Effects on intestinal microbiota and immune genes of Solea senegalensis after suspension of the administration of Shewanella putrefaciens Pdp11

Fish and Shellfish Immunology

Volumn 58, Issue , 2016, Pages 274-283

  Vidal, Sara ^a   Tapia Paniagua, Silvana Teresa ^a   Moriñigo, Jesús Miguel ^a   Lobo, Carmen ^b   García de la Banda, Inés ^b   Balebona, María del Carmen ^a   Moriñigo, Miguel Ángel ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b Centro Oceanográfico de Santander   (Spain)

Author keywords

Alginate; DGGE; Real time PCR; Shewanella putrefaciens Pdp11; Solea senegalensis

Indexed keywords

ALGINIC ACID; FISH PROTEIN; GLUCURONIC ACID; HEXURONIC ACID; PREBIOTIC AGENT; PROBIOTIC AGENT;

ANALYSIS; ANIMAL; ANIMAL FOOD; DIET; DRUG EFFECTS; FLATFISH; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; SHEWANELLA PUTREFACIENS; VETERINARY;

ALGINATES; ANIMAL FEED; ANIMALS; DIET; FISH PROTEINS; FLATFISHES; GASTROINTESTINAL MICROBIOME; GLUCURONIC ACID; HEXURONIC ACIDS; IMMUNITY, INNATE; OXIDATIVE STRESS; PREBIOTICS; PROBIOTICS; SHEWANELLA PUTREFACIENS; TRANSCRIPTION, GENETIC;

EID: 84988838386     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2016.09.010     Document Type: Article

References (66)

1. [1] Heuer, O.E., Kruse, H., Grave, K., Collignon, P., Karunasagar, I., Angulo, J., Human health consequences of use of antimicrobial agents in aquaculture. Clin. Infect. Dis. 49 (2009), 1248–1253.
2. [2] Dimitroglou, A., Merrifield, D.L., Carnevali, O., Pichietti, S., Avella, M., Daniels, C., Güroy, D., Davies, S.J., Microbial manipulations to improve fish health and production- A Mediterranean perspective. Fish. Shellfish Immunol. 30 (2011), 1–16.
3. [3] Merrifield, D.L., Dimitroglou, A., Foey, A., Davies, S.J., Baker, R.T.M., Bøgwald, J., Castex, M., Ringø, E., The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302 (2010), 1–18.
4. [4] Pérez-Sánchez, T., Ruiz-Zarzuela, I., de Blas, I., Balcázar, J.L., Probiotics in aquaculture: a current assessment. Rev. Aquacult 5 (2013), 1–14.
5. [5] Bidhan, C.B.C., Meena, D.K., Behera, B.K., Das, P., Mohapatra, P.K., Sharma, A.P., Probiotics in fish and shellfish culture: immunomodulatory and ecophysiological responses. Fish. Physiol. Biochem. 40 (2014), 921–971.
6. [6] Dos Santos, L.E., De Araújo, E.A., Da Conceição, L.L., De Moraes, C.A., De Carvalho, A.F., Survival of Lactobacillus delbrueckii UFV H2b20 in ice cream produced with different fat levels and after submission to stress acid and bile salts. J. Funct. Foods 5 (2013), 503–507.
7. [7] Todorov, S.D., Leblanc, J.G., Franco, B.D.G.M., Evaluation of the probiotic potential and effect of encapsulation on survival for Lactobacillus plantarum ST16Pa isolated from papaya. World J. Microbiol. Biotechnol. 28 (2012), 973–984.
8. [8] Peso-Echarri, P., Frontela-Saseta, C., González-Bermúdez, C.A., Ros-Berruezo, G.F., Martínez-Graciá, C., Polisacáridos de algas como ingredientes funcionales en acuicultura marina: alginato, carragenato y ulvano. Rev. Biol. Mar. Oceanogr. 47 (2012), 373–381.
9. [9] Sáenz de Rodrigáñez, M.A., Díaz-Rosales, P., Chabrillóon, M., Smidt, H., Arijo, S., León-Rubio, J.M., Alarcón, F.J., Balebona, M.C., Moriñigo, M.A., Cara, J.B., Moyano, F.J., Effect of dietary administration of probiotics on growth and intestine functionality of juvenile Senegalese sole (Solea senegalensis, Kaup 1858). Aquacult. Nutr. 15 (2009), 177–185.
10. [10] Tapia-Paniagua, S.T., Chabrillón, M., Díaz-Rosales, P., García de la Banda, I., Lobo, C., Clavijo, E., Balebona, M.C., Moriñigo, M.A., Intestinal microbiota diversity of the flat fish Solea senegalensis (Kaup, 1858) following probiotic administration. Microbiol. Ecol. 60 (2010), 310–319.
11. [11] Tapia-Paniagua, S.T., Díaz-Rosales, P., León-Rubio, J.M., García de la Banda, I., Lobo, C., Alarcón, F.J., Chabrillón, M., Rosas-Ledesma, P., Varela, J.L., Ruiz-Járabo, I., Arijo, S., Esteban, M.A., Martínez Manazanares, E., Mancera, J.M., Balebona, M.C., Moriñigo, M.A., Use of the probiotic Shewanella putrefaciens Pdp11 on the culture of Senegalese sole (Solea senegalensis, Kaup 1858) and gilthead seabream (Sparus aurata L.). Aquacult. Int. 20 (2012), 1025–1039.
12. [12] Cordero, H., Guardiola, F., Tapia-Paniagua, S.T., Cuesta, A., Meseguer, J., Balebona, M.C., Moriñigo, M.A., Esteban, M.A., Modulation of immunity and gut microbiota after dietary administration of alginate encapsulated Shewanella putrefaciens Pdp11 to gilthead seabream (Sparus aurata L). Fish. Shellfish Immunol. 45 (2015), 608–618.
13. [13] Díaz-Rosales, P., Arijo, S., Chabrillón, M., Alarcón, F.J., Tapia-Paniagua, S.T., Martínez-Manzanares, E., Balebona, M.C., Moriñigo, M.A., Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Solea senegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 293 (2009), 16–21.
14. [14] Bricknell, I., Dalmo, R.A., The use of immunostimulants in fish larval aquaculture. Fish. Shellfish Immunol. 19 (2005), 457–472.
15. [15] Tapia-Paniagua, S.T., Vidal, S., Lobo, C., Prieto-Alamo, M.J., Jurado, J., Cordero, H., Cerezuela, R., García de la Banda, I., Esteban, M.A., Balebona, M.C., Moriñigo, M.A., The treatment with the probiotic Shewanella putrefaciens Pdp11 of specimens of Solea senegalensis exposed to high stocking densities to enhance their resistance to disease. Fish. Shellfish Immunol. 41 (2014), 209–221.
16. [16] Tapia-Paniagua, S.T., Vidal, S., Lobo, C., García de la Banda, I., Esteban, M.A., Balebona, M.C., Moriñigo, M.A., Dietary administration of the probiotic SpPdp11: effects on the intestinal microbiota and immune-related gene expression of farmed Solea senegalensis treated with oxytetracycline. Fish. Shellfish Immunol. 46 (2015), 449–458.
17. [17] Roselers, G., Mittge, E., Stephens, W.Z., Parichy, D., Cavanaugh, C.M., Guillermin, K., Rawls, J.F., Evidence for a core gut microbiota in the zebrafish. ISME J. 5 (2011), 1595–1608.
18. [18] Harrison, O.J., Maloy, K.J., Innate immune activation in intestinal homeostasis. J. Innate Immun. 3 (2011), 585–593.
19. [19] Moffitt, C.S., Mobin, M.A., Profile of microflora of the posterior intestine of Chinook salmon before, during, and after administration of rations with and without erythromycin. N. Am. J. Aquacult 68 (2006), 176–185.
20. [20] Nayak, S.K., Role of gastrointestinal microbiota in fish. Aquacult. Res. 41 (2010), 1553–1573.
21. [21] Pérez, T., Balcázar, J.L., Ruiz-Zarzuela, I., Halaihel, N., Vendrell, D., de Blas, I., Múzquiz, J.L., Host– microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol. 3 (2010), 355–360.
22. [22] García de La Banda, I., Lobo, C., León-Rubio, J.M., Tapia-Paniagua, S., Balebona, M.C., Moriñigo, M.A., Moreno-Ventas, X., Lucas, L.M., Linares, F., Arce, F., Arijo, S., Influence of two closely related probiotics on juvenile Senegalese sole (Solea senegalensis, Kaup 1858) performance and protection against Photobacterium damselae subsp. piscicida. Aquaculture 306 (2010), 281–288.
23. [23] Martínez, G., Shaw, E.M., Carrillo, M., Zanuy, S., Protein salting-out method applied to genomic DNA isolation from fish whole blood. Biotechniques 24 (1998), 238–239.
24. [24] Muyzer, G., de Waal, E.C., Uitterlinden, A.G., Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes for 16S rRNA. Appl. Environ. Microbiol. 59 (1993), 695–700.
25. [25] Sanguinetti, C.J., Dias-Neto, E., Simpson, A.J.G., Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17 (1994), 914–921.
26. [26] Salas-Leiton, E., Anguis, V., Martín-Antonio, B., Crespo, D., Planas, J.V., Infante, C., Cañavate, J.P., Manchado, M., Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): Potential effects on the immune response. Fish. Shellfish Immunol. 28 (2010), 296–302.
27. [27] Prieto-Álamo, M.J., Abril, N., Osuna-Jiménez, I., Pueyo, C., Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges: large-scale identification by suppression subtractive hybridization and absolute quantification of transcriptional profiles by real-time-PCR. Aquat. Toxicol. 91 (2009), 312–319.
28. [28] Teles, M., MacKenzie, S., Boltana, S., Callol, A., Tort, L., Gene expression and TNF-alpha secretion profile in rainbow trout macrophages following exposures to copper and bacterial lipopolysaccharide. Fish. Shellfish Immunol. 30 (2011), 340–346.
29. [29] Infante, C., Matsuoka, M.P., Asensio, E., Cañavate, J.P., Reith, M., Manchado, M., Selection of housekeeping genes for gene expression studies in larvae from flatfish using real-time PCR. BMC Mol. Biol., 9, 2008, 28.
30. [30] Livak, J.K., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25 (2001), 402–408.
31. [31] Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. J. Mol. Biol. 215 (1990), 403–410.
32. [32] Janczyk, P., Pieper, R., Smidt, H., Souffrant, W.B., Effect of alginate and inulin on intestinal microbial ecology of weanling pigs reared under different husbandry conditions. FEMS Microbiol. Ecol. 72 (2010), 132–142.
33. [33] Wang, Y., Han, F., Hu, B., Li, J., Yu, W., In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutr. Res. 26 (2006), 597–603.
34. [34] Chabrillón, M., Rico, R.M., Arijo, S., Díaz-Rosales, P., Balebona, M.C., Moriñigo, M.A., Interactions of microorganisms isolated from gilthead seabream, Sparus aurata L., on Vibrio harveyi, a pathogen of farmed Senegalese sole, Solea senegalensis (Kaup). J. Fish. Dis. 28 (2005), 531–537.
35. [35] Chabrillón, M., Rico, R.M., Balebona, M.C., Moriñigo, M.A., Adhesion to sole, Solea senegalensis Kaup, mucus of microorganisms isolated from farmed fish, and their interaction with Photobacterium damselae subsp piscicida. J. Fish. Dis. 28 (2005), 229–237.
36. [36] Tapia-Paniagua, S.T., Díaz-Rosales, P., García de la Banda, I., Lobo, C., Clavijo, E., Balebona, M.C., Moriñigo, M.A., Modulation of certain liver fatty acids in Solea senegalensis is influenced by the dietary administration of probiotic microorganisms. Aquaculture 424–425 (2014), 234–238.
37. [37] Lobo, C., Tapia-Paniagua, S.T., Moreno-Ventas, X., Alarcón, F.J., Rodríguez, C., Balebona, M.C., Moriñigo, M.A., García de la Banda, I., Benefits of probiotic administration on growth and performance along metamorphosis and weaning of Senegalese sole (Solea senegalensis). Aquaculture 433 (2014), 183–195.
38. [38] Lobo, C., Moreno-Ventas, X., Tapia-Paniagua, S.T., Rodríguez, C., Moriñigo, M.A., García de la Banda, I., Dietary probiotic supplementation (Shewanella putrefaciens Pdp11) modulates gut microbiota and promotes growth and condition in Senegalese sole larviculture. Fish. Physiol. Biochem. 40 (2014), 295–309.
39. [39] Bagni, M., Romano, N., Finoia, M.G., Abelli, L., Scapigliati, G., Tiscar, P.G., Sarti, M., Marion, G., Short- and long-term effects of a dietary yeast b-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). Fish. Shellfish Immunol. 18 (2005), 311–325.
40. [40] Harikrishnan, R., Kim, M.C., Kim, J.S., Han, Y.J., Jang, I.S., Balasundaram, C., Heo, M.S., Immunomodulatory effect of sodium alginate enriched diet in kelp grouper Epinephelus bruneus against Streptococcus iniae. Fish. Shellfish Immunol. 30 (2011), 543–549.
41. [41] Encinas, P., Rodriguez-Milla, M.A., Novoa, B., Estepa, A., Figueras, A., Coll, J., Zebrafish fill immune responses during high mortality infections with viral haemorrhagic septicemia rhabdovirus. A proteomic and transcriptomic approach. BMC Genomics, 11, 2010, 518.
42. [42] Bossi, F., Rizzi, L., Bulla, R., Debeus, A., Tripodo, C., Picotti, P., Betto, E., Macor, P., Pucillo, C., Würzner, R., Tedesco, F., C7 is expressed on endothelial cells as a trap for the assembling terminal complement complex and may exert anti-inflammatory function. Blood 113 (2009), 3640–3648.
43. [43] Shen, Y., Zhang, J., Xu, X., Fu, J., Li, J., Expression of complement component C7 and involvement in innate immune responses to bacteria in grass carp. Fish. Shellfish Immunol. 33 (2012), 448–454.
44. [44] Larsen, A.N., Solstad, T., Svineng, G., Seppola, M., Jørgensen, T.Ø., Molecular characterization of a goose-type lysozyme gene in Atlantic cod (Gadus morhua L). Fish. Shellfish Immunol. 26 (2009), 122–132.
45. [45] Ye, X., Zhang, L., Tian, Y., Tan, A., Bai, J., Li, S., Identification and expression analysis of the g-type and c-type lysozymes in grass carp Ctenopharyngodon idellus. Dev. Comp. Immunol. 34 (2010), 501–509.
46. [46] Caipang, C.M.A., Brichmann, M.F., Kiron, V., Profiling gene expression in the spleen of Atlantic cod, Gadus morhua, upon vaccination with Vibrio anguillarum antigen. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 153 (2009), 261–267.
47. [47] Peatman, E., Baoprasertkul, P., Terhune, J., Xu, P., Nandi, S., Kucuktas, H., Li, P., Wang, S., Somridhivej, B., Dunham, R., Liu, Z., Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a Gram-negative bacterium. Dev. Comp. Immunol. 31 (2007), 1183–1196.
48. [48] Segal, B.H., Grimm, M.J., Khan, N.H., Han, W., Blackwell, T.S., Regulation of immunity by NADPH oxidase. Free Radic. Biol. Med. 53 (2012), 72–80.
49. [49] De Minicis, S., Brenner, D.A., Oxidative stress in alcoholic liver disease: role of NADPH oxidase complex. J. Gastroenterol. Hepatol. 23 (2008), S98–S103.
50. [50] Paik, Y.H., Brenner, D.A., NADPH oxidase mediated oxidative stress in hepatic fibrogenesis. Korean J. Hepatol. 17 (2011), 251–257.
51. [51] Fujiki, K., Yano, T., Effects of sodium alginate on the non-specific defence system of the common carp (Cyprinus carpio L). Fish. Shellfish Immunol. 7 (1997), 417–427.
52. [52] Cerezuela, R., Guardiola, F.A., González, P., Meseguer, J., Esteban, M.A., Effects of dietary Bacillus subtilis, Tetraselmis chuii, and Phaeodactylum tricornutum, singularly or in combination, on the immune response and disease resistance of sea bream (Sparus aurata). Fish. Shellfish Immunol. 33 (2012), 342–349.
53. [53] Geng, X., Dong, X.H., Tan, B.P., Yang, Q.H., Chi, S.Y., Liu, H.Y., Liu, X.Q., Effects of dietary chitosan and Bacillus subtilis on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Fish. Shellfish Immunol. 31 (2011), 400–406.
54. [54] Geraylou, Z., Souffreau, C., Rurangwa, E., D'Hondt, S., Callewaert, L., Courtin, C.M., Delcour, J.A., Buyse, K., Ollevier, F., Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish. Shellfish Immunol. 33 (2012), 718–724.
55. [55] Schaumburg, F., Hippe, D., Vutova, P., Luder, C.G., Pro- and anti-apoptotic activities of protozoan parasites. Parasitology 132 (2006), S69–S85.
56. [56] Pincemail, J., Bonjean, K., Cayeux, K., Defraigne, J.O., Physiological action of antioxidant defences. Nutr. Clin. Metabol. 16 (2002), 233–239.
57. [57] Apel, K., Hirt, H., Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55 (2004), 373–399.
58. [58] Chiu, S.T., Tsai, R.T., Hsu, J.P., Liu, C.H., Cheng, W., Dietary sodium alginate administration to enhance the nonspecific immune responses, and disease resistance of the juvenile grouper Epinephelus fuscoguttatus. Aquaculture 277 (2008), 66–72.
59. [59] Yeh, S.P., Chang, C.A., Chang, C.Y., Liu, C.H., Cheng, W., Dietary sodium alginate administration affects fingerling growth and resistance to Streptococcus sp. and iridovirus, and juvenile non-specific immune responses of the orange-spotted grouper, Epinephelus coioides. Fish. Shellfish Immunol. 25 (2008), 19–27.
60. [60] Liu, B., Xu, L., Ge, X., Xie, J., Xu, P., Shou, Q., Pan, L., Zhang, Y., Effects of mannan oligosaccharide on the physiological responses, HSP70 gene expression and disease resistance of Allogynogenetic crucian carp (Carassius auratus gibelio) under Aeromonas hydrophila infection. Fish. Shellfish Immunol. 34 (2013), 1395–1403.
61. [61] Musch, M.W., Sugi, K., Strauss, D., Chang, E., Heat shock protein 72 protects against oxidant induced injury of barrier function of human colonic epithelial Caco2/bbe cells. Gastroenterology 117 (1999), 115–122.
62. [62] Sandilands, J., Drynan, K.D., Roberts, R.J., Preliminary studies on the enhancement of storage time of chilled milt of Atlantic salmon, Salmo salar L., using an extender containing the Tex-OE® heat shock-stimulating factor. Aquacult. Res. 41 (2010), 568–571.
63. [63] Guo, S., Wharton, W., Mosely, P., Shi, H., Heat shock protein 70 regulates cellular redox status by modulating glutathione-related enzyme activities. Cell Stress Chaperones 12 (2007), 245–254.
64. [64] Azad, P., Ryu, J., Haddad, G.G., Distinct role of Hsp70 in Drosophila hemocytes during severe hypoxia. Free Radic. Biol. Med. 51 (2011), 530–538.
65. [65] Fromin, N., Hamelin, J., Tarnawski, S., Roesti, D., Jourdain-Miserez, K., Forestier, N., Teyssier-Cuvelle, S., Gillet, F., Aragno, M., Rossi, P., Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ. Microbiol. 4 (2002), 634–643.
66. [66] Tapia-Paniagua, S.T., Lobo, C., Moreno-Ventas, X., García de la Banda, I., Moriñigo, M.A., Balebona, M.C., Probiotic supplementation influences the diversity of the intestinal microbiota during early stages of farmed Senegalese sole (Solea senegalensis, Kaup 1858). Mar. Biotechnol. 16 (2014), 716–728.