Functional characterization of novel Faecalibacterium prausnitzii strains isolated from healthy volunteers: A step forward in the use of F. prausnitzii as a next-generation probiotic

Frontiers in Microbiology

Volumn 8, Issue JUN, 2017, Pages

  Martín, Rebeca ^a   Miquel, Sylvie ^a,b   Benevides, Leandro ^a,c   Bridonneau, Chantal ^a   Robert, Véronique ^a   Hudault, Sylvie ^a   Chain, Florian ^a   Berteau, Olivier ^a   Azevedo, Vasco ^c   Chatel, Jean M ^a   Sokol, Harry ^a,d,e   Bermúdez Humarán, Luis G ^a   Thomas, Muriel ^a   Langella, Philippe ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d INSERM   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

Commensal; Faecalibacterium; Immune modulatory properties; Molecular and metabolic characterization; Probiotic

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 8; LACTIC ACID; NEXT GENERATION PROBIOTIC AGENT; PROBIOTIC AGENT; RNA 16S; SHORT CHAIN FATTY ACID; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM COLONY; BIFIDOBACTERIUM LONGUM SUBSP. INFANTIS; BIODIVERSITY; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; CROHN DISEASE; ESCHERICHIA COLI; EXTREMELY OXYGEN SENSITIVE STRAIN; FAECALIBACTERIUM PRAUSNITZII; FIRMICUTES; GENE CLUSTER; GENETIC ANALYSIS; HEMOLYSIS; HT-29 CELL LINE; HUMAN; HUMAN CELL; IMMUNOMODULATION; INTESTINE FLORA; LISTERIA MONOCYTOGENES; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLOGENY; PLASMID; POLYMERASE CHAIN REACTION; RNA SEQUENCE; SCANNING ELECTRON MICROSCOPY; WHOLE GENOME SEQUENCING;

EID: 85021740602     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01226     Document Type: Article

References (50)

1. Balamurugan, R., Rajendiran, E., George, S., Samuel, G. V., and Ramakrishna, B. S. (2008). Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer. J. Gastroenterol. Hepatol. 23(8 Pt 1), 1298-1303. doi: 10.1111/j.1440-1746.2008.05490.x
2. Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H., Stewart, C. S., Henderson, C., et al. (2000). Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66, 1654-1661. doi: 10.1128/AEM.66.4.1654-1661.2000
3. Binnendijk, K. H., and Rijkers, G. T. (2013). What is a health benefit? An evaluation of EFSA opinions on health benefits with reference to probiotics. Benef. Microbes 4, 223-230. doi: 10.3920/BM2013.0019
4. Bocker, U., Nebe, T., Herweck, F., Holt, L., Panja, A., Jobin, C., et al. (2003). Butyrate modulates intestinal epithelial cell-mediated neutrophil migration. Clin. Exp. Immunol. 131, 53-60. doi: 10.1046/j.1365-2249.2003.02056.x
5. De Palma, G., Nadal, I., Medina, M., Donat, E., Ribes-Koninckx, C., Calabuig, M., et al. (2010). Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol. 10:63. doi: 10.1186/1471-2180-10-63
6. Duncan, S. H., Hold, G. L., Harmsen, H. J., Stewart, C. S., and Flint, H. J. (2002). Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 52(Pt 6), 2141-2146. doi: 10.1099/00207713-52-6-2141
7. Duncan, S. H., Holtrop, G., Lobley, G. E., Calder, A. G., Stewart, C. S., and Flint, H. J. (2004). Contribution of acetate to butyrate formation by human faecal bacteria. Br. J. Nutr. 91, 915-923. doi: 10.1079/BJN20041150
8. Eaton, T. J., and Gasson, M. J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67, 1628-1635. doi: 10.1128/AEM.67.4.1628-1635.2001
9. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2012). Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10:2740. doi: 10.2903/j.efsa.2012.2740
10. FAO/WHO (2002). FAO/WHO and Agriculture Organization Guidelines for the Evaluation of Probiotics in Food. London: Food and Agriculture Organization, 11.
11. 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
12. Furet, J. P., Kong, L. C., Tap, J., Poitou, C., Basdevant, A., Bouillot, J. L., et al. (2010). Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59, 3049-3057. doi: 10.2337/db10-0253
13. Fusunyan, R. D., Quinn, J. J., Fujimoto, M., MacDermott, R. P., and Sanderson, I. R. (1999). Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Mol. Med. 5, 631-640.
14. Hold, G. L., Schwiertz, A., Aminov, R. I., Blaut, M., and Flint, H. J. (2003). Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl. Environ. Microbiol. 69, 4320-4324. doi: 10.1128/AEM.69.7.4320-4324.2003
15. Joly, F., Mayeur, C., Bruneau, A., Noordine, M. L., Meylheuc, T., Langella, P., et al. (2010). Drastic changes in fecal and mucosa-associated microbiota in adult patients with short bowel syndrome. Biochimie 92, 753-761. doi: 10.1016/j.biochi.2010.02.015
16. Kamitani, H., Ikawa, H., Hsi, L. C., Watanabe, T., DuBois, R. N., and Eling, T. E. (1999). Regulation of 12-lipoxygenase in rat intestinal epithelial cells during differentiation and apoptosis induced by sodium butyrate. Arch. Biochem. Biophys. 368, 45-55. doi: 10.1006/abbi.1999.1284
17. Kechaou, N., Chain, F., Gratadoux, J. J., Blugeon, S., Bertho, N., Chevalier, C., et al. (2012). Identification of one novel candidate probiotic Lactobacillus plantarum strain active against influenza virus infection in mice by a large-scale screening. Appl. Environ. Microbiol. 79, 1491-1499. doi: 10.1128/AEM.03075-12
18. Khan, M. T., van Dijl, J. M., and Harmsen, H. J. (2014). Antioxidants keep the potentially probiotic but highly oxygen-sensitive human gut bacterium Faecalibacterium prausnitzii alive at ambient air. PLoS ONE 9:e96097. doi: 10.1371/journal.pone.0096097
19. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581
20. Lan, A., Bruneau, A., Bensaada, M., Philippe, C., Bellaud, P., Rabot, S., et al. (2008). Increased induction of apoptosis by Propionibacterium freudenreichii TL133 in colonic mucosal crypts of human microbiota-associated rats treated with 1,2-dimethylhydrazine. Br. J. Nutr. 100, 1251-1259. doi: 10.1017/S0007114508978284
21. Lopez-Siles, M., Duncan, S. H., Garcia-Gil, L. J., and Martinez-Medina, M. (2017). Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J. 11, 841-852. doi: 10.1038/ismej.2016.176
22. Lopez-Siles, M., Khan, T. M., Duncan, S. H., Harmsen, H. J., Garcia-Gil, L. J., and Flint, H. J. (2012). Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl. Environ. Microbiol. 78, 420-428. doi: 10.1128/AEM.06858-11
23. Louis, P., Duncan, S. H., McCrae, S. I., Millar, J., Jackson, M. S., and Flint, H. J. (2004). Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J. Bacteriol. 186, 2099-2106. doi: 10.1128/JB.186.7.2099-2106.2004
24. Mack, D. R. (2004). D(-)-lactic acid-producing probiotics, D(-)-lactic acidosis and infants. Can. J. Gastroenterol. 18, 671-675. doi: 10.1155/2004/342583
25. Martin, R., Chain, F., Miquel, S., Lu, J., Gratadoux, J. J., Sokol, H., et al. (2014). The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm. Bowel Dis. 20, 417-430. doi: 10.1097/01.MIB.0000440815.76627.64
26. Martin, R., Miquel, S., Ulmer, J., Kechaou, N., Langella, P., and Bermudez-Humaran, L. G. (2013). Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb. Cell Fact. 12:71. doi: 10.1186/1475-2859-12-71
27. Martin, R., Sanchez, B., Urdaci, M. C., Langella, P., Suarez, J. E., and Bermudez-Humaran, L. G. (2015). Effect of iron on the probiotic properties of the vaginal isolate Lactobacillus jensenii CECT 4306. Microbiology 161(Pt 4), 708-718. doi: 10.1099/mic.0.000044
28. Mayeur, C., Gratadoux, J. J., Bridonneau, C., Chegdani, F., Larroque, B., Kapel, N., et al. (2013). Faecal D/L lactate ratio is a metabolic signature of microbiota imbalance in patients with short bowel syndrome. PLoS ONE 8:e54335. doi: 10.1371/journal.pone.0054335
29. Miquel, S. R., Martìn Bridonneau, C., Robert, V., Sokol, H., Bermúdez-Humarán, L., Thomas, M., et al. (2014). Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes 5, 146-151. doi: 10.4161/gmic.27651
30. Miquel, S., Beaumont, M., Martin, R., Langella, P., Braesco, V., and Thomas, M. (2015a). A proposed framework for an appropriate evaluation scheme for microorganisms as novel foods with a health claim in Europe. Microb. Cell Fact. 14, 48. doi: 10.1186/s12934-015-0229-1
31. Miquel, S., Leclerc, M., Martin, R., Chain, F., Lenoir, M., Raguideau, S., et al. (2015b). Identification of metabolic signatures linked to anti-inflammatory effects of Faecalibacterium prausnitzii. Mbio 6:e00300-15. doi: 10.1128/mBio.00300-15
32. Miquel, S., Martin, R., Rossi, O., Bermudez-Humaran, L., Chatel, J., 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
33. Neish, A. S. (2009). Microbes in gastrointestinal health and disease. Gastroenterology 136, 65-80. doi: 10.1053/j.gastro.2008.10.080
34. Pineiro, M., and Stanton, C. (2007). Probiotic bacteria: legislative framework- requirements to evidence basis. J. Nutr. 137(3 Suppl. 2), 850S-853S.
35. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59-65. doi: 10.1038/nature08821
36. Quevrain, E., Maubert, M. A., Michon, C., Chain, F., Marquant, R., Tailhades, J., et al. (2016). Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut 65, 415-425. doi: 10.1136/gutjnl-2014-307649
37. Radziwill-Bienkowska, J. M., Le, D. T., Szczesny, P., Duviau, M. P., Aleksandrzak-Piekarczyk, T., Loubiere, P., et al. (2016). Adhesion of the genome-sequenced Lactococcus lactis subsp. cremoris IBB477 strain is mediated by specific molecular determinants. Appl. Microbiol. Biotechnol. 100, 9605-9617. doi: 10.1007/s00253-016-7813-0
38. Radziwill-Bienkowska, J. M., Zochowska, D., Bardowski, J., Mercier-Bonin, M., and Kowalczyk, M. (2014). Lactococcus lactis IBB477 presenting adhesive and muco-adhesive properties as a candidate carrier strain for oral vaccination against influenza virus. Acta Biochim. Pol. 61, 603-607.
39. Rajilic-Stojanovic, M., Biagi, E., Heilig, H. G., Kajander, K., Kekkonen, R. A., Tims, S., and de Vos, W. M. (2011). Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 141, 1792-1801. doi: 10.1053/j.gastro.2011.07.043
40. Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G., and Louis, P. (2009). Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br. J. Nutr. 101, 541-550. doi: 10.1017/S0007114508019880
41. Rossi, O., Khan, M. T., Schwarzer, M., Hudcovic, T., Srutkova, D., Duncan, S. H., et al. (2015). Faecalibacterium prausnitzii strain HTF-F and its extracellular polymeric matrix attenuate clinical parameters in DSS-induced colitis. PLoS ONE 10:e0123013. doi: 10.1371/journal.pone.0123013
42. Sanders, M. E., Akkermans, L. M., Haller, D., Hammerman, C., Heimbach, J., Hormannsperger, G., et al. (2010). Safety assessment of probiotics for human use. Gut Microbes 1, 164-185. doi: 10.4161/gmic.1.3.12127
43. Sarrabayrouse, G., Bossard, C., Chauvin, J. M., Jarry, A., Meurette, G., Quevrain, E., et al. (2014). CD4CD8aa lymphocytes, a novel human regulatory T cell subset induced by colonic bacteria and deficient in patients with inflammatory bowel disease. PLoS Biol. 12:e1001833. doi: 10.1371/journal.pbio.1001833
44. Schmidt, C. (2013). The startup bugs. Nat. Biotechnol. 31, 279-281. doi: 10.1038/nbt.2544
45. 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
46. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
47. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. doi: 10.1093/nar/22.22.4673
48. van Tongeren, S. P., Slaets, J. P., Harmsen, H. J., and Welling, G. W. (2005). Fecal microbiota composition and frailty. Appl. Environ. Microbiol. 71, 6438-6442. doi: 10.1128/AEM.71.10.6438-6442.2005
49. Wiseman, L. R., Lamb, H., and Cefpirome, M. (1997). A review of its antibacterial activity, pharmacokinetic properties and clinical efficacy in the treatment of severe nosocomial infections and febrile neutropenia. Drugs 54, 117-140. doi: 10.2165/00003495-199754010-00013
50. Wrzosek, L., Miquel, S., Noordine, M. L., Bouet, S., Chevalier-Curt, M. J., Robert, V., et al. (2013). Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 11:61. doi: 10.1186/1741-7007-11-61