The effect of dietary supplementation with Clostridium butyricum on the growth performance, immunity, intestinal microbiota and disease resistance of tilapia (Oreochromis niloticus)


Autoři: Hongqin Li aff001;  Ying Zhou aff003;  Huayun Ling aff003;  Li Luo aff004;  Desheng Qi aff001;  Lin Feng aff005
Působiště autorů: Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China aff001;  Animal Feed Science Research Institute, New Hope Liuhe Co., Ltd, Chengdu, Sichuan, China aff002;  Technology Center, Sun HY Bio Co., Ltd, Wuhan, Hubei, China aff003;  Department of Aquaculture, Southwest University, Chongqing, China aff004;  Animal Nutrition Institute, Sichuan Agricultural University, Chengdu, China aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223428

Souhrn

This study was conducted to assess the effects of dietary Clostridium butyricum on the growth, immunity, intestinal microbiota and disease resistance of tilapia (Oreochromis niloticus). Three hundreds of tilapia (56.21 ± 0.81 g) were divided into 5 groups and fed a diet supplemented with C. butyricum at 0, 1 x 104, 1 x 105, 1 x 106 or 1 x 107 CFU g-1 diet (denoted as CG, CB1, CB2, CB3 and CB4, respectively) for 56 days. Then 45 fish from each group were intraperitoneally injected with Streptococcus agalactiae, and the mortality was recorded for 14 days. The results showed that dietary C. butyricum significantly improved the specific growth rate (SGR) and feed intake in the CB2 group and decreased the cumulative mortality post-challenge with S. agalactiae in the CB2, CB3 and CB4 groups. The serum total antioxidant capacity and intestinal interleukin receptor-associated kinase-4 gene expression were significantly increased, and serum malondialdehyde content and diamine oxidase activity were significantly decreased in the CB1, CB2, CB3 and CB4 groups. Serum complement 3 and complement 4 concentrations and intestinal gene expression of tumour necrosis factor α, interleukin 8, and myeloid differentiation factor 88 were significantly higher in the CB2, CB3 and CB4 groups. Intestinal toll-like receptor 2 gene expression was significantly upregulated in the CB3 and CB4 groups. Dietary C. butyricum increased the diversity of the intestinal microbiota and the relative abundance of beneficial bacteria (such as Bacillus), and decreased the relative abundance of opportunistic pathogenic bacteria (such as Aeromonas) in the CB2 group. These results revealed that dietary C. butyricum at a suitable dose enhanced growth performance, elevated humoral and intestinal immunity, regulated the intestinal microbial components, and improved disease resistance in tilapia. The optimal dose was 1 x 105 CFU g-1 diet.

Klíčová slova:

Bacterial pathogens – Colon – Cytokines – Diet – Gastrointestinal tract – Gene expression – Microbiome – Probiotics


Zdroje

1. Hai NV. The use of probiotics in aquaculture. J Appl Microbiol. 2015;119: 917–935. doi: 10.1111/jam.12886 26119489

2. Wang A, Ran C, Wang Y, Zhang Z, Ding Q, Yang Y, et al. Use of probiotics in aquaculture of China-a review of the past decade. Fish Shellfish Immunol. 2019;86: 734–755. doi: 10.1016/j.fsi.2018.12.026 30553887

3. Chauhan A, Singh R. Probiotics in aquaculture: a promising emerging alternative approach. Symbiosis. 2019;77: 99–113.

4. Lazado CC, Caipang CM, Estante EG. Prospects of host-associated microorganisms in fish and penaeids as probiotics with immunomodulatory functions. Fish Shellfish Immunol. 2015;45: 2–12. doi: 10.1016/j.fsi.2015.02.023 25703713

5. Son VM, Chang CC, Wu MC, Guu YK, Chiu CH, Cheng W. Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immunol. 2009;26: 691–698. doi: 10.1016/j.fsi.2009.02.018 19264134

6. Gupta A, Gupta P, Dhawan A. Dietary supplementation of probiotics affects growth, immune response and disease resistance of Cyprinus carpio fry. Fish Shellfish Immunol. 2014;41: 113–119. doi: 10.1016/j.fsi.2014.08.023 25160796

7. Ramos MA, Goncalves JF, Batista S, Costas B, Pires MA, Rema P, et al. Growth, immune responses and intestinal morphology of rainbow trout (Oncorhynchus mykiss) supplemented with commercial probiotics. Fish Shellfish Immunol. 2015;45: 19–26. doi: 10.1016/j.fsi.2015.04.001 25865055

8. Aly SM, Ahmed YA-G, Ghareeb AA-A, Mohamed MF. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol. 2008;25: 128–136. doi: 10.1016/j.fsi.2008.03.013 18450477

9. Aly SM, Mohamed MF, John G. Effect of probiotics on the survival, growth and challenge infection in tilapia nilotica (Oreochromis niloticus). Aquac Res. 2008;39: 647–656.

10. Geng X, Dong XH, Tan BP, Yang QH, Chi SY, Liu HY, et al. Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish Shellfish Immunol. 2011;31: 400–406. doi: 10.1016/j.fsi.2011.06.006 21693191

11. Panigrahi A, Kiron V, Satoh S, Hirono I, Kobayashi T, Sugita H, et al. Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Dev Comp Immunol. 2007;31: 372–382. doi: 10.1016/j.dci.2006.07.004 17045337

12. Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, et al. Probiotic Pediococcus acidilactici modulates both localised intestinal- and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2013;35: 1097–1104. doi: 10.1016/j.fsi.2013.07.018 23871840

13. Selim KM, Reda RM. Improvement of immunity and disease resistance in the nile tilapia, Oreochromis niloticus, by dietary supplementation with Bacillus amyloliquefaciens. Fish Shellfish Immunol. 2015;44: 496–503. doi: 10.1016/j.fsi.2015.03.004 25783002

14. Iwashita MK, Nakandakare IB, Terhune JS, Wood T, Ranzani-Paiva MJ. Dietary supplementation with Bacillus subtilis, Saccharomyces cerevisiae and Aspergillus oryzae enhance immunity and disease resistance against Aeromonas hydrophila and Streptococcus iniae infection in juvenile tilapia Oreochromis niloticus. Fish Shellfish Immunol. 2015;43: 60–66. doi: 10.1016/j.fsi.2014.12.008 25530581

15. Zhao X, Guo Y, Liu H, Gao J, Nie W. Clostridium butyricum reduce lipogenesis through bacterial wall components and butyrate. Appl Microbiol Biotechnol. 2014;98: 7549–7557. doi: 10.1007/s00253-014-5829-x 24878750

16. Kong Q, He GQ, Jia JL, Zhu QL, Ruan H. Oral administration of Clostridium butyricum for modulating gastrointestinal microflora in mice. Curr Microbiol. 2011;62: 512–517. doi: 10.1007/s00284-010-9737-8 20711781

17. Gao Q, Qi L, Wu T, Xia T, Wang J. Immunomodulatory effects of Clostridium butyricum on human enterocyte-like HT-29 cells. Anim Cells Syst. 2013;17: 121–126.

18. Pan X, Wu T, Song Z, Tang H, Zhao Z. Immune responses and enhanced disease resistance in Chinese drum, Miichthys miiuy (Basilewsky), after oral administration of live or dead cells of Clostridium butyrium CB2. J Fish Dis. 2008;31: 679–686. doi: 10.1111/j.1365-2761.2008.00955.x 18786030

19. Li H, Tian X, Zhao K, Jiang W, Dong S. Effect of Clostridium butyricum in different forms on growth performance, disease resistance, expression of genes involved in immune responses and mTOR signaling pathway of Litopenaeus vannamai. Fish Shellfish Immunol. 2019;87: 13–21. doi: 10.1016/j.fsi.2018.12.069 30599253

20. Li H-D, Tian X-L, Dong S-L. Growth performance, non-specific immunity, intestinal histology and disease resistance of Litopenaeus vannamei fed on a diet supplemented with live cells of Clostridium butyricum. Aquaculture. 2019;498: 470–481.

21. Sakai M, Yoshida T, Atsuta S, Kobayashi M. Enhancement of resistance to vibriosis in rainbow trout, Oncorhynchus mykiss (Walbaum), by oral administration of Clostridium butyricum bacterin. J Fish Dis. 1995;18: 187–190.

22. Li T, Ke F, Gui J-F, Zhou L, Zhang X-J, Zhang Q-Y. Protective effect of Clostridium butyricum against Carassius auratus herpesvirus in gibel carp. Aquac Int. 2019;27: 905–914.

23. Hai NV. Research findings from the use of probiotics in tilapia aquaculture: a review. Fish Shellfish Immunol. 2015;45: 592–597. doi: 10.1016/j.fsi.2015.05.026 26003738

24. Wu P, Jiang J, Liu Y, Hu K, Jiang WD, Li SH, et al. Dietary choline modulates immune responses, and gene expressions of TOR and eIF4E-binding protein2 in immune organs of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol. 2013;35: 697–706. doi: 10.1016/j.fsi.2013.05.030 23774323

25. Wen LM, Jiang WD, Liu Y, Wu P, Zhao J, Jiang J, et al. Evaluation the effect of thiamin deficiency on intestinal immunity of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2015;46: 501–515. doi: 10.1016/j.fsi.2015.07.001 26159094

26. Wang B, Feng L, Chen GF, Jiang WD, Liu Y, Kuang SY, et al. Jian carp (Cyprinus carpio var. Jian) intestinal immune responses, antioxidant status and tight junction protein mRNA expression are modulated via Nrf2 and PKC in response to dietary arginine deficiency. Fish Shellfish Immunol. 2016;51: 116–124. doi: 10.1016/j.fsi.2015.10.032 26518504

27. Perez-Sanchez T, Balcazar JL, Merrifield DL, Carnevali O, Gioacchini G, de Blas I, et al. Expression of immune-related genes in rainbow trout (Oncorhynchus mykiss) induced by probiotic bacteria during Lactococcus garvieae infection. Fish Shellfish Immunol. 2011;31: 196–201. doi: 10.1016/j.fsi.2011.05.005 21620974

28. Sun Y-Z, Xia H-Q, Yang H-L, Wang Y-L, Zou W-C. TLR2 signaling may play a key role in the probiotic modulation of intestinal microbiota in grouper Epinephelus coioides. Aquaculture. 2014;430: 50–56.

29. He S, Zhang Y, Xu L, Yang Y, Marubashi T, Zhou Z, et al. Effects of dietary Bacillus subtilis C-3102 on the production, intestinal cytokine expression and autochthonous bacteria of hybrid tilapia Oreochromis niloticus ♀×Oreochromis aureus ♂. Aquaculture. 2013;412–413: 125–130.

30. Gao Q, Qi L, Wu T, Wang J. Clostridium butyricum activates TLR2-mediated MyD88-independent signaling pathway in HT-29 cells. Mol Cell Biochem. 2012;361: 31–37. doi: 10.1007/s11010-011-1084-y 21956671

31. Gao Q, Qi L, Wu T, Wang J. An important role of interleukin-10 in counteracting excessive immune response in HT-29 cells exposed to Clostridium butyricum. BMC Microbiol. 2012;12: 100. doi: 10.1186/1471-2180-12-100 22681958

32. Sui SJ, Tian ZB, Wang QC, Chen R, Nie J, Li JS, et al. Clostridium butyricum promotes intestinal motility by regulation of TLR2 in interstitial cells of Cajal. Eur Rev Med Pharmacol Sci. 2018;22: 4730–4738. doi: 10.26355/eurrev_201807_15533 30058712

33. Kanai T, Mikami Y, Hayashi A. A breakthrough in probiotics: Clostridium butyricum regulates gut homeostasis and anti-inflammatory response in inflammatory bowel disease. J Gastroenterol. 2015;50: 928–939. doi: 10.1007/s00535-015-1084-x 25940150

34. Liu L, Zeng D, Yang M, Wen B, Lai J, Zhou Y, et al. Probiotic Clostridium butyricum improves the growth performance, immune function, and gut microbiota of weaning rex rabbits. Probiotics Antimicrob Proteins. 2018. doi: 10.1007/s12602-018-9476-x 30324399

35. Li L, Feng L, Jiang WD, Jiang J, Wu P, Kuang SY, et al. Dietary pantothenic acid deficiency and excess depress the growth, intestinal mucosal immune and physical functions by regulating NF-kappaB, TOR, Nrf2 and MLCK signaling pathways in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2015;45: 399–413. doi: 10.1016/j.fsi.2015.04.030 25957886

36. Ruan Z, Liu S, Zhou Y, Mi S, Liu G, Wu X, et al. Chlorogenic acid decreases intestinal permeability and increases expression of intestinal tight junction proteins in weaned rats challenged with LPS. PLoS One. 2014;9: e97815. doi: 10.1371/journal.pone.0097815 24887396

37. Gong Y, Li H, Li Y. Effects of Bacillus subtilis on epithelial tight junctions of mice with inflammatory bowel disease. J Interferon Cytokine Res. 2016;36: 75–85. doi: 10.1089/jir.2015.0030 26720180

38. Anderson RC, Cookson AL, McNabb WC, Park Z, McCann MJ, Kelly WJ, et al. Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol. 2010;10: 316. doi: 10.1186/1471-2180-10-316 21143932

39. Zhang L, Zhang L, Zhan X, Zeng X, Zhou L, Cao G, et al. Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J Anim Sci Biotechnol. 2016;7: 3. doi: 10.1186/s40104-016-0061-4 26819705

40. Li HH, Li YP, Zhu Q, Qiao JY, Wang WJ. Dietary supplementation with Clostridium butyricum helps to improve the intestinal barrier function of weaned piglets challenged with enterotoxigenic Escherichia coli K88. J Appl Microbiol. 2018;125: 964–975. doi: 10.1111/jam.13936 29851202

41. Duan Y, Zhang Y, Dong H, Wang Y, Zhang J. Effect of the dietary probiotic Clostridium butyricum on growth, intestine antioxidant capacity and resistance to high temperature stress in kuruma shrimp Marsupenaeus japonicus. J Therm Biol. 2017;66: 93–100. doi: 10.1016/j.jtherbio.2017.04.004 28477915

42. Duan Y, Zhang Y, Dong H, Wang Y, Zheng X, Zhang J. Effect of dietary Clostridium butyricum on growth, intestine health status and resistance to ammonia stress in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol. 2017;65: 25–33. doi: 10.1016/j.fsi.2017.03.048 28359948

43. Li H, Gong Y, Xie Y, Sun Q, Li Y. Clostridium butyricum protects the epithelial barrier by maintaining tight junction protein expression and regulating microflora in a murine model of dextran sodium sulfate-induced colitis. Scand J Gastroenterol. 2018;53: 1031–1042. doi: 10.1080/00365521.2016.1192678 30141701

44. Hagihara M, Yamashita R, Matsumoto A, Mori T, Inagaki T, Nonogaki T, et al. The impact of probiotic Clostridium butyricum MIYAIRI 588 on murine gut metabolic alterations. J Infect Chemother. 2019;25: 571–577. doi: 10.1016/j.jiac.2019.02.008 31101528

45. Gao Q, Xiao Y, Sun P, Peng S, Yin F, Ma X, et al. In vitro protective efficacy of Clostridium butyricum against fish pathogen infections. Indian J Microbiol. 2013;53: 453–459. doi: 10.1007/s12088-013-0394-z 24426150

46. Pan X, Wu T, Zhang L, Song Z, Tang H, Zhao Z. In vitro evaluation on adherence and antimicrobial properties of a candidate probiotic Clostridium butyricum CB2 for farmed fish. J Appl Microbiol. 2008;105: 1623–1629. doi: 10.1111/j.1365-2672.2008.03885.x 18795975

47. Duan Y, Wang Y, Dong H, Ding X, Liu Q, Li H, et al. Changes in the intestine microbial, digestive, and immune-related genes of litopenaeus vannamei in response to dietary probiotic Clostridium butyricum supplementation. Front Microbiol. 2018;9: 2191. doi: 10.3389/fmicb.2018.02191 30283419

48. Zhang L, Cao GT, Zeng XF, Zhou L, Ferket PR, Xiao YP, et al. Effects of Clostridium butyricum on growth performance, immune function, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poult Sci. 2014;93: 46–53. doi: 10.3382/ps.2013-03412 24570422

49. Yang CM, Cao GT, Ferket PR, Liu TT, Zhou L, Zhang L, et al. Effects of probiotic, Clostridium butyricum, on growth performance, immune function, and cecal microflora in broiler chickens. Poult Sci. 2012;91: 2121–2129. doi: 10.3382/ps.2011-02131 22912445

50. Zhan HQ, Dong XY, Li LL, Zheng YX, Gong YJ, Zou XT. Effects of dietary supplementation with Clostridium butyricum on laying performance, egg quality, serum parameters, and cecal microflora of laying hens in the late phase of production. Poult Sci. 2019;98: 896–903. doi: 10.3382/ps/pey436 30285187

51. Lin Y-H, Ku C-Y, Shiau S-Y. Estimation of dietary magnesium requirements of juvenile tilapia, Oreochromis niloticus×Oreochromis aureus, reared in freshwater and seawater. Aquaculture. 2013;380–383: 47–51.

52. Shiau SY, Lo PS. Dietary choline requirements of juvenile hybrid tilapia, Oreochromis niloticus x O. aureus. J Nutr. 2000;130: 100–103. doi: 10.1093/jn/130.1.100 10613774

53. Zhou P, Wang M, Xie F, Deng D-F, Zhou Q. Effects of dietary carbohydrate to lipid ratios on growth performance, digestive enzyme and hepatic carbohydrate metabolic enzyme activities of large yellow croaker (Larmichthys crocea). Aquaculture. 2016;452: 45–51.

54. Hoseinifar SH, Mirvaghefi A, Amoozegar MA, Sharifian M, Esteban MA. Modulation of innate immune response, mucosal parameters and disease resistance in rainbow trout (Oncorhynchus mykiss) upon synbiotic feeding. Fish Shellfish Immunol. 2015;45: 27–32. doi: 10.1016/j.fsi.2015.03.029 25827628

55. Bayha KM, Ortell N, Ryan CN, Griffitt KJ, Krasnec M, Sena J, et al. Crude oil impairs immune function and increases susceptibility to pathogenic bacteria in southern flounder. PLoS One. 2017;12: e0176559. doi: 10.1371/journal.pone.0176559 28464028

56. Li W, Zhang X, Song W, Deng B, Liang Q, Fu L, et al. Effects of Bacillus preparations on immunity and antioxidant activities in grass carp (Ctenopharyngodon idellus). Fish Physiol Biochem. 2012;38: 1585–1592. doi: 10.1007/s10695-012-9652-y 22585415

57. Lei K, Li YL, Yu DY, Rajput IR, Li WF. Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poult Sci. 2013;92: 2389–2395. doi: 10.3382/ps.2012-02686 23960122

58. Sun YZ, Yang HL, Ma RL, Lin WY. Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immunol. 2010;29: 803–809. doi: 10.1016/j.fsi.2010.07.018 20637875

59. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25: 402–408. doi: 10.1006/meth.2001.1262 11846609

60. Zhao J, Liu Y, Jiang J, Wu P, Chen G, Jiang W, et al. Effects of dietary isoleucine on growth, the digestion and absorption capacity and gene expression in hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture. 2012;368–369: 117–128.

61. Wang J, Xu H, Zuo R, Mai K, Xu W, Ai Q. Effects of oxidised dietary fish oil and high-dose vitamin E supplementation on growth performance, feed utilisation and antioxidant defence enzyme activities of juvenile large yellow croaker (Larmichthys crocea). Br J Nutr. 2016;115: 1531–1538. doi: 10.1017/S0007114516000398 26948923

62. Liao XD, Ma G, Cai J, Fu Y, Yan XY, Wei XB, et al. Effects of Clostridium butyricum on growth performance, antioxidation, and immune function of broilers. Poult Sci. 2015;94: 662–667. doi: 10.3382/ps/pev038 25717087

63. Duan Y, Zhang J, Huang J, Jiang S. Effects of dietary Clostridium butyricum on the growth, digestive enzyme activity, antioxidant capacity, and resistance to nitrite stress of Penaeus monodon. Probiotics Antimicrob Proteins. 2019;11: 938–945. doi: 10.1007/s12602-018-9421-z 29858778

64. Sumon MS, Ahmmed F, Khushi SS, Ahmmed MK, Rouf MA, Chisty MAH, et al. Growth performance, digestive enzyme activity and immune response of Macrobrachium rosenbergii fed with probiotic Clostridium butyricum incorporated diets. J King Saud Univ Sci. 2018;30: 21–28.

65. Song ZF, Wu TX, Cai LS, Zhang LJ, Zheng XD. Effects of dietary supplementation with Clostridium butyricum on the growth performance and humoral immune response in Miichthys miiuy. J Zhejiang Univ Sci B. 2006;7: 596–602. doi: 10.1631/jzus.2006.B0596 16773736

66. Gao Q, Xiao C, Min M, Zhang C, Peng S, Shi Z. Effects of probiotics dietary supplementation on growth performance, innate immunity and digestive enzymes of silver pomfret, Pampus argenteus. Indian J Anim Res. 2016;50: 936–941.

67. Xu HJ, Jiang WD, Feng L, Liu Y, Wu P, Jiang J, et al. Dietary vitamin C deficiency depresses the growth, head kidney and spleen immunity and structural integrity by regulating NF-kappaB, TOR, Nrf2, apoptosis and MLCK signaling in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2016;52: 111–138. doi: 10.1016/j.fsi.2016.02.033 26944716

68. Wei Z, Yi L, Xu W, Zhou H, Zhang Y, Zhang W, et al. Effects of dietary nucleotides on growth, non-specific immune response and disease resistance of sea cucumber Apostichopus japonicas. Fish Shellfish Immunol. 2015;47: 1–6. doi: 10.1016/j.fsi.2015.08.017 26299704

69. Zhou Q, Wang L, Wang H, Xie F, Wang T. Effect of dietary vitamin C on the growth performance and innate immunity of juvenile cobia (Rachycentron canadum). Fish Shellfish Immunol. 2012;32: 969–975. doi: 10.1016/j.fsi.2012.01.024 22366311

70. Zhao J, Liu Y, Jiang J, Wu P, Jiang W, Li S, et al. Effects of dietary isoleucine on the immune response, antioxidant status and gene expression in the head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol. 2013;35: 572–580. doi: 10.1016/j.fsi.2013.05.027 23742869

71. Neissi A, Rafiee G, Nematollahi M, Razavi SH, Maniei F. Influence of supplemented diet with Pediococcus acidilactici on non-specific immunity and stress indicators in green terror (Aequidens rivulatus) during hypoxia. Fish Shellfish Immunol. 2015;45: 13–18. doi: 10.1016/j.fsi.2015.04.008 25891275

72. Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, et al. Modulation of intestinal morphology and immunity in nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci. 2011;91: e92–e97. doi: 10.1016/j.rvsc.2011.02.014 21536310

73. Wang Y-B, Tian Z-Q, Yao J-T, Li W-F. Effect of probiotics, Enteroccus faecium, on tilapia (Oreochromis niloticus) growth performance and immune response. Aquaculture. 2008;277: 203–207.

74. Sun YZ, Yang HL, Ma RL, Song K, Li JS. Effect of Lactococcus lactis and Enterococcus faecium on growth performance, digestive enzymes and immune response of grouper Epinephelus coioides. Aquac Nutr. 2012;18: 281–289.

75. Wang J, Qi L, Mei L, Wu Z, Wang H. C. butyricum lipoteichoic acid inhibits the inflammatory response and apoptosis in HT-29 cells induced by S. aureus lipoteichoic acid. Int J Biol Macromol. 2016;88: 81–87. doi: 10.1016/j.ijbiomac.2016.03.054 27020942

76. Villeger R, Saad N, Grenier K, Falourd X, Foucat L, Urdaci MC, et al. Characterization of lipoteichoic acid structures from three probiotic Bacillus strains: involvement of D-alanine in their biological activity. Antonie Van Leeuwenhoek. 2014;106: 693–706. doi: 10.1007/s10482-014-0239-8 25090957

77. Monefeldt K, Helgeland K, Tollefsen T. In vitro activation of the classical pathway of complement by a streptococcal lipoteichoic acid. Oral Microbiol Immunol. 1994;9: 70–76. 8008432

78. Biller-Takahashi JD, Takahashi LS, Mingatto FE, Urbinati EC. The immune system is limited by oxidative stress: dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish Shellfish Immunol. 2015;47: 360–367. doi: 10.1016/j.fsi.2015.09.022 26370542

79. Duan GL, Wang CN, Liu YJ, Yu Q, Tang XL, Ni X, et al. Resveratrol alleviates endotoxemia-associated adrenal insufficiency by suppressing oxidative/nitrative stress. Endocr J. 2016;63: 569–580. doi: 10.1507/endocrj.EJ15-0610 27052214

80. Wang FY, Liu JM, Luo HH, Liu AH, Jiang Y. Potential protective effects of Clostridium butyricum on experimental gastric ulcers in mice. World J Gastroenterol. 2015;21: 8340–8351. doi: 10.3748/wjg.v21.i27.8340 26217085

81. He R-P, Feng J, Tian X-L, Dong S-L, Wen B. Effects of dietary supplementation of probiotics on the growth, activities of digestive and non-specific immune enzymes in hybrid grouper (Epinephelus lanceolatus ♂ × Epinephelus fuscoguttatus ♀). Aquac Res. 2017;48: 5782–5790.

82. Zhang B, Yang X, Guo Y, Long F. Effects of dietary lipids and Clostridium butyricum on the performance and the digestive tract of broiler chickens. Arch Anim Nutr. 2011;65: 329–339. 21888038

83. Nakanishi S, Kataoka K, Kuwahara T, Ohnishi Y. Effects of high amylose maize starch and Clostridium butyricum on metabolism in colonic microbiota and formation of azoxymethane-induced aberrant crypt foci in the rat colon. Microbiol Immunol. 2003;47: 951–958. doi: 10.1111/j.1348-0421.2003.tb03469.x 14695445

84. Dan J, Fang Z, Chin SX, Tian XF, Su TC. Biohydrogen production from hydrolysates of selected tropical biomass wastes with Clostridium butyricum. Sci Rep. 2016;6: 27205. doi: 10.1038/srep27205 27251222

85. Rosignoli P, Fabiani R, De Bartolomeo A, Spinozzi F, Agea E, Pelli MA, et al. Protective activity of butyrate on hydrogen peroxide-induced DNA damage in isolated human colonocytes and HT29 tumour cells. Carcinogenesis. 2001;22: 1675–1680. doi: 10.1093/carcin/22.10.1675 11577008

86. Courtois F, Seidman EG, Delvin E, Asselin C, Bernotti S, Ledoux M, et al. Membrane peroxidation by lipopolysaccharide and iron-ascorbate adversely affects Caco-2 cell function: beneficial role of butyric acid. Am J Clin Nutr. 2003;77: 744–750. doi: 10.1093/ajcn/77.3.744 12600871

87. Zhou HX, Han B, Hou LM, An TT, Jia G, Cheng ZX, et al. Protective effects of hydrogen gas on experimental acute pancreatitis. PLoS One. 2016;11: e0154483. doi: 10.1371/journal.pone.0154483 27115738

88. Zhao J, Feng L, Liu Y, Jiang W, Wu P, Jiang J, et al. Effect of dietary isoleucine on the immunity, antioxidant status, tight junctions and microflora in the intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol. 2014;41: 663–673. doi: 10.1016/j.fsi.2014.10.002 25451003

89. Liu W, Yang Y, Zhang J, Gatlin DM, Ringo E, Zhou Z. Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidised oil. Br J Nutr. 2014;112: 15–29. doi: 10.1017/S0007114514000610 24774835

90. Alva-Murillo N, Medina-Estrada I, Baez-Magana M, Ochoa-Zarzosa A, Lopez-Meza JE. The activation of the TLR2/p38 pathway by sodium butyrate in bovine mammary epithelial cells is involved in the reduction of Staphylococcus aureus internalization. Mol Immunol. 2015;68: 445–455. doi: 10.1016/j.molimm.2015.09.025 26471700

91. Kim TW, Staschke K, Bulek K, Yao J, Peters K, Oh KH, et al. A critical role for IRAK4 kinase activity in toll-like receptor-mediated innate immunity. J Exp Med. 2007;204: 1025–1036. doi: 10.1084/jem.20061825 17470642

92. Rashidi N, Mirahmadian M, Jeddi-Tehrani M, Rezania S, Ghasemi J, Kazemnejad S, et al. Lipopolysaccharide- and lipoteichoic acid-mediated pro-inflammatory cytokine production and modulation of TLR2, TLR4 and MyD88 expression in human endometrial cells. J Reprod Infertil. 2015;16: 72–81. 25927023

93. Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13: 321–335. doi: 10.1038/nri3430 23618829

94. Molloy MJ, Bouladoux N, Belkaid Y. Intestinal microbiota: shaping local and systemic immune responses. Semin Immunol. 2012;24: 58–66. doi: 10.1016/j.smim.2011.11.008 22178452

95. Nowak P, Troseid M, Avershina E, Barqasho B, Neogi U, Holm K, et al. Gut microbiota diversity predicts immune status in HIV-1 infection. AIDS. 2015;29: 2409–2418. doi: 10.1097/QAD.0000000000000869 26355675

96. Standen BT, Rodiles A, Peggs DL, Davies SJ, Santos GA, Merrifield DL. Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Appl Microbiol Biotechnol. 2015;99: 8403–8417. doi: 10.1007/s00253-015-6702-2 26115752

97. Zhai Q, Yu L, Li T, Zhu J, Zhang C, Zhao J, et al. Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie Van Leeuwenhoek. 2017;110: 501–513. doi: 10.1007/s10482-016-0819-x 28028640

98. Ferguson RM, Merrifield DL, Harper GM, Rawling MD, Mustafa S, Picchietti S, et al. The effect of Pediococcus acidilactici on the gut microbiota and immune status of on-growing red tilapia (Oreochromis niloticus). J Appl Microbiol. 2010;109: 851–862. doi: 10.1111/j.1365-2672.2010.04713.x 20353430

99. Zhang Z, Li D, Refaey MM, Xu W. High spatial and temporal variations of microbial community along the southern Catfish gastrointestinal tract: insights into dynamic food digestion. Front Microbiol. 2017;8: 1531. doi: 10.3389/fmicb.2017.01531 28848535

100. She R, Li TT, Luo D, Li JB, Yin LY, Li H, et al. Changes in the intestinal microbiota of gibel carp (Carassius gibelio) associated with Cyprinid herpesvirus 2 (CyHV-2) infection. Curr Microbiol. 2017;74: 1130–1136. doi: 10.1007/s00284-017-1294-y 28748273

101. Larsen AM, Mohammed HH, Arias CR. Characterization of the gut microbiota of three commercially valuable warmwater fish species. J Appl Microbiol. 2014;116: 1396–1404. doi: 10.1111/jam.12475 24529218

102. Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X. Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb Ecol. 2015;69: 25–36. doi: 10.1007/s00248-014-0480-8 25145494

103. Tsuchiya C, Sakata T, Sugita H. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol. 2008;46: 43–48. doi: 10.1111/j.1472-765X.2007.02258.x 17944860

104. Liu Y, Yao Y, Li H, Qiao F, Wu J, Du ZY, et al. Influence of endogenous and exogenous estrogenic endocrine on intestinal microbiota in Zebrafish. PLoS One. 2016;11: e0163895. doi: 10.1371/journal.pone.0163895 27701432

105. Gainza O, Ramirez C, Ramos AS, Romero J. Intestinal microbiota of white shrimp Penaeus vannamei under intensive cultivation conditions in ecuador. Microb Ecol. 2018;75: 562–568. doi: 10.1007/s00248-017-1066-z 28929202

106. Zhang M, Sun Y, Chen L, Cai C, Qiao F, Du Z, et al. Symbiotic bacteria in gills and guts of Chinese mitten crab (Eriocheir sinensis) differ from the free-living bacteria in water. PLoS One. 2016;11: e0148135. doi: 10.1371/journal.pone.0148135 26820139

107. van der Marel M, Schroers V, Neuhaus H, Steinhagen D. Chemotaxis towards, adhesion to, and growth in carp gut mucus of two Aeromonas hydrophila strains with different pathogenicity for common carp, Cyprinus carpio L. J Fish Dis. 2008;31: 321–330. doi: 10.1111/j.1365-2761.2008.00902.x 18355183

108. Harikrishnan R, Balasundaram C. Modern trends in Aeromonas hydrophila disease management with fish. Reviews in Fisheries Science. 2005;13: 281–320.

109. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53: 685–693. doi: 10.1136/gut.2003.025403 15082587

110. Sun J, Wang F, Ling Z, Yu X, Chen W, Li H, et al. Clostridium butyricum attenuates cerebral ischemia/reperfusion injury in diabetic mice via modulation of gut microbiota. Brain Res. 2016;1642: 180–188. doi: 10.1016/j.brainres.2016.03.042 27037183

111. Konstantinov SR, Favier CF, Zhu WY, Williams BA, Klüß J, Souffrant W, et al. Microbial diversity studies of the porcine gastrointestinal ecosystem during weaning transition. Anim Res. 2004;53: 317–324.

112. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81: 1031–1064. doi: 10.1152/physrev.2001.81.3.1031 11427691

113. Fang CL, Sun H, Wu J, Niu HH, Feng J. Effects of sodium butyrate on growth performance, haematological and immunological characteristics of weanling piglets. J Anim Physiol Anim Nutr (Berl). 2014;98: 680–685.

114. Jiang WD, Tang RJ, Liu Y, Kuang SY, Jiang J, Wu P, et al. Manganese deficiency or excess caused the depression of intestinal immunity, induction of inflammation and dysfunction of the intestinal physical barrier, as regulated by NF-kappaB, TOR and Nrf2 signalling, in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2015;46: 406–416. doi: 10.1016/j.fsi.2015.06.007 26072140

115. Nebot-Vivinus M, Harkat C, Bzioueche H, Cartier C, Plichon-Dainese R, Moussa L, et al. Multispecies probiotic protects gut barrier function in experimental models. World J Gastroenterol. 2014;20: 6832–6843. doi: 10.3748/wjg.v20.i22.6832 24944474


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2019 Číslo 12