The potential of class II bacteriocins to modify gut microbiota to improve host health

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Umu, Özgün C O ^a   Bäuerl, Christine ^b   Oostindjer, Marije ^a   Pope, Phillip B ^a   Hernández, Pablo E ^c   Pérez Martínez, Gaspar ^b   Diep, Dzung B ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; ENTEROCIN L50; ENTEROCIN P; ENTEROCIN Q; GARVICIN ML; PEDIOCIN PA 1; PLANTARICIN EF; PLANTARICIN JK; PROBIOTIC AGENT; SAKACIN A; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; RNA 16S;

ANIMAL EXPERIMENT; ARTICLE; CLOSTRIDIUM; COMMUNITY STRUCTURE; CONTROLLED STUDY; ENTEROCOCCACEAE; FECES MICROFLORA; FEMALE; INTESTINE FLORA; LACTIC ACID BACTERIUM; MOUSE; NONHUMAN; STAPHYLOCOCCUS; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN; ANIMAL; ANTIBIOSIS; BACTERIAL PHENOMENA AND FUNCTIONS; BIODIVERSITY; DRUG EFFECTS; FECES; HOMEOSTASIS; METABOLISM; METAGENOME; METAGENOMICS; MICROBIOLOGY;

ANIMALS; ANTIBIOSIS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIOCINS; BIODIVERSITY; BIOMARKERS; FECES; GASTROINTESTINAL MICROBIOME; HOMEOSTASIS; METAGENOME; METAGENOMICS; MICE; RNA, RIBOSOMAL, 16S;

EID: 84991251478     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0164036     Document Type: Article

References (72)

1. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489: 220-30. doi: 10.1038/nature11550 PMID: 22972295
2. Umu OC, Oostindjer M, Pope PB, Svihus B, Egelandsdal B, Nes IF, et al. Potential applications of gut microbiota to control human physiology. Antonie Van Leeuwenhoek. 2013; 104: 609-618. doi: 10.1007/s10482-013-0008-0 PMID: 23975514
3. O'Toole PW, Cooney JC. Probiotic bacteria influence the composition and function of the intestinal microbiota. Interdiscip Perspect Infect Dis. 2008;175285. doi: 10.1155/2008/175285 PMID: 19277099
4. Nes IF, Yoon S-S, Diep DB. Ribosomally Synthesiszed Antimicrobial Peptides (Bacteriocins) in Lactic Acid Bacteria: A Review. Food Sci Biotechnol. 2007; 16: 675-690.
5. Jack RW, Tagg JR, Ray B. Bacteriocins of gram-positive bacteria. Microbiol Rev. 1995; 59: 171-200. PMID: 7603408
6. Dobson A, Cotter PD, Paul Ross R, Hill C. Bacteriocin production: A probiotic trait? Appl Environ Microbiol. 2012; 78: 1-6. doi: 10.1128/AEM.05576-11 PMID: 22038602
7. Cotter PD, Hill C, Ross PR. Bacteriocins: Developing innate immunity for food. 2005; 3: 777-788. doi: 10.1038/nrmicro1240 PMID: 16205711
8. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102: 11070-5. doi: 10.1073/pnas.0504978102 PMID: 16033867
9. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci. 2007; 104: 979-984. doi: 10.1073/pnas. 0605374104 PMID: 17210919
10. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010; 4: 232-41. doi: 10.1038/ismej.2009.112 PMID: 19865183
11. Desbonnet L, Clarke G, Traplin A, O'Sullivan O, Crispie F, Moloney RD, et al. Gut microbiota depletion from early adolescence in mice: Implications for brain and behaviour. Brain Behav Immun. 2015; 48: 165-173. doi: 10.1016/j.bbi.2015.04.004 PMID: 25866195
12. Jeffery IB, O'Toole PW. Diet-microbiota interactions and their implications for healthy living. Nutrients. 2013; 5: 234-52. doi: 10.3390/nu5010234 PMID: 23344252
13. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488: 178-84. doi: 10.1038/nature11319 PMID: 22797518
14. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011; 473: 174-180. doi: 10.1038/nature10187 PMID: 21508958
15. Rea MC, Dobson A, O'Sullivan O, Crispie F, Fouhy F, Cotter PD, et al. Effect of broad-and narrowspectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon. Proc Natl Acad Sci. 2011; 108: 4639-4644. doi: 10.1073/pnas.1001224107 PMID: 20616009
16. Million M, Lagier JC, Yahav D, Paul M. Gut bacterial microbiota and obesity. Clinical Microbiology and Infection. 2013; 19: 305-313. doi: 10.1111/1469-0691.12172 PMID: 23452229
17. Luoto R, Collado MC, Salminen S, Isolauri E. Reshaping the gut microbiota at an early age: functional impact on obesity risk? Ann Nutr Metab. 2013; 63: 17-26. doi: 10.1159/000354896 PMID: 24217033
18. Collado MC, Isolauri E, Laitinen K, Salminen S. Effect of mother's weight on infant's microbiota acquisition, composition, and activity during early infancy: A prospective follow-up study initiated in early pregnancy. Am J Clin Nutr. 2010; 92: 1023-1030. doi: 10.3945/ajcn.2010.29877 PMID: 20844065
19. de Vos WM, de Vos EA. Role of the intestinal microbiome in health and disease: From correlation to causation. Nutr Rev. 2012; 70: S45-56. doi: 10.1111/j.1753-4887.2012.00505.x PMID: 22861807
20. Bhardwaj A, Gupta H, Kapila S, Kaur G, Vij S, Malik RK. Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. Int J Food Microbiol. 2010; 141: 156-164. doi: 10.1016/j.ijfoodmicro.2010.05.001 PMID: 20570005
21. Dabour N, Zihler A, Kheadr E, Lacroix C, Fliss I. In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int J Food Microbiol. 2009; 133: 225-233. doi: 10.1016/j.ijfoodmicro.2009.05.005 PMID: 19541383
22. Rea MC, Alemayehu D, Ross RP, Hill C. Gut solutions to a gut problem: Bacteriocins, probiotics and bacteriophage for control of Clostridium difficile infection. J Med Microbiol. 2013; 62: 1369-1378. doi: 10.1099/jmm.0.058933-0 PMID: 23699066
23. Mota-Meira M, Morency H, Lavoie MC. In vivo activity of mutacin B-Ny266. J Antimicrob Chemother. 2005; 56: 869-71. doi: 10.1093/jac/dki295 PMID: 16155061
24. Kommineni S, Bretl DJ, Lam V, Chakraborty R, Hayward M, Simpson P, et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature. 2015; 526: 719-22. doi: 10.1038/nature15524 PMID: 26479034
25. Millette M, Cornut G, Dupont C, Shareck F, Archambault D, Lacroix M. Capacity of human nisin-and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol. 2008; 74: 1997-2003. doi: 10.1128/AEM.02150-07 PMID: 18245231
26. Clarke SF, Murphy EF, O'Sullivan O, Ross RP, O'Toole PW, Shanahan F, et al. Targeting the Microbiota to Address Diet-Induced Obesity: A Time Dependent Challenge. PLoS One. 2013; 8: e65790. doi: 10.1371/journal.pone.0065790 PMID: 23762426
27. Cotter PD, Ross RP, Hill C. Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol. 2013; 11: 95-105. doi: 10.1038/nrmicro2937 PMID: 23268227
28. Schillinger U, Lücke FK. Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol. 1989; 55: 1901-1906. doi: 10.1016/S0168-1605(03)00051-5 PMID: 2782870
29. Marugg JD, Gonzalez CF, Kunka BS, Ledeboer AM, Pucci MJ, Toonen MY, et al. Cloning, expression, and nucleotide sequence of genes involved in production of pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0. Appl Environ Microbiol. 1992; 58: 2360-2367. doi: 10.1007/s00436-011-2552-8 PMID: 1514784
30. Cintas LM, Casaus P, Holo H, Hernandez PE, Nes IF, Håvarstein LS. Enterocins L50A and L50B, Two Novel Bacteriocins from Enterococcus faecium L50, Are Related to Staphylococcal Hemolysins. J Bacteriology. 1998; 180: 1988-1994.
31. Anderssen EL, Diep DB, Nes IF, Eijsink VGH, Nissen-Meyer J. Antagonistic activity of Lactobacillus plantarum C11: Two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Appl Environ Microbiol. 1998; 64: 2269-2272. PMID: 9603847
32. Borrero J, Brede DA, Skaugen M, Diep DB, Herranz C, Nes IF, et al. Characterization of garvicin ML, a novel circular bacteriocin produced by lactococcus garvieae DCC43, isolated from mallard ducks (Anas platyrhynchos). Appl Environ Microbiol. 2011; 77: 369-373. doi: 10.1128/AEM.01173-10 PMID: 21057028
33. Criado R, Diep DB, Aakra A, Gutiérrez J, Nes IF, Hernández PE, et al. Complete sequence of the enterocin Q-encoding plasmid pCIZ2 from the multiple bacteriocin producer Enterococcus faecium L50 and genetic characterization of enterocin Q production and immunity. Appl Environ Microbiol. 2006; 72: 6653-66. doi: 10.1128/AEM.00859-06 PMID: 17021217
34. Daeschel MA, McKenney MC, McDonald LC. Bacterilcidal activity of lactobacillus plantarum C-11. Food Microbiology. 1990; 7: 91-98.
35. Gabrielsen C, Brede DA, Salehian Z, Nes IF, Diep DB. Functional genetic analysis of the garml gene cluster in Lactococcus garvieae DCC43 gives new insights into circular bacteriocin biosynthesis. J Bacteriol. 2014; 196: 911-919. doi: 10.1128/JB.01115-13 PMID: 24336941
36. Illumina. 16S Metagenomic Sequencing Library Preparation. 1-28. Available: http://www.illumina. com/content/dam/illumina-support/documents/documentation/chemistry-documentation/16s/16smetagenomic-library-prep-guide-15044223-b.pdf.
37. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013; 41: e1. doi: 10.1093/nar/gks808 PMID: 22933715
38. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013; 10: 996-8. doi: 10.1038/nmeth.2604 PMID: 23955772
39. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-2461. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
40. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-2200. doi: 10.1093/bioinformatics/btr381 PMID: 21700674
41. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72: 5069-5072. doi: 10.1128/AEM.03006-05 PMID: 16820507
42. Caporaso JG, Bittinger K, Bushman FD, Desantis TZ, Andersen GL, Knight R. PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26: 266-267. doi: 10.1093/bioinformatics/btp636 PMID: 19914921
43. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73: 5261-5267. doi: 10.1128/AEM.00062-07 PMID: 17586664
44. Price MN, Dehal PS, Arkin AP. FastTree 2-Approximately maximum-likelihood trees for large alignments. PLoS One. 2010; 5: e9490. doi: 10.1371/journal.pone.0009490 PMID: 20224823
45. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71: 8228-8235. doi: 10.1128/AEM.71.12.8228-8235.2005 PMID: 16332807
46. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014; 30: 3123-24. doi: 10.1093/bioinformatics/btu494 PMID: 25061070
47. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012; 8: e1002606. doi: 10.1371/journal. pcbi.1002606 PMID: 22807668
48. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13: 2498-504. doi: 10.1101/gr.1239303 PMID: 14597658
49. Riboulet-Bisson E, Sturme MHJ, Jeffery IB, O'Donnell MM, Neville BA, Forde BM, et al. Effect of lactobacillus salivarius bacteriocin ABP118 on the mouse and pig intestinal microbiota. PLoS One. 2012; 7: e 31113. doi: 10.1371/journal.pone.0031113 PMID: 22363561
50. Walsh MC, Gardiner GE, Hart OM, Lawlor PG, Daly M, Lynch B, et al. Predominance of a bacteriocinproducing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiol Ecol. 2008; 64: 317-327. doi: 10.1111/j.1574-6941.2008. 00454.x PMID: 18373687
51. Kwok LY, Guo Z, Zhang J, Wang L, Qiao J, Hou Q, et al. The impact of oral consumption of Lactobacillus plantarum P-8 on faecal bacteria revealed by pyrosequencing. Benef Microbes. 2015; 6: 405-413. doi: 10.3920/BM2014.0063 PMID: 25653153
52. Eijsink VGH, Axelsson L, Diep DB, Håvarstein LS, Holo H, Nes IF. Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol. 2002; 81: 639-654. doi: 10.1023/A:1020582211262 PMID: 12448760
53. Kjos M, Borrero J, Opsata M, Birri DJ, Holo H, Cintas LM, et al. Target recognition, resistance, immunity and genome mining of class II bacteriocins from Gram-positive bacteria. Microbiology. 2011; 157: 3256-3267. doi: 10.1099/mic.0.052571-0 PMID: 21980118
54. Malys MK, Campbell L, Malys N. Symbiotic and antibiotic interactions between gut commensal microbiota and host immune system. Medicina. 2015; 51: 69-75. doi: 10.1016/j.medici.2015.03.001 PMID: 25975874
55. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008; 8: 125. doi: 10.1186/1471-2180-8-125 PMID: 18652685
56. Bien J, Palagani V, Bozko P. The intestinal microbiota dysbiosis and Clostridium difficile infection: is there a relationship with inflammatory bowel disease? Therap Adv Gastroenterol. 2013; 6: 53-68. doi: 10.1177/1756283X12454590 PMID: 23320050
57. La Rosa SL, Casey PG, Hill C, Diep DB, Nes IF, Brede DA. In vivo assessment of growth and virulence gene expression during commensal and pathogenic lifestyles of luxABCDE-tagged Enterococcus faecalis strains in murine gastrointestinal and intravenous infection models. Appl Environ Microbiol. 2013; 79: 3986-3997. doi: 10.1128/AEM.00831-13 PMID: 23603680
58. Abdulamir AS, Hafidh RR, Abu Bakar F. The association of Streptococcus bovis/gallolyticus with colorectal tumors: the nature and the underlying mechanisms of its etiological role. J Exp Clin Cancer Res. 2011; 30: 11. doi: 10.1186/1756-9966-30-11 PMID: 21247505
59. Acton DS, Tempelmans Plat-Sinnige MJ, Van Wamel W, De Groot N, Van Belkum A. Intestinal carriage of Staphylococcus aureus: How does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis. 2009; 28: 115-127. doi: 10.1007/s10096-008-0602-7 PMID: 18688664
60. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012; 9: 577-589. doi: 10.1038/nrgastro.2012.156 PMID: 22945443
61. Pessione E. Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front Cell Infect Microbiol. 2012; 2: 1-15. doi: 10.3389/fcimb.2012.00086 PMID: 22919677
62. Parkinson J. Communication Modules in Bacterial Signaling Proteins. Annu Rev Genet. 1992; 26: 71-112. doi: 10.1146/annurev.genet.26.1.71 PMID: 1482126
63. Kleerebezem M, Quadri LE, Kuipers OP, de Vos WM. Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol. 1997; 24: 895-904. doi: 10.1046/j.1365-2958.1997.4251782.x PMID: 9219998
64. Diep DB, Axelsson L, Grefsli C, Nes IF. The synthesis of the bacteriocin sakacin A is a temperaturesensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology. 2000; 146: 2155-2160. doi: 10.1099/00221287-146-9-2155 PMID: 10974103
65. Diep DB, Straume D, Kjos M, Torres C, Nes IF. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides. 2009; 30: 1562-1574. doi: 10.1016/j.peptides.2009.05.014 PMID: 19465075
66. Holzapfel WH, Geisen R, Schillinger U. Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Int J Food Microbiol. 1995; 24: 343-362. doi: 10.1016/0168-1605(94)00036-6 PMID: 7710912
67. Magnusson J, Schnürer J. Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broadspectrum proteinaceous antifungal compound. Appl Environ Microbiol. 2001; 67: 1-5. doi: 10.1128/AEM.67.1.1-5.2001 PMID: 11133421
68. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol. 2008; 6: 121-31. doi: 10.1038/nrmicro1817 PMID: 18180751
69. Kles KA, Chang EB. Short-chain fatty acids impact on intestinal adaptation, inflammation, carcinoma, and failure. Gastroenterology. 2006; 130: 100-105. doi: 10.1053/j.gastro.2005.11.048 PMID: 16473056
70. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ and Bakken BM. The role of shortchain fatty acids in the interplay between diet, gut microbiota and host energy metabolism. J Lipid Res. 2013; 54(9): 2325-2340. doi: 10.1007/s11548-012-0737-y PMID: 23821742
71. Chang YH, Kim JK, Kim HJ, Kim WY, Kim YB, Park YH. Selection of a potential probiotic Lactobacillus strain and subsequent in vivo studies. Antonie Van Leeuwenhoek. 2001; 80: 193-199. doi: 10.1023/A:1012213728917 PMID: 11759052
72. Gourbeyre P, Denery S, Bodinier M. Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol. 2011; 89: 685-695. doi: 10.1189/jlb.1109753 PMID: 21233408