The use of macroscopic fungi as immunostimulants in fish: state of the art in 2018
DOI:
https://doi.org/10.24275/uam/izt/dcbs/hidro/2018v28n2/TintosKeywords:
fish, fungi, immunostimulants, macromycetes, teleostAbstract
Background. Different methods are currently used for the prevention and control of diseases in aquaculture. Prophylaxis with immunostimulants from microscopic fungi provides protection against diseases and increases resistance to parasites. In this context, Basidiomycota fungi could have high potential for use in aquaculture because they contain different compounds, such as fungal proteins, polysaccharides, terpenoids, vitamins, and minerals, which could work as immunostimulants. Goals. Collect and disseminate the information on species of macroscopic fungi that have been used as immunostimulants in the farming of teleost fish and the fungi that have not been tested in fish but have shown positive results in other organisms. Methods. We gather, discuss and compare the experimental, scientific and theoretical literature related to the immunostimulant effect of macroscopic fungi in the cultivation of teleosts, as well as fungi whose stimulating effect has been positive in other organisms. Results. We evaluated more than 50 species of fungi with immunostimulating properties. Nevertheless, in recent years, the effects of only eight species of macromycetes, belonging to the genera Ganoderma, Inonotus, Lentinula, Pleurotus, and Trametes, have been evaluated in 17 published papers regarding the immune response of nine species of fish. Seven of these papers are about isolated glucans, six about crude and alcoholic extracts, two about pulverized basidiomata, and one about a mushroom fermented by-product. Conclusions. Due to the limited information on the immunostimulating effect of macromycetes on fish, more research is needed regarding other fungi species with immunostimulant properties, the correct determination of fungi species, their culture, and in vivo and in vitro tests that confirm their immune system effects on the model organism and target organism.
Downloads
References
Abasali, H. & S. Mohamad. 2010. Immune response of common carp (Cyprinus carpio) fed with herbal immunostimulants diets. Agricultural Journal 5: 163-172. DOI:10.3923/javaa.2010.1839.1847
Anderson, D. P. 1992. Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annual Review of Fish Diseases 2: 281-307. DOI: 10.1016/0959-8030(92)90067-8
Baba, E., G. Uluköy & C. Öntaş. 2015. Effects of feed supplemented with Lentinula edodes mushroom extract on the immune response of rainbow trout, Oncorhynchus mykiss, and disease resistance against Lactococcus garvieae. Aquaculture 448: 476-482. DOI: 10.1016/j.aquaculture.2015.04.031
Bilen, S., S. Yilmaz & A. M. Bilen. 2013. Influence of Tetra (Conitus coggygria) extract against Vibrio anguillarum infection in koi carp, Cyprinus carpio with referenced to haematological and immunological changes. Turkish Journal of Fisheries and Aquatic Sciences 13: 517-522. DOI: 10.4194/1303-2712-v13_3_16
Bilen, S., S. Ünal & H. Güvensoy. 2016. Effects of oyster mushroom (Pleurotus ostreatus) and nettle (Urtica dioica) methanolic extracts on immune responses and resistance to Aeromonas hydrophila in raibonw trout (Oncorhynchus mykiss). Aquaculture 454 (1): 90-94. DOI: 10.1016/j.aquaculture.2015.12.010
Bricknell, I. & R. A. Dalmo. 2005. The use of immunostimulants in fish larval aquaculture. Fish & Shellfish Immunology 19: 457-472. DOI:10.1016/j.fsi.2005.03.008
Çag larlrmak, N., K. Ünal & S. Ötles. 2002. Nutritional value of edible wild mushrooms collected from the Black Sea region of Turkey. Micología Aplicada Internacional 14 (1): 1-5.
Carbonero, E. R., A. C. Ruthes, C. S. Freitas, P. Utrilla, J. Gálvez, E. V. da Silva, G. L. Sassaki, P. A. Gorin & M. Iacomini. 2012. Chemical and biological properties of a highly branched -glucan from edible mushroom Pleurotus sajor-caju. Carbohydrate Polymers 90 (2): 814-819. DOI: 10.1016/j.carbpol.2012.06.005
Catap , E. S., M. R. Jiménez, S. C. O. Liquido, M. A. K. B. Cabujat & M. M. Sadaya. 2013. Immunomodulatory effects of Ganoderma lucidum and virgin coconut oil in Nile tilapia artificially-infected with Aeromonas hydrophila. Fish & Shellfish Immunology 34 (6): 1644. DOI:10.1016/j.fsi.2013.03.030
Cha, Y. J., N. Alam, J. S. Lee, K. R. Lee, M. J. Shim, M. W. Lee, H. Y. Kim, P. G. Shin, J. C. Cheong, Y. B. Yoo & T. S. Lee. 2012. Anticancer and immunopotentiating activities of crude polysaccharides from Pleurotus nebrodensis on mouse sarcoma 180. Micobiology 40 (4): 236-243. DOI: 10.5941/MYCO.2012.40.4.236
Chang, C. S., S. L. Huang, S. Chen & S. N. Chen. 2013. Innate immune responses and efficacy of using mushroom beta-glucan mixture (MBG) on orange-spotted grouper, Epinephelus coioides, aquaculture. Fish & Shellfish Immunology 35 (1): 115-125. DOI: 10.1016/j.fsi.2013.04.004
Chen, Y. H., D. Han, X. M. Zhu, Y. X. Yang & S. Q. Xie. 2014. Effects of dietary inclusion of extracts from Ganoderma lucidum on growth performance, immune response and disease resistance in gibel carp (Carassius auratus gibelio). Acta Hydrobiologica Sinica 38 (4): 609- 618. DOI: 10.7541/2014.87
Del Rio-Zarag oza, O. B., E. J. Fajer-Ávila & P. Almazán-Rueda. 2011. Influence of -glucan on innate immunity and resistance of Lutjanus guttatus to an experimental infection of dactylogyrid monogeneans. Parasite Immunology 33: 483-494. DOI:10.1111/j.1365-3024.2011.01309.x
Dey, B., S. K. Bhunia, K. K. Maity, S. Patra, S. Mandal, S. Maiti, T. K. Maiti, S. R. Sikdar & S. S. Islam. 2010. Chemical analysis of an immunoenhancing water-soluble polysaccharide of an edible mushroom, Pleurotus florida blue variant. Carbohydrate Research 345 (18): 2736-2741. DOI:10.1016/j.carres.2010.09.032
Djordjevic, B., S. Škugor, S. M. Jorgensen, M. Overland, L. T. Mydland & A. Krasnov. 2009. Modulation of splenic immune responses to bacterial lipopolysaccharide in rainbow trout (Oncorhynchus mykiss) fed lentinan, a beta-glucan from mushroom Lentinula edodes. Fish & Shellfish Immunology 26: 201-209. DOI:10.1016/j.fsi.2008.10.012
Dobšíková, R., J. Blahová, I. Mikulíková, H. Modrá, E. Prášková, Z. Svobodová, M. Škorič, J. Jarkovský & A. K. Swicki. 2013. The effect of oyster mushroom -1.3/1.6-D-glucan and oxytetracycline antibiotic on biometrical, haematological, biochemical, and immunological indices, and histopathological changes in common carp (Cyprinus carpio L.). Fish & Shellfish Immunology 35: 1813-1823. DOI:10.1016/j.fsi.2013.09.006
El-Boshy, M. E., A. M. El-Ashram, F. M. Abdelhamid & H. A. Gadalla. 2010. Immunomodulatory effect of dietary Saccharomyces cerevisiae, -glucan and laminaran in mercuric chloride treated Nile tilapia (Oreochromis niloticus) and experimentally infected with Aeromonas hydrophila. Fish & Shellfish Immunology 28: 802-808. DOI:10.1016/j.fsi.2010.01.017
El-Enshasy, H. A. & R. Hatti-Kaul. 2013. Mushroom immunomodulators: unique molecules with unlimited applications. Trends in Biotechnology 31 (12): 668-677. DOI: 10.1016/j.tibtech.2013.09.003
Ghazanfari, T., R. Yaraee, Z. Farahnejad, B. Rahmati & H. Hakimzadeh. 2010. Macrophages activation and nitric oxide alterations in mice treated with Pleurotus florida. Immunopharmacology and Immunotoxicology 32: 47-50. DOI:10.1080/08923970903117357
Guimarães, I. G., C. Lim, M. Yildirim-Aksoy, M. H. Li & P. H. Klesius. 2014. Effects of dietary levels of vitamin A on growth, hematology, immune response and resistance of Nile tilapia (Oreochromis niloticus) to Streptococcus iniae. Animal Feed Science and Technology 188: 126-136. DOI:10.1016/j.anifeedsci.2013.12.003.
Harikrishnan, R., C. Balasundaram & M. S. Heo. 2011. Diet enriched with mushroom Phellinus linteus extract enhances the growth, innate immune response, and disease resistance of kelp grouper, Epinephelus bruneus against vibriosis. Fish & Shellfish Immunology 30 (1): 128-134. DOI:10.1016/j.fsi.2010.09.013
Harikrishnan, R., C. Balasundaram & M. S. Heo. 2012. Effect of Inonotus obliquus enriched diet on hematology, immune response, and disease protection in kelp grouper, Epinephelus bruneus against Vibrio harveyi. Aquaculture 344-349: 48-53. DOI:10.1016/j.aquaculture. 2012.03.010
Hu, T., Q. Huang, K. Wong & H. Yang. 2017. Structure, molecular conformation, and immunomodulatory activity of four polysaccharide fractions from Lignosus rhinocerotis sclerotia. International Journal of Biological Macromolecules 94: 423-430. DOI:10.1016/j.ijbiomac. 2016.10.051
Huerta, I., J. Molina, M. G. Garnica & J. Yahuaca. 2016. Total polyphenols and antioxidant activity of Ganoderma curtisii extracts. Journal of Medicinal Plants Studies 4 (4): 136-141.
Jeong, S. C., S. R. Koyyalamudi, Y. T. Jeon, C. H. Song & G. Pang. 2012. Macrophage immunomodulating and antitumor activities of polysaccharides isolated from Agaricus bisporus white button mushrooms. Journal of Medicinal Food 15: 58-65. DOI:10.1089/jmf.2011.1704
Jeong, Y. T., S. C. Jeong, Y. A. Gu, R. Islam & C. H. Song. 2010. Antitumor and immunomodulating activities of endo-biopolymers obtained from a submerged culture of Pleurotus eryngii. Food Science and Biotechnology 19 (2): 399-404. DOI:10.1007/s10068-010-0056-4
Jiao, Y., T. Xie, L. H. Zou, Q. Wei, L. Qiu & L. X. Chen. 2016. Lanostane triterpenoids from Ganoderma curtisii an their production inhibitory activities of LPS-induced microglia. Bioorganic & Medicinal Chemistry Letters: en prensa. DOI:10.1016/j.bmcl.2016.06.023
Kamilya, D., D. Ghosh, S. Bandyopadhyay, B. C. Mal & T. K. Maiti. 2006a. In vitro effects of bovine lactoferrin, mushroom glucan and Abrus agglutinin on Indian major carp, catla (Catla catla) head kidney leukocytes. Aquaculture 253: 130-139. DOI:10.1016/j.aquaculture. 2005.07.038
Kamilya, D., T. K. Maiti, S. N. Joardar & B. C. Mal. 2006b. Adjuvant effect of mushroom glucan and bovine lactoferrin upon Aeromonas hydrophila vaccination in catla, Catla catla (Hamilton). Journal of Fish Diseases 29: 331-337. DOI:10.1111/j.1365-2761.2006.00722.x
Kamilya, D., S. N. Joardar, B. C. Mal & T. K. Maiti. 2008. Effects of a glucan from the edible mushroom (Pleurotus florida) as an immunostimulant in farmed Indian major carp (Catla catla). The Israeli Journal of Aquaculture - Bamidgeh 60: 37-45.
Katya, K., Y. Yun, G. Park, J. Y. Lee, G. Yoo & S. C. Bai. 2014. Evaluation of the efficacy of fermented by-product of mushroom, Pleurotus ostreatus, as a fish meal replacer in juveline amur catfish, Silurus asotus: effects on growth, serological characteristics and immune responses. Asian-Australasian Journal of Animal Sciences 27 (10): 1478-1486. DOI:10.5713/ajas.2014.14038
Kim, J. Y., S. E. Byeon, Y. G. Lee, J. Y. Lee, J. Park, E. K. Hong & J. Y. Cho. 2008. Immunostimulatory activities of polysaccharides from liquid culture of pine-mushroom Tricholoma matsutake. Journal of Microbiology and Biotechnology 18: 95-103.
Kozarski, M., A. Klaus, M. Niksic, D. Jakovljevic, J. P. F. G. Helsper & L. J. K. D. Van Griensven. 2011. Antioxidative and immunomodulating activities of polysaccharide extracts of the medicinal mushrooms Agaricus bisporus, Agaricus brasiliensis, Ganoderma lucidum and Phellinus linteus. Food Chemistry 129: 1667-1675. DOI:10.1016/j.foodchem.2011.06.029
Krishnamoorthy, M. & V. Ramasubramanian. 2014. Dietary supplementation with chitosan on haematology and innate immune response in Cyprinus carpio haematopterus against Aeromonas hidrophila. Indian Journal of Applied Research 4: 67- 69.
Kumar, V., S. Roy & D. Barman. 2015. Effect of Mikania cordata (Burm) B. L. Robins on non-specific immune response of Catla catla (Hamilton, 1822) against Aphanomyces invadans. Fishery Technology 52 (1): 20-25.
Lin, S., S. Mao, Y. Guan, L. Lou, L. Lou & Y. Pan. 2012. Effects of dietary chitosan oligosaccharides and Bacillus coagulans on the growth innate immunity and resistance of koi (Cyprinus carpio koi). Aquaculture 342-343: 36-41. DOI:10.1016/j.aquaculture.2012.02.009
Lin, S., Y. Pan, L. Luo & L. Luo. 2011. Effects of dietary b-1, 3-glucan, chitosan or raffinose on the growth, innate immunity and resistance of koi (Cyprinus carpio koi). Fish Shellfish Immunology 31 (6): 788-794. DOI:10.1016/j.fsi.2011.07.013
Lin, Y., Y. Zhou, X. Wang, P. Wang, Y. Xiao, X. Cheng, Y. Zhang, Y. Liu & Q. Liu. 2016. Fruit extract from Pyropolyporus fomentarius (L. ex Fr.) Teng induces mitochondria-dependent apoptosis in leukemia cells but enhances immunomodulatory activities of splenic lymphocytes. Nutrition and Cancer 68 (4): 708-717. DOI:10.1080/01635581.2016.1158290
Maiti, S., S. K. Bhutia, S. K. Mallick, A. Kumar, N. Khadgi & T. K. Maiti. 2008. Antiproliferative and immunostimulatory protein fraction from edible mushrooms. Environmental Toxicology and Pharmacology 26: 187-191. DOI:10.1016/j.etap.2008.03.009
Mallick, S. K., S. Maiti, S. K. Bhutia & T. K. Maiti. 2010. Immunostimulatory properties of a polysaccharide isolated from Astraeus hygrometricus. Journal of Medicinal Food 13 (3): 665-672. DOI:10.1089/jmf.2009.1300
Mandal, E. K., K. Maity, S. Maity, S. K. Gantait, S. Maiti, T. K. Maiti, S. R. Sikdar & S. S Islam. 2011. Structural characterization of an immunoenhancing cytotoxic heteroglycan isolated from an edible mushroom Calocybe indica var. APK2. Carbohydrate Research 346 (14): 2237-2243. DOI:10.1016/j.carres.2011.07.009
Raa, J. 2000. The use of immune-stimulants in fish and shellfish feeds. In: Cruz-Suárez, L. E., D. Ricque-Marie, M. Tapia-Salazar, M. A. Olvera-Novoa, R. Civera-Cerecedo (Eds.). Avances en Nutrición Acuícola V. Memorias del V Simposium Internacional de Nutrición Acuícola. Mérida, Yucatán, México, pp. 47-56.
Reverter, M., N. Bontemps, D. Lecchini, B. Banaigs & P. Sasal. 2014. Use of plant extracts in fish aquaculture as an alternative to chemotherapy: current status and future perspectives. Aquaculture 433: 50-61. DOI:10.1016/j.aquaculture.2014.05.048
Roberts, R. 1983. Fish pathology. Fourth edition. London: Balliere-Tindall, 581 p.
Rondón-Barrag án, I. 2004. Inmunoestimulantes en medicina veterinaria. Orinoquia 8: 56-75.
Sadler, M. 2003. Nutritional properties of edible fungi. British Nutrition Foundation Nutrition Bulletin 28: 305-308. DOI:10.1046/j.1467-3010.2003.00354.x
Sakai, M. 1999. Current research status of fish immunostimulants. Aquaculture 162: 63-92. DOI:10.1016/S0044-8486(98)00436-0
Suabjakyong, P., K. Nishimura, T. Toida & L. J. L. D. Van Griensven. 2015. Structural characterization and immunomodulatory effects of polysaccharides from Phellinus linteus and Phellinus ignarius on the IL-6/IL-10 cytokine balance of the mouse macrophage cell lines (RAW 264.7). Food & Function 6: 2834-2844. DOI:10.1039/c5fo00491h
Tewary, A. & B. C. Patra. 2008. Use of vitamin C as an immunostimulant. Effect on growth, nutritional quality, and immune response of Labeo rohita (Ham.). Fish Physiology and Biochemistry 34 (3): 251-259.DOI:10.1007/s10695-007-9184-z
Uluköy, G., E. Baba & C. Öntaş. 2016. Effect of oyster mushroom, Pleurotus ostreatus, extract on hemato-immunological parameters of rainbow trout, Oncorhynchus mykiss. Journal of the World Aquaculture Society 47 (5): 676- 684. DOI:10.1111/jwas.12318
Van Doan, H., S. Doolgindachbap orn & A. Suksri. 2016. Effects of Eryngii mushroom (Pleurotus eryngii) and Lactobacillus plantarum on growth performance, inmmunity and disease resistance of Pangasius catfish (Pangasius bocourti, Sauvage 1880). Fish Physiology and Biochemistry 42 (5): 1427-1440. DOI:10.1007/s10695-016-0230-6
Vázquez-Piñeros, M. A., I. S. Rondón-Barraga n & P. R. Eslava-Mocha. 2012. Inmunoestimulantes en teleósteos: probióticos, -glucanos y LPS. Orinoquia 16 (1): 46-62.
Wang, C. R., W. T. Qiao, Y. N. Zhang & F. Liu. 2013. Effects of adenosine extract from Pholiota adipose (Fr.) Quel on mRNA expressions of superoxide dismutase and immunomodulatory cytokines. Molecules 18 (2): 1775-1782. DOI:10.3390/molecules18021775
Wang, D., S. Q. Sun, W. Z. Wu, S. L. Yang & J. M. Tan. 2014. Characterization of a water-soluble polysaccharide from Boletus edulis and its antitumor and immunomodulatory activities on renal cancer in mice. Carbohydrate Polymers 105: 127-134. DOI:10.1016/j.carbpol.2013.12.085
Wang, M., Y. X. Meng, R. L. Yang, T. Qin, X. Y. Wang, K. Y. Zhang, C. Z. Fei, Y. Li, Y. L. Hu & F. Q. Xue. (2012) Cordyceps militaris polysaccharides can enhance the immunity and antioxidation activity in immunosuppressed mice. Carbohydrate Polymers 89: 461-466. DOI:10.1016/j.carbpol.2012.03.029
Watanuki, H., K. Ota, A. C. M. Tassaka, T. Kato & M. Sakai. 2006. Immunostimulant effects of dietary Spirulina plantensis on carp, Cyprinus carpio. Aquaculture 258: 157-163. DOI:10.1016/j.aquaculture.2006.05.003
Wasser, S. P. 2002. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Applied Microbiology and Biotechnology 60: 258-274. DOI:10.1007/s00253-002-1076-7
Wasser, S. P. 2011. Current findings, future trends, and unsolved problems in studies of medicinal mushrooms. Applied Microbiology and Biotechnology 89: 1323-1332. DOI:10.1007/s00253-010-3067-4
Yin, G., L. Ardó, Z. Jeney, P. Xu & G. Jeney. 2008. Chinese herbs (Lonicera japonica y Ganoderma lucidum) enhance non-specific immune response of tilapia, Oreochromis niloticus, and protection against Aeromonas hydrophila. In: Bondad-Reantaso, M. G., C. V. Mohan, M. Crumlish & R. P. Subasinghe (Eds.). Diseases in Asian Aquaculture VI. Fish Health Section, Asian Fisheries Society, Manila, Philippines, pp. 269-282.
Yin, G., L. Ardó, K. D. Thompson, A. Adams, Z. Jeney & G. Jeney. 2009. Chinese herbs (Astragalus radix and Ganoderma lucidum) enhance immune response of carp, Cyprinus carpio, and protection against Aeromonas hydrophila. Fish & Shellfish Immunology 26 (1): 140-145. DOI:10.1016/j.fsi.2008.08.015
Zheng, Y., W. Wang & Y. Li. 2015. Antitumor and immunomodulatory activity of polysaccharide isolated from Trametes orientalis. Carbohydrate Polymers 131: 248-254. DOI:10.1016/j.carbpol.2015.05.074
Downloads
Published
How to Cite
Issue
Section
License
Los autores/as que publiquen en esta revista aceptan las siguientes condiciones:
De acuerdo con la legislación de derechos de autor, HIDROBIOLÓGICA reconoce y respeta el derecho moral de los autores, así como la titularidad del derecho patrimonial, el cual será cedido a la revista para su difusión en acceso abierto.
Publicar en la revista HIDROBIOLÓGICA tiene un costo de recuperación de $500 pesos mexicanos por página en blanco y negro (aproximadamente 29 dólares americanos) y $1000 pesos por página a color (aproximadamente 58 dólares americanos).
Todos los textos publicados por HIDROBIOLÓGICA sin excepción se distribuyen amparados bajo la licencia Creative Commons 4.0Atribución-No Comercial (CC BY-NC 4.0 Internacional), que permite a terceros utilizar lo publicado siempre que mencionen la autoría del trabajo y a la primera publicación en esta revista.
Los autores/as pueden realizar otros acuerdos contractuales independientes y adicionales para la distribución no exclusiva de la versión del artículo publicado en HIDROBIOLÓGICA (por ejemplo incluirlo en un repositorio institucional o publicarlo en un libro) siempre que indiquen claramente que el trabajo se publicó por primera vez en HIDROBIOLÓGICA.
Para todo lo anterior, el o los autor(es) deben remitir el formato de Carta-Cesión de la Propiedad de los Derechos de la primera publicación debidamente requisitado y firmado por el autor(es). Este formato se puede enviar por correo electrónico en archivo pdf al correo: enlacerebvistahidrobiológica@gmail.com; rehb@xanum.uam.mx (Carta-Cesión de Propiedad de Derechos de Autor).
Esta obra está bajo una licencia de Creative Commons Reconocimiento-No Comercial 4.0 Internacional.