal.pone.0070803
105. Wexler, H. M. (2007). Bacteroides: the good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20, 593-621. doi: 10.1128/CMR.00008-07
106. Yanagibashi, T., Hosono, A., Oyama, A., Tsuda, M., Hachimura, S., Takahashi, Y., et al. (2009). Bacteroides induce higher IgA production than Lactobacillus by increasing activation-induced cytidine deaminase expression in B cells in murine Peyer's patches. Biosci. Biotechnol. Biochem. 73, 372-377. doi: 10.1271/bbb.80612
107. Yassour, M., Lim, M. Y., Yun, H. S., Tickle, T. L., Sung, J., Song, Y. M., et al. (2016). Sub-clinical detection of gut microbial biomarkers of obesity and type 2 diabetes. Genome Med. 8:17. doi: 10.1186/s13073-016-0271-6
108. Yasueda, A., Mizushima, T., Nezu, R., Sumi, R., Tanaka, M., Nishimura, J., et al. (2016). The effect of Clostridium butyricum MIYAIRI on the prevention of pouchitis and alteration of the microbiota profile in patients with ulcerative colitis. Surg Today 46, 939-949. doi: 10.1007/s00595-015-1261-9
109. Zhang, X., Shen, D., Fang, Z., Jie, Z., Qiu, X., Zhang, C., et al. (2013). Human gut microbiota changes reveal the progression of glucose intolerance. PLoS ONE 8:e71108. doi: 10.1371/journal.pone.0071108
110. Zhao, X., Guo, Y., Liu, H., Gao, J., and Nie, W. (2014). Clostridium butyricum reduce lipogenesis through bacterial wall components and butyrate. Appl. Microbiol. Biotechnol. 98, 7549-7557. doi: 10.1007/s00253-014-5829-x