Probiotic Effects of a Novel Strain, Acinetobacter KU011TH, on the Growth Performance, Immune Responses, and Resistance against Aeromonas hydrophila of Bighead Catfish (Clarias macrocephalus Günther, 1864)

Microorganisms - Tập 7 Số 12 - Trang 613
Anurak Bunnoy1, Uthairat Na‐Nakorn2, Prapansak Srisapoome1
1Laboratory of Aquatic Animal Health Management, Department of Aquaculture, Faculty of Fisheries, Kasetsart University, 50 Paholayothin Rd, Ladyao, Chatuchak, Bangkok 10900, Thailand
2Laboratory of Aquatic Animal Genetics, Department of Aquaculture, Faculty of Fisheries, Kasetsart University, 50 Paholayothin Rd, Ladyao, Chatuchak, Bangkok 10900, Thailand

Tóm tắt

In the present study, the novel probiotic strain Acinetobacter KU011TH with an evident lack of pathogenicity in catfish was experimented. Three practical administration routes, namely, feed additive (FD), water-soluble additive (SOL), and a combination route (FD+SOL), were applied in two sizes of catfish. After 120 days of FD+SOL administration, catfish fingerlings (15 g) exhibited a significant improvement in all tested growth performance parameters. For 15- and 30-day applications at the juvenile stage (150 g), phagocytic activity, phagocytic index, lysozyme activity, respiratory burst activity, alternative complement pathway, and bactericidal activity were significantly increased. Furthermore, probiotic-administered bighead catfish exhibited an upregulated expression of several immune-related genes in tested organs. Significant colonization by Acinetobacter KU011TH in rearing water and on skin and gills was observed among experimental groups. Histological analysis clearly indicated enhanced physical characteristics of skin mucosal immunity in the treated groups. No histopathological changes in the gills, skin, intestine or liver were observed among the fish groups. Interestingly, after challenge with Aeromonas hydrophila, the survival rates of the treated groups were significantly higher than those of the controls. In conclusion, the novel probiont Acinetobacter KU011TH provides a potent strategy for improvement in growth and disease resistance, which is an important steppingstone for sustaining catfish aquaculture.

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Tài liệu tham khảo

Food and Agriculture Organization of the United Nations (FAO) (2018, December 01). Fishstat Plus Rome 2017. In: FAO Fisheries and Aquaculture Department. Rome. Updated 14 September 2017. Available online: http://www.fao.org/fishery/statistics/software/fishstat/en.

Kamonrat, 2004, Genetic diversity of walking catfish, Clarias macrocephalus, in Thailand and evidence of genetic introgression from introduced farmed C. gariepinus, Aquaculture, 240, 145, 10.1016/j.aquaculture.2004.08.001

Chatchaiphan, 2017, De novo transcriptome characterization and growth-related gene expression profiling of diploid and triploid bighead catfish (Clarias macrocephalus Gunther, 1864), Mar. Biotechnol. (Ny), 19, 36, 10.1007/s10126-017-9730-3

Suanyuk, 2014, Mortality and pathology of hybrid catfish, Clarias macrocephalus (Gunther) x Clarias gariepinus (Burchell), associated with Edwardsiella ictaluri infection in southern Thailand, J. Fish. Dis., 37, 385, 10.1111/jfd.12127

Chantsawang, 1995, Response to mass selection for disease resistance in walking catfish, Clarias macrocephalus, J. Appl. Aquac., 4, 65, 10.1300/J028v04n04_06

Hoseinifar, 2017, Modulation of nutrient digestibility and digestive enzyme activities in aquatic animals: The functional feed additives scenario, Aquac. Res., 48, 3987, 10.1111/are.13368

Nawaz, 2018, The functionality of prebiotics as immunostimulant: Evidences from trials on terrestrial and aquatic animals, Fish Shellfish Immunol., 76, 272, 10.1016/j.fsi.2018.03.004

Fuller, 1989, Probiotics in man and animals, J. Appl. Bacteriol., 66, 365, 10.1111/j.1365-2672.1989.tb05105.x

Merrifield, 2010, The current status and future focus of probiotic and prebiotic applications for salmonids, Aquaculture, 302, 1, 10.1016/j.aquaculture.2010.02.007

2012, Use of probiotics in aquaculture, ISRN Microbiol., 2012, 916845

Van Doan, H., Hoseinifar, S.H., Ringø, E., Ángeles Esteban, M., Dadar, M., Dawood, M.A.O., and Faggio, C. (2019). Host-Associated Probiotics: A Key Factor in Sustainable Aquaculture. Rev. Fish. Sci. Aquac., 1–27.

Bunnoy, A., Na-Nakorn, U., Kayansamruaj, P., and Srisapoome, P. (2019). Acinetobacter strain KUO11TH, a unique organism related to Acinetobacter pittii and isolated from the skin mucus of healthy bighead catfish and its efficacy against several fish pathogens. Microorganisms, 7.

Chinedu, 2013, A new method for determining acute toxicity in animal models, Int. J. Toxicol., 20, 224, 10.4103/0971-6580.121674

Boyum, 1968, Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g, Scand. J. Clin. Lab. Invest. Suppl., 97, 77

Bernet, 1999, Histopathology in fish: proposal for a protocol to assess aquatic pollution, J. Fish. Dis., 22, 25, 10.1046/j.1365-2761.1999.00134.x

Lugert, 2016, A review on fish growth calculation: multiple functions in fish production and their specific application, Rev. Aquac., 8, 30, 10.1111/raq.12071

Ito, 1992, Colorimetric assay for lysozyme using Micrococcus luteus labeled with a blue dye, Remazol brilliant blue R, as a substrate, Chem. Pharm. Bull. (Tokyo), 40, 1523, 10.1248/cpb.40.1523

Segal, 1975, Cell damage and dye reduction in the quantitative nitroblue tetrazolium (NBT) test, Clin. Exp. Immunol., 19, 309

Nayak, 2018, Analyzing complement activity in the serum and body homogenates of different fish species, using rabbit and sheep red blood cells, Vet. Immunol. Immunopathol., 199, 39, 10.1016/j.vetimm.2018.03.008

Guo, 2019, Antibacterial activity and action mechanism of questin from marine Aspergillus flavipes HN4-13 against aquatic pathogen Vibrio harveyi, 3 Biotech., 9, 1, 10.1007/s13205-018-1535-1

Koenigsknecht, 2004, Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism, J. Neurosci., 24, 9838, 10.1523/JNEUROSCI.2557-04.2004

Panigrahi, 2004, Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136, Vet. Immunol. Immunopathol., 102, 379, 10.1016/j.vetimm.2004.08.006

Hai, 2015, Research findings from the use of probiotics in tilapia aquaculture: A review, Fish Shellfish Immunol., 45, 592, 10.1016/j.fsi.2015.05.026

Hoseinifar, 2019, Enhanced mucosal immune responses, immune related genes and growth performance in common carp (Cyprinus carpio) juveniles fed dietary Pediococcus acidilactici MA18/5M and raffinose, Dev. Comp. Immunol., 94, 59, 10.1016/j.dci.2019.01.009

Liu, 2012, Dietary administration of the probiotic, Bacillus subtilis E20, enhances the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides, Fish Shellfish Immunol., 33, 699, 10.1016/j.fsi.2012.06.012

Meidong, 2018, Evaluation of probiotic Bacillus aerius B81e isolated from healthy hybrid catfish on growth, disease resistance and innate immunity of Pla-mong Pangasius bocourti, Fish Shellfish Immunol., 73, 1, 10.1016/j.fsi.2017.11.032

Tri, 2017, Effects of the dietary supplementation of mixed probiotic spores of Bacillus amyloliquefaciens 54A, and Bacillus pumilus 47B on growth, innate immunity and stress responses of striped catfish (Pangasianodon hypophthalmus), Fish Shellfish Immunol., 60, 391, 10.1016/j.fsi.2016.11.016

Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method, Methods, 25, 402, 10.1006/meth.2001.1262

Fischer, 2008, Hematoxylin and eosin staining of tissue and cell sections, Csh. Protoc., 49, 86

Torrecillas, 2015, Dietary mannan oligosaccharides: counteracting the side effects of soybean meal oil inclusion on European sea bass (Dicentrarchus labrax) gut health and skin mucosa mucus production?, Front. Immunol., 6, 397, 10.3389/fimmu.2015.00397

Sosa, 2014, Development and application of MIPAR™: a novel software package for two- and three-dimensional microstructural characterization, IMMI, 3, 10

Kent, 2009, Recommendations for control of pathogens and infectious diseases in fish research facilities, Comp. Biochem. Physiol. Toxicol. Pharm., 149, 240, 10.1016/j.cbpc.2008.08.001

Bewick, 2004, Statistics review 12: survival analysis, Crit Care, 8, 389, 10.1186/cc2955

Kim, 2014, Acinetobacter apis sp. nov., isolated from the intestinal tract of a honey bee, Apis mellifera, J. Microbiol., 52, 639, 10.1007/s12275-014-4078-0

Liu, 2017, Acinetobacter larvae sp. nov., isolated from the larval gut of Omphisa fuscidentalis, Int. J. Syst. Evol. Microbiol., 67, 806, 10.1099/ijsem.0.001644

Thornton, 1992, Probiotic bacteria: myth or reality?, Trends Food Sci. Technol., 3, 309, 10.1016/S0924-2244(10)80018-4

Brunt, 2005, Use of a probiotic to control lactococcosis and streptococcosis in rainbow trout, Oncorhynchus mykiss (Walbaum), J. Fish. Dis., 28, 693, 10.1111/j.1365-2761.2005.00672.x

Salinas, 2005, Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses, Fish Shellfish Immunol., 19, 67, 10.1016/j.fsi.2004.11.007

Aly, 2008, 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., 25, 128, 10.1016/j.fsi.2008.03.013

Azimirad, 2016, The effects of feeding with synbiotic (Pediococcus acidilactici and fructooligosaccharide) enriched adult Artemia on skin mucus immune responses, stress resistance, intestinal microbiota and performance of angelfish (Pterophyllum scalare), Fish Shellfish Immunol., 54, 516, 10.1016/j.fsi.2016.05.001

Irianto, 2002, Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum), J. Fish. Dis., 25, 333, 10.1046/j.1365-2761.2002.00375.x

Aly, 2008, Effect of probiotics on the survival, growth and challenge infection in Tilapia nilotica (Oreochromis niloticus), Aquac. Res., 39, 647, 10.1111/j.1365-2109.2008.01932.x

Nayak, 2017, Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham.), Fish Shellfish Immunol., 23, 892, 10.1016/j.fsi.2007.02.008

Thurlow, 2019, Bacillus velezensis AP193 exerts probiotic effects in channel catfish (Ictalurus punctatus) and reduces aquaculture pond eutrophication, Aquaculture, 503, 347, 10.1016/j.aquaculture.2018.11.051

Mohammadian, 2019, Administrations of autochthonous probiotics altered juvenile rainbow trout Oncorhynchus mykiss health status, growth performance and resistance to Lactococcus garvieae, an experimental infection, Fish Shellfish Immunol., 86, 269, 10.1016/j.fsi.2018.11.052

Park, 2016, Comparison of the effects of dietary single and multi-probiotics on growth, non-specific immune responses and disease resistance in starry flounder, Platichthys stellatus, Fish Shellfish Immunol., 59, 351, 10.1016/j.fsi.2016.11.006

Hoseinifar, 2018, Host-associated probiotics boosted mucosal and serum immunity, disease resistance and growth performance of Nile tilapia (Oreochromis niloticus), Aquaculture, 491, 94, 10.1016/j.aquaculture.2018.03.019

Butel, 2014, Probiotics, gut microbiota and health, Med. Mal. Infect., 44, 1, 10.1016/j.medmal.2013.10.002

Aloisio, 2014, Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants, Appl. Microbiol. Biotechnol., 98, 563, 10.1007/s00253-013-5405-9

Vieira, 2013, The role of probiotics and prebiotics in inducing gut immunity, Front. Immunol., 4, 445, 10.3389/fimmu.2013.00445

Sun, 2010, 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., 29, 803, 10.1016/j.fsi.2010.07.018

Ramesh, 2018, Effects of potential probiotic Bacillus subtilis KADR1 and its subcellular components on immune responses and disease resistance in Labeo rohita, Aquac. Res., 49, 367, 10.1111/are.13467

Parnham, M. (2015). Pathogen-associated molecular patterns (PAMPs). Encyclopedia of Inflammatory Diseases, Springer Basel.

Lazado, 2014, Mucosal immunity and probiotics in fish, Fish Shellfish Immunol., 39, 78, 10.1016/j.fsi.2014.04.015

Fernandes, 2002, Anti-microbial properties of histone H2A from skin secretions of rainbow trout, Oncorhynchus mykiss, Biochem. J., 368, 611, 10.1042/bj20020980

Noga, 2003, Piscidins: a novel family of peptide antibiotics from fish, Drug News Perspect., 16, 87, 10.1358/dnp.2003.16.2.829325

Rakers, 2010, ‘Fish matters’: the relevance of fish skin biology to investigative dermatology, Exp. Derm., 19, 313, 10.1111/j.1600-0625.2009.01059.x

Rakers, 2013, Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology, J. Investig. Derm., 133, 1140, 10.1038/jid.2012.503

Subramanian, 2007, A comparative study on innate immune parameters in the epidermal mucus of various fish species, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 148, 256, 10.1016/j.cbpb.2007.06.003

Loganathan, 2011, Studies on the role of mucus from Clarias batrachus (Linn) against selected microbes, IJPA, 2, 202

Modanloo, 2017, The effects of single or combined administration of galactooligosaccharide and Pediococcus acidilactici on cutaneous mucus immune parameters, humoral immune responses and immune related genes expression in common carp (Cyprinus carpio) fingerlings, Fish Shellfish Immunol., 70, 391, 10.1016/j.fsi.2017.09.032

Pittman, 2013, Body site matters: an evaluation and application of a novel histological methodology on the quantification of mucous cells in the skin of Atlantic salmon, Salmo salar L., J. Fish. Dis., 36, 115, 10.1111/jfd.12002

Ellis, 1999, Immunity to bacteria in fish, Fish Shellfish Immunol., 9, 291, 10.1006/fsim.1998.0192

Kurath, 2011, Foreword: pathogens and immune responses of fish and reptiles, Vet. Res., 42, 101, 10.1186/1297-9716-42-101

Brunt, 2007, The development of probiotics for the control of multiple bacterial diseases of rainbow trout, Oncorhynchus mykiss (Walbaum), J. Fish. Dis., 30, 573, 10.1111/j.1365-2761.2007.00836.x