Broad bean (Vicia faba L.) induces intestinal inflammation in grass carp (Ctenopharyngodon idellus C. et V) by increasing relative abundances of intestinal gram-negative and flagellated bacteria

Frontiers in Microbiology

Volumn 9, Issue AUG, 2018, Pages

  Li, Zhifei ^a,b   Yu, Ermeng ^a,b   Wang, Guangjun ^a,b   Yu, Deguang ^a,b   Zhang, Kai ^a,b   Gong, Wangbao ^a,b   Xie, Jun ^a,b  

^a SOUTH CHINA SEA FISHERIES RESEARCH INSTITUTE   (China)

^b Guangdong Ecological Remediation of Aquaculture Pollution Research Center   (China)

Author keywords

Broad bean; Flagellin; Gram negative bacteria; Grass carp; Gut inflammation

Indexed keywords

ENDOTOXIN; FLAGELLIN; RNA 16S; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL FLAGELLUM; CONTROLLED STUDY; DIET; ENTERITIS; GENE EXPRESSION REGULATION; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; GRASS CARP; HISTOLOGY; HOST PATHOGEN INTERACTION; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; INTESTINE WALL; MICROVILLUS; NONHUMAN; PENNISETUM; PENNISETUM SINESE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SCANNING ELECTRON MICROSCOPY; UPREGULATION; VICIA FABA;

EID: 85051653731     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.01913     Document Type: Article

References (63)

1. Byndloss, M. X., Olsan, E. E., Rivera-Chávez, F., Tiffany, C. R., Cevallos, S. A., Lokken, K. L., et al. (2017). Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion. Science 357, 570-575. doi: 10.1126/science.aam9949
2. Caporaso, J. G., Kuczynski, J., Stombaugh, J., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303
3. Chassaing, B., Van de Wiele, T., De Bodt, J., Marzorati, M., and Gewirtz, A. T. (2017). Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation. Gut 66, 1414-1427. doi: 10.1136/gutjnl-2016-313099
4. Chikwati, E. M., Sahlmann, C., Holm, H., Penn, M. H., Krogdahl, Å, and Bakke, A. M. (2013). Alterations in digestive enzyme activities during the development of diet-induced enteritis in Atlantic salmon, Salmo salar L. Aquaculture 402-403, 28-37. doi: 10.1016/j.aquaculture.2013.03.023
5. Derrien, M., and Veiga, P. (2017). Rethinking diet to aid human-microbe symbiosis. Trends Microbiol. 25, 100-112. doi: 10.1016/j.tim.2016.09.011
6. Dimitroglou, A., Merrifield, D., Moate, R., Davies, S., Spring, P., Sweetman, J., et al. (2009). Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout Oncorhynchus mykiss (Walbaum). J. Anim. Sci. 87, 3226-3234. doi: 10.2527/jas.2008-1428
7. Duck, L. W., Walter, M. R., Novak, J., Kelly, D., Tomasi, M., Cong, Y., et al. (2007). Isolation of flagellated bacteria implicated in Crohn's disease. Inflamm. Bowel Dis. 13, 1191-1201. doi: 10.1002/ibd.20237
8. Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996-998. doi: 10.1038/nmeth.2604
9. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
10. Fang, W., Ma, Y., Qiu, X., and Chen, B. (1994). Study of the nutritive value and comprehensive use of broad bean protein. J. Nanchang Univ. 16, 11-13
11. Feng, L., and Zhou, X. (2006). Anti-nutritional effects of soybean agglutinin (SBA) on animals. Feed Ind. 27, 19-24
12. Gajardo, K., Rodiles, A., Kortner, T. M., Krogdahl, Å., Bakke, A. M., Merrifield, D. L., et al. (2016). A high-resolution map of the gut microbiota in Atlantic salmon (salmo salar): a basis for comparative gut microbial research. Sci. Rep. 6:30893. doi: 10.1038/srep30893
13. Gewirtz, A. T., Navas, T. A., Lyons, S., Godowski, P. J., and Madara, J. L. (2001a). Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167, 1882-1885. doi: 10.4049/jimmunol.167.4.1882
14. Gewirtz, A. T., Simon, P. O., Schmitt, C. K., Taylor, L. J., Hagedorn, C. H., O'Brien, A. D., et al. (2001b). Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Invest. 107, 99-109. doi: 10.1172/JCI10501
15. Ghanbari, M., Kneifel, W., and Domig, K. J. (2015). A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448, 464-475. doi: 10.1016/j.aquaculture.2015.06.033
16. Hedrera, M. I., Galdames, J. A., Jimenez-Reyes, M. F., Reyes, A. E., Avendaño-Herrera, R., Romero, J., et al. (2013). Soybean meal induces intestinal inflammation in zebrafish larvae. PLoS One 8:e69983. doi: 10.1371/journal.pone.0069983
17. Huang, R., Li, T., Ni, J., Bai, X., Gao, Y., Li, Y., et al. (2018). Different sex-based responses of gut microbiota during the development of hepatocellular carcinoma in liver-specific Tsc1-knockout mice. Front. Microbiol. 9:1008. doi: 10.3389/fmicb.2018.01008
18. Hughes, E. R., Winter, M. G., Duerkop, B. A., Spiga, L., Furtado, de Carvalho, T., et al. (2017). Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe 21, 208-219. doi: 10.1016/j.chom.2017.01.005
19. Imhann, F., Vila, A. V., Bonder, M. J., Fu, J., Gevers, D., Visschedijk, M. C., et al. (2017). Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut 67, 108-119. doi: 10.1136/gutjnl-2016-312135
20. Ingerslev, H.-C., Strube, M. L., von GersdorffJørgensen, L., Dalsgaard, I., Boye, M., and Madsen, L. (2014). Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immun. 40, 624-633. doi: 10.1016/j.fsi.2014.08.021
21. Karczewski, J., Troost, F. J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R. J., et al. (2010). Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G851-G859. doi: 10.1152/ajpgi.00327.2009
22. Langille, M. G. I., Zaneveld, J., Caporaso, J. G., Mcdonald, D., Dan, K., Reyes, J. A., et al. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814-821. doi: 10.1038/nbt.2676
23. Lee, H. S., Han, S. Y., Bae, E. A., Huh, C. S., Ahn, Y. T., Lee, J. H., et al. (2008). Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immounopharmacol. 8, 574-580. doi: 10.1016/j.intimp.2008.01.009
24. Ley, R. E., Backhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., and Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U.S.A. 102, 11070-11075. doi: 10.1073/pnas.0504978102
25. Ley, R. E., and Gewirtz, A. T. (2016). Corralling colonic flagellated microbiota. N. Engl. J. Med. 375, 85-87. doi: 10.1056/NEJMcibr1604801
26. Li, B., Leng, X., Li, X., Liu, X., Hu, B., and Li, J. (2008). Effects of feeding broad bean on growth, muscle composition and intestine protease activity of different sizes of grass carp, Ctenopharyngodon idella. J. Shanghai Fish. Univ. 17, 310-315
27. Li, Z., Che, J., Xie, J., Wang, G., Yu, E., Xia, Y., et al. (2017). Microbial succession in biofilms growing on artificial substratum in subtropical freshwater aquaculture ponds. FEMS. Microbiol. Lett. 364:fnx017. doi: 10.1093/femsle/fnx017
28. Liu, B., Wang, G., Ermeng, Y. U., Xie, J., Deguang, Y. U., Wang, H., et al. (2011). Comparison and evaluation of nutrition composition in muscle of grass carp Ctenopharyngodon idellus fed with broad bean. South China Fish. Sci. 7, 58-65
29. Llewellyn, M. S., Boutin, S., Hoseinifar, S. H., and Derome, N. (2014). Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front. Microbiol. 5:207. doi: 10.3389/fmicb.2014.00207
30. Magoc, T., and Salzberg, S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957-2963. doi: 10.1093/bioinformatics/btr507
31. Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., 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
32. Mazmanian, S. K., Round, J. L., and Kasper, D. L. (2008). A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625. doi: 10.1038/nature07008
33. Miyake, S., Nguqi, D. K., and Stingl, U. (2015). Diet strongly influences the gut microbiota of surgeonfishes. Mol. Ecol. 24, 656-672. doi: 10.1111/mec.13050
34. Moschen, A. R., Wieser, V., and Tilg, H. (2012). Dietary factors: major regulators of the gut's microbiota. Gut Liver 6, 411-416. doi: 10.5009/gnl.2012.6.4.411
35. Muegge, B. D., Kuczynski, J., Dan, K., Clemente, J. C., González, A., Fontana, L., 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
36. Ni, J., Li, X., He, Z., and Xu, M. (2017). A novel method to determine the minimum number of sequences required for reliable microbial community analysis. J. Microbiol. Methods 139, 196-201. doi: 10.1016/j.mimet.2017.06.006
37. Ni, J., Yan, Q., Yu, Y., and Zhang, T. (2014a). Factors influencing the grass carp gut microbiome and its effect on metabolism. FEMS. Microbiol. Ecol. 87, 704-714. doi: 10.1111/1574-6941.12256
38. Ni, J., Yan, Q., Yu, Y., and Zhang, T. (2014b). Fish gut microecosystem: a model for detecting spatial pattern of microorganisms. Chin. J. Oceanol. Limnol. 32, 54-57. doi: 10.1007/s00343-014-3072-z
39. Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., et al. (2012). Host-gut microbiota metabolic interactions. Science 336, 1262-1267. doi: 10.1126/science.1223813
40. Ouwehand, A. C., Salminen, S., and Isolauri, E. (2002). Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82, 279-289. doi: 10.1023/A:1020620607611
41. Parks, D. H., Tyson, G. W., Hugenholtz, P., and Beiko, R. G. (2014). STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123-3124. doi: 10.1093/bioinformatics/btu494
42. Philippot, L., Andersson, S. G. E., Battin, T. J., Prosser, J. I., Schimel, J. P., Whitman, W. B., et al. (2010). The ecological coherence of high bacterial taxonomic ranks. Nat. Rev. Microbiol. 8, 523-529. doi: 10.1038/nrmicro2367
43. Schirmer, M., Franzosa, E. A., Lloyd-Price, J., Mclver, L. J., Schwager, R., Poon, T. W., et al. (2018). Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat. Microbiol. 3, 337-346. doi: 10.1038/s41564-017-0089-z
44. Schrezenmeir, J., and de Vrese, M. (2001). Probiotecs, prebiotics, and synbiotics-approaching a definition. Am. J. Clin. Nutr. 73, 361S-364S. doi: 10.1093/ajcn/73.2.361s
45. Sipka, S., and Bruckner, G. (2014). The immunomodulatory role of bile acids. Int. Arch. Allergy Immunol. 165, 1-8. doi: 10.1159/000366100
46. Song, X., Zhao, J., Bo, Y., Liu, Z., Wu, K., and Gong, C. (2014). Aeromonas hydrophila induces intestinal inflammation in grass carp (Ctenopharyngodon idella): an experimental model. Aquaculture 434, 171-178. doi: 10.1016/j.aquaculture.2014.08.015
47. Tacon, A. G. J. (1993). Feed Ingredients for Warmwater Fish: Fish Meal and Other Processed Feedstuffs. Rome: FAO Fisheries Circular
48. Urán, P. A., Gonçalves, A. A., Taverne-Thiele, J. J., Schrama, J. W., Verreth, J. A., and Rombout, J. H. (2008). Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immun. 25, 751-760. doi: 10.1016/j.fsi.2008.02.013
49. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267. doi: 10.1128/AEM.00062-07
50. Wu, G., and Bi, T. (2010). Exploitation and utilization of broad bean. Cereal Oil Process. 9, 45-46
51. Wu, L., Qin, G., Sun, L., and Zhou, D. (2007). Soybean agglutinin and the effects on animal health. Soybean Sci. 26, 259-263
52. Wu, S., Wang, G., Angert, E. R., Wang, W., Li, W., and Zou, H. (2012). Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440. doi: 10.1371/journal.pone.0030440
53. Xiang, J., He, T., Wang, P., Xie, M., Xiang, J., and Ni, J. (2018). Opportunistic pathogens are abundant in the gut of cultured giant spiny frog (paa spinosa). Aquac. Res. 49, 2033-2041. doi: 10.1111/are.13660
54. Yan, Q., Li, J., Yu, Y., Wang, J., He, Z., Van Nostrand, J. D., et al. (2016). Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ. Microbiol. 18, 4739-4754. doi: 10.1111/1462-2920.13365
55. Yu, E. M., Zhang, H. F., Li, Z. F., Wang, G. J., Wu, H. K., Xie, J., et al. (2017). Proteomic signature of muscle fibre hyperplasia in response to faba bean intake in grass carp. Sci. Rep. 7:45950. doi: 10.1038/srep45950
56. Yuen, K., Woo, P., Teng, J., Leung, K., Wong, M., and Lau, S. (2001). Laribacter hongkongensis gen. nov., sp. nov., a novel gram-negative bacterium isolated from a cirrhotic patient with bacteremia and empyema. J. Clin. Microbiol. 39, 4227-4232. doi: 10.1128/JCM.39.12.4227-4232.2001
57. Zeng, H., Carlson, A. Q., Guo, Y., Yu, Y., Collier-Hyams, L. S., Madara, J. L., et al. (2003). Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J. Immunol. 171, 3668-3674. doi: 10.4049/jimmunol.171.7.3668
58. Zhang, H. L., Yu, L. X., Yang, W., Tang, L., Lin, Y., Wu, H., et al. (2012). Profound impact of gut homeostasis on chemically-induced pro-tumorigenic inflammation and hepatocarcinogenesis in rats. J. Hepatol. 57, 803-812. doi: 10.1016/j.jhep.2012.06.011
59. Zhang, Z. (2015). The Changes and Regulation of Immune Function of Ctenopharyngodon idellus in Different Crisping Periods. Shanghai: Shanghai Ocean University
60. Zhang, Z., Yu, E., Xie, J., Wang, G., Yu, D., Li, Z., et al. (2015). Intestinal microflora dynamic change, serum enzyme and growth performance of the grass carp (Ctenopharyngodon idellus) at different stages of feeding broad bean (Vicia faba). J. Agric. Biotechnol. 23, 151-160
61. Zhao, J., Bu, Y., Liu, Z., Shi, M., Xu, X., and Song, X. (2014). A TNBS-induced enteritis model in grass carp. J. Fish China 38, 559-568
62. Zhou, M., He, J., Shen, Y., Zhang, C., Wang, J., and Chen, Y. (2017). New frontiers in genetics, gut microbiota, and immunity: a rosetta stone for the pathogenesis of inflammatory bowel disease. Biomed Res. Int. 2017:8201672. doi: 10.1155/2017/8201672
63. Zuo, T., Kamm, M. A., Colombel, J.-F., and Ng, S. C. (2018). Urbanization and the gut microbiota in health and inflammatory bowel disease. Nat. Rev. Gastroenterol. Hepatol. 15, 440-452. doi: 10.1038/s41575-018-0003-z