Evaluation of Lactococcus lactis HNL12 combined with Schizochytrium limacinum algal meal in diets for humpback grouper (Cromileptes altivelis)

Fish and Shellfish Immunology

Volumn 94, Issue , 2019, Pages 880-888

  Sun, Yun ^a   Xiang, Yajing ^a   He, Mingwang ^a   Zhang, Xiang ^a   Wang, Shifeng ^a   Guo, Weiliang ^a   Liu, Chunsheng ^a   Cao, Zhenjie ^a   Zhou, Yongcan ^a  

^a HAINAN UNIVERSITY   (China)

Author keywords

Cromileptes altivelis; Growth; Innate immunity; Lactococcus lactis; Protection; Schizochytrium limacinum; Transcriptomes

Indexed keywords

ALKALINE PHOSPHATASE; APOPTOSIS SIGNAL REGULATING KINASE 1; BINDING PROTEIN; COMPLEMENTARY DNA; E3 UBIQUITIN LIGASE HERC4; HLA A ANTIGEN; IMMUNOGLOBULIN M; LYSOZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS IIALPHA; MESSENGER RNA; NUCLEAR RECEPTOR NUR77; PREBIOTIC AGENT; PROBIOTIC AGENT; RECEPTOR; SUPEROXIDE DISMUTASE; TAX1 BINDING PROTEIN 1; TOLL LIKE RECEPTOR 2; TRANSCRIPTOME; TRANSFERRING RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; IMMUNOLOGICAL ADJUVANT;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; AQUACULTURE; ARTICLE; BODY WEIGHT; BODY WEIGHT GAIN; COMPARATIVE STUDY; CONTROLLED STUDY; CROMILEPTES ALTIVELIS; DIET SUPPLEMENTATION; DIGESTIVE SYSTEM; DISEASE RESISTANCE; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; EPINEPHELUS; EXPERIMENTAL DIET; FISH GENETICS; GENE EXPRESSION; GENE ONTOLOGY; GENE SEQUENCE; GENETIC DATABASE; GROWTH; GROWTH RATE; HEAD KIDNEY; IMMUNOREGULATION; INNATE IMMUNITY; JUVENILE ANIMAL; LACTOCOCCUS LACTIS; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REFERENCE DATABASE; RESPIRATORY BURST; SCHIZOCHYTRIUM; SCHIZOCHYTRIUM LIMACINUM; SURVIVAL; TRANSCRIPTOMICS; VIBRIO HARVEYI; ANIMAL; BASS; CHEMISTRY; DRUG EFFECT; FISH DISEASE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; PHYSIOLOGY; STRAMENOPILE; VETERINARY MEDICINE; VIBRIO; VIBRIOSIS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BASS; DISEASE RESISTANCE; FISH DISEASES; IMMUNITY, INNATE; LACTOCOCCUS LACTIS; PREBIOTICS; PROBIOTICS; STRAMENOPILES; VIBRIO; VIBRIO INFECTIONS;

EID: 85073002330     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2019.09.059     Document Type: Article

References (69)

1. K.C. Williams, D.M. Smith, I.H. Williams, S.J. Irvin, M. Barclay, ACIAR grouper grow out feeds program and related CSIRO research, Aquaculture Asia Magazine 10 (2005) 29-33.
2. M.W. Johnston, S.J. Purkis, Correction: modeling the potential spread of the recently identified non-native panther grouper (Chromileptes altivelis) in the Atlantic using a cellular automaton approach, PLos One 8 (2013) e73023.
3. J. Qin, D. Hu, W. Yang, J. Xiao, Complete mitochondrial genome of the humpback grouper Cromileptes altivelis, Mitochondr. DNA 25 (2014) 200-201.
4. K. Mahardika, Y.A. Zafran, T. Miyazaki, Susceptibility of juvenile humpback grouper Cromileptes altivelis to grouper sleepy disease iridovirus (GSDIV), Dis. Aquat. Organ 59 (2004) 1-9.
5. K.C. Williams, S. Irvin, M. Barclay, Polka dot grouper Cromileptes altivelis fingerlings require high protein and moderate lipid diets for optimal growth and nutrient retention, Aquacult. Nutr. 10 (2004) 125-134.
6. G. Subha, P. Indira, K.M. Sunit, Application and effectiveness of immunostimulants, probiotics, and prebiotics in aquaculture: a review, Isr. J. Aquacult-Bamid. 62 (2010) 130-138.
7. R. Einar, E.O. Rolf, T.OE. Gifstad, A.D. Roy, A. Heidi, H. Gro-Ingunn, et al., Prebiotics in aquaculture: a review, Aquacult. Nutr. 16 (2010) 117-136.
8. Q. Zhang, H. Yu, T. Tong, W. Tong, L. Dong, M. Xu, et al., Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus, Fish Shellfish Immunol. 38 (2014) 7-14.
9. A.M. Bakke-McKellep, M. Penn, P. Salas, S. Refstie, S. Sperstad, T. Landsverk, et al., Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.), Br. J. Nutr. 97 (2007) 699-713.
10. R. Cerezuela, F.A. Guardiola, J. Meseguer, M.A. Esteban, Enrichment of gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the immune system, Fish Physiol. Biochem. 38 (2012) 1729-1739.
11. M. Reyes-Becerril, F. Guardiola, M. Rojas, F. Ascencio, M.A. Esteban, Dietary administration of microalgae Navicula sp. affects immune status and gene expression of gilthead seabream (Sparus aurata), Fish Shellfish Immunol. 35 (2013) 883-889.
12. B.K.Y. Kwan, A.K. Chan, S.G. Cheung, Marine microalgae as dietary supplements in the culture of juvenile Chinese horseshoe crabs, Tachypleus tridentatus (Xiphosura), Aquac. Res. 48 (2017) 3910-3924.
13. D.J.R. Maria, D.M. Alcina, D.M. Rui, Emergent sources of prebiotics: seaweeds and microalgae, Mar. Drugs 14 (2016) 27.
14. Y.K. Lee, P.F. Chew, B.S. Soh, L.Y. Tham, Enhancing phagocytic activity of hemocytes and disease resistance in the prawn Penaeus merguieneis by feeding Spirulina platensis, J. Appl. Phycol. 15 (2003) 279-287.
15. N. Sheikhzadeh, A.K. Pashaki, K. Nofouzi, M. Heidarieh, H.T. Nasrabadi, Effects of dietary Ergosan on cutaneous mucosal immune response in rainbow trout (Oncorhyncus mykiss), Fish Shellfish Immunol. 32 (2012) 407-410.
16. M.M. Rahman, C.M. Escobedo-Bonilla, M. Wille, V. Alday-Sanz, L. Audoorn, J. Neyts, et al., Clinical effect of cidofovir and a diet supplemented with Spirulina platensis in white spot syndrome virus (WSSV) infected specific pathogen-free Litopenaeus vannamei juveniles, Aquaculture 255 (2006) 600-605.
17. C.M. Tayag, Y.C. Lin, C.C. Li, C.H. Liou, J.C. Chen, Administration of the hot-water extract of Spirulina platensis enhanced the immune response of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus, Fish Shellfish Immunol. 28 (2010) 764-773.
18. G. Immanuel, M. Sivagnanavelmurugan, T. Marudhupandi, S. Radhakrishnan, A. Palavesam, The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon, Fish Shellfish Immunol. 32 (2012) 551-564.
19. A. Garcia-Ortega, K.R. Kissinger, J.T. Trushenski, Evaluation of fish meal and fish oil replacement by soybean protein and algal meal from Schizochytrium limacinum in diets for giant grouper Epinephelus lanceolatus, Aquaculture 452 (2016) 1-8.
20. Y. Wang, M. Li, K. Filer, Y. Xue, Q. Ai, K. Mai, Evaluation of Schizochytrium meal in microdiets of Pacific white shrimp (Litopenaeus vannamei) larvae, Aquac. Res. 48 (2016) 2328-2336.
21. S. Patnaik, T.M. Samocha, D.A. Davis, R.A. Bullis, C.L. Browdy, The use of HUFA-rich algal meals in diets for Litopenaeus vannamei, Aquacult. Nutr. 12 (2006) 395-401.
22. M.R. Miller, P.D. Nichols, C.G. Carter, Replacement of fish oil with thraustochytrid Schizochytrium sp. L. oil in Atlantic salmon parr (Salmo salar L.) diets, Comp. Biochem. Phys. A. 148 (2007) 382-392.
23. E. Ganuza, T. Benitez-Santana, O. Atalah, E. Vega-Orellana, R. Ganga, M.S. Izquierdo, Crypthecodinium cohnii and Schizochytrium sp. as potential substitutes to fisheries-derived oils from seabream (Sparus aurata) microdiets, Aquaculture 277 (2008) 109-116.
24. M.H. Li, E.H. Robinson, C.S. Tucker, B.B. Manning, L. Khoo, Effects of dried algae Schizochytrium sp., a rich source of docosahexaenoic acid, on growth, fatty acid composition, and sensory quality of channel catfish Lctalurus punctatus, Aquaculture 292 (2009) 232-236.
25. R. Harikrishnan, M.C. Kim, J.S. Kim, C. Balasundaram, M.S. Heo, Protective effect of herbal and probiotics enriched diet on haematological and immunity status of Oplegnathus fasciatus (Temminck & Schlegel) against Edwardsiella tarda, Fish Shellfish Immunol. 30 (2011) 886-893.
26. G.R.D. Geovanny, S. Ma, Influence of Probiotics on the Growth and Digestive Enzyme Activity of White Pacific Shrimp (Litopenaeus Vannamei), J. Ocean Univ. China vol. 7 (2008) 215-218.
27. B.C. De, D.K. Meena, B.K. Behera, P. Das, P.K.D. Mohapatra, A.P. Sharma, Probiotics in fish and shellfish culture: immunomodulatory and ecophysiological responses, Fish Physiol. Biochem. 40 (2014) 921-971.
28. M.D. Vrese, J. Schrezenmeir, Probiotics, Prebiotics, and Synbiotics, Food Biotechnolo. (2008) pp. 1-66.
29. M.A. Al-Dohail, R. Hashim, P.M. Aliyu, Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling, Aquacult. Res. 40 (2009) 1642-1652.
30. M. Reyes-Becerril, F. Ascencio, M.E. Macias, M. Maldonado, M. Rojas, M.A. Esteban, Effects of marine silages enriched with Lactobacillus sakei 5-4 on haemato-immunological and growth response in Pacific red snapper (Lutjanus peru) exposed to Aeromonas veronii, Fish Shellfish Immunol. 33 (2012) 984-992.
31. D. Kim, B.R. Beck, S.B. Heo, J. Kim, H.D. Kim, S.M. Lee, et al., Lactococcus lactis, BFE920 activates the innate immune system of olive flounder (Paralichthys olivaceus), resulting in protection against Streptococcus iniae, infection and enhancing feed efficiency and weight gain in large-scale field studies, Fish Shellfish Immunol. 35 (2013) 1585-1590.
32. T.L. Nguyen, C.I. Park, D.H. Kim, Improved growth rate and disease resistance in olive flounder, Paralichthys olivaceus, by probiotic Lactococcus lactis WFLU12 isolated from wild marine fish, Aquaculture 471 (2017) 113-120.
33. Y. Sun, M.W. He, Z.J. Cao, Z.Y. Xie, C.S. Liu, S.F. Wang, et al., Effects of dietary administration of Lactococcus lactis HNL12 on growth, innate immune response, and disease resistance of humpback grouper (Cromileptes altivelis), Fish Shellfish Immunol. 82 (2018) 296-303.
34. M. Reyes-Becerril, C. Angulo, N. Estrada, Y. Murillo, F. Ascencio, Dietary administration of microalgae alone or supplemented with Lactobacillus sakei affects immune response and intestinal morphology of Pacific red snapper (Lutjanus peru), Fish Shellfish Immunol. 40 (2014) 208-216.
35. R. Cerezuela, J. Meseguer, M.A. Esteban, Effects of dietary inulin, Bacillus subtilis and microalgae on; intestinal gene expression in gilthead seabream (Sparus aurata L.), Fish Shellfish Immunol. 34 (2013) 843-848.
36. X.T. Hong, L.X. Xiang, J.Z. Shao, The immunestimulating effect of bacterial genomic DNA on the innate immune responses of bivalve mussel, Hyriopsis cumingii Lea, Fish Shellfish Immunol. 21 (2006) 357-364.
37. Z.G. Tu, H.Y. Li, X. Zhang, Y. Sun, Y.C. Zhou, Complete genome sequence and comparative genomics of the golden pompano (Trachinotus ovatus) pathogen, Vibrio harveyi strain QT520, PeerJ 5 (2017) e4127.
38. Y.H. Hu, J. Zhang, CsCCL17, a CC chemokine of Cynoglossus semilaevis, induces leukocyte trafficking and promotes immune defense against viral infection, Fish Shellfish Immunol. 45 (2015) 771-779.
39. P. Pandiyan, D. Balaraman, R. Thirunavukkarasu, E.G.J. George, K. Subaramaniyan, S. Manikkam, et al., Probiotics in aquaculture, Drug Invent. Today 5 (2013) 55-59.
40. M.A. Dawood, S. Koshio, Recent advances in the role of probiotics and prebiotics in carp aquaculture: a review, Aquaculture 454 (2016) 243-251.
41. Z.H. Qi, X.H. Zhang, N. Boon, P. Bossier, Probiotics in aquaculture of China-current state, problems and prospect, Aquaculture 290 (2009) 15-21.
42. R. Harikrishnan, C. Balasundaram, M.S. Heo, Lactobacillus sakei BK19 enriched diet enhances the immunity status and disease resistance to streptococcosis infection in kelp grouper, Epinephelus bruneus, Fish Shellfish Immunol. 29 (2010) 1037-1043.
43. C.N. Zhang, X.F. Li, W.N. Xu, D.D. Zhang, K.L. Lu, L.N. Wang, et al., Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on growth performance, body composition, intestinal enzymes activities and gut histology of triangular bream (Megalobrama terminalis), Aquac. Nutr. 21 (2014) 755-766.
44. S.S. Giri, V. Sukumaran, M. Oviya, Potential probiotic Lactobacillus plantarum VSG3 improves the growth, immunity, and disease resistance of tropical freshwater fish, Labeo rohita, Fish Shellfish Immunol. 34 (2013) 660-666.
45. H.T. Liu, S.F. Wang, Y. Cai, X.H. Guo, Z.J. Cao, Y.Z. Zhang, et al., Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus, Fish Shellfish Immunol. 60 (2017) 326-333.
46. B.R. Beck, D. Kim, J. Jeon, S.M. Lee, H.K. Kim, O.J. Kim, et al., The effects of combined dietary probiotics Lactococcus lactis BFE920 and Lactobacillus plantarum FGL0001 on innate immunity and disease resistance in olive flounder (Paralichthys olivaceus), Fish Shellfish Immunol. 42 (2015) 177-183.
47. X.X. Zhou, Y.B. Wang, J.T. Yao, W.F. Li, Inhibition ability of probiotic, Lactococcus lactis, against A. hydrophila and study of its immunostimulatory effect in tilapia (Oreochromis niloticus), Int. J. Eng. Sci. Technol. 2 (2011) 73-80.
48. B.H. Xu, Y.B. Wang, J.R. Li, Q. Lin, Effect of prebiotic xylooligosaccharides on growth performances and digestive enzyme activities of allogynogenetic crucial carp (Carassius auratus gibelio), Fish Physiol. Biochem. 35 (2009) 351-357.
49. A. Dimitroglou, M.D. Lee, P. Spring, J. Sweetman, R. Moate, S.J. Davies, Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata), Aquaculture 300 (2010) 182-188.
50. Z.Y. Ju, I. Forster, W. Dominy, Effects of supplementing two species of marine algae or their fractions to a formulated diet on growth, survival and composition of shrimp (Litopenaeus vannamei), Aquaculture 292 (2009) 237-243.
51. Z.Y. Ju, D.F. Deng, W. Dominy, A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fish meal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931), Aquaculture 354 (2012) 50-55.
52. B. Guroy, I. Sahin, S. Mantoglu, S. Kayal, Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellow tail cichlid Pseudotropheus acei, Aquacult. Int. 20 (2012) 869-878.
53. G. Rafiee, A. Pourbabaee, A. Agharokh, M. Avakhkeysami, Effects of the mixed probiotic microalgae-bacteria, skeletonema costatum-Bacillus subtilis, on stress tolerance and innate immunity prophenoloxidase (proPO) activating in Penaeus monodon larvae, J. Bio. & Env. Sci. 4 (2014) 273-284.
54. R.A. Dalmo, K. Ingebrigtsen, J. Boegwald, Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES), J. Fish Dis. 20 (1997) 241-273.
55. B.M. Babior, R.S. Kipnes, J.T. Curnutte, Biological defense mechanisms: the production by leukocytes of superoxide, a potential bactericidal agent, J. Clin. Invest. 52 (1973) 741-744.
56. N. D. Pedro, A.E. Guijarro, M.A. Lopez-Patino, R. Marinez-Alvarez, M. Delgado, Daily and seasonal variations in haematological and blood biochemical parameters in the tench, Tinca tinca Linnaeus, 1758, Aquac. Res. 36 (2005) 85-96.
57. J.L. Balcazar, I.D. Blas, I.R. Zarzuela, D. Vendrell, O. Girones, J.L. Muzquiz, Enhancement of the immune response and protection induced by probiotic lactic acid bacteria against furunculosis in rainbow trout (Oncorhynchus mykiss), Fems. Immunol. Med. Microbiol. 51 (2007) 185-193.
58. P. Diaz-Rosales, M. Chabrillon, R.A. Diaz, F.L. Figueroa, M.C. Balebona, M.A. Morinigo, Effect of dietary administration of Porphyridium cruentum on the respiratory burst activity of sole, Solea senegalensis (Kaup), phagocytes, J. Fish Dis. 31 (2008) 489-495.
59. J.L. Balcazar, I.D. Blas, I. Ruiz-Zarzuela, D. Vendrell, A.C. Calvo, I. Marquez, et al., Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta), Br. J. Nutr. 97 (2007) 522-527.
60. C. Lim, M. Yildirim-Aksoy, M.H. Li, T.L. Welker, P.H. Klesius, Influence of dietary levels of lipid and vitamin E on growth and resistance of Nile tilapia to Streptococcus iniae challenge, Aquaculture 298 (2009) 76-82.
61. H.C. Liu, Z.Y. Cheng, S.L. Zhai, C.L. Lin, J. Wang, X.T. Qiao, et al., Effects of Dietary Schizochytrium on the growth performance, serum nonspecific immunity indices, and disease resistance of Cyprinus carpio var. Jian, Progress in Fishery Sciences 37 (2016) 42-48.
62. T. Manning, G. Gibson, Prebiotics, Best Pract. & Res. Cl. Ga. 18 (2004) 287-298.
63. D. Bhowmik, J. Dubey, S. Mehra, Probiotic efficiency of Spirulina platensis-stimulating growth of lactic acid bacteria, World J. Dairy Food Sci. 42 (2009) 160-163.
64. J.L. Parada, G.Z. Caire, M.C.Z. Mule, M.M.S. Cano, Lactic acid bacteria growth promoters from Spirulina platensis, Int. J. Food Microbiol. 45 (1998) 222-228.
65. E. Sucu, D. Udum, N. Gunes, O. Canbolat, I. Filya, Influence of supplementing diet with microalgae (Schizochytrium limacinum) on growth and metabolism in lambs during the summer, Turk. J. Vet. Anim. Sci. 41 (2017) 167-174.
66. M. Bahey-El-Din, P.G. Casey, B.T. Griffin, C.G. Gahan, Lactococcus lactis-expressing listeriolysin O (LLO) provides protection and specific CD8(+) T cells against Listeria monocytogenes in the murine infection model, Vaccine 26 (2008) 5304-5314.
67. M.Y. Li, J. Li, P. Chen, Q. Wang, Effects of VE and Schizochytrium on growth and TLR / NF-κB expression level of Fenneropenaeus chinensis, Chinese Fishery Quality and Standards 2 (2012) 37-44.
68. S. Guzman, A. Gato, M. Lamela, M. Freire-Garabal, J.M. Calleja, Anti-inflammatory and immunomodulatory activities of polysaccharide from Chlorella stigmatophora and Phaeodactylum tricornutum, Phytother. Res. 17 (2003) 665-670.
69. S. Guzman, A. Gato, J.M. Calleja, Antiinflammatory, analgesic and free radical scavenging activities of the marine microalgae Chlorella stigmatophora and Phaeodactylum tricornutum, Phytother. Res. 15 (2001) 224-230.