Antinutritional effect of lectin from faveira (Parkia platycephala) seeds in tambatinga (Colossoma macropomum x Piaractus brachypomus)

Rafael Carvalho Da Silva; Claudener Souza Teixeira; Alexandra Pretto; Thaisa Sales Costa; Jefferson Costa de Siqueira; Bruna Tássia Santos Pantoja; Bernardo Baldisserotto; Jane Mello Lopes

doi:10.20950/1678-2305/bip.2022.48.e745

Authors

Rafael Carvalho Da Silva Universidade Federal Rural do Rio de Janeiro, Programa de Pós-Graduação em Zootecnia – Seropédica (RJ), Brazil. https://orcid.org/0000-0002-2543-3561
Claudener Souza Teixeira Universidade Federal do Cariri, Centro de Ciências Agrárias e da Biodiversidade – Crato (CE), Brazil. https://orcid.org/0000-0002-9792-0369
Alexandra Pretto Universidade Federal do Pampa, Curso Superior de Tecnologia em Aquicultura – Uruguaiana (RS), Brazil. https://orcid.org/0000-0002-5874-9108
Thaisa Sales Costa Universidade Federal do Maranhão, Centro de Ciências de Chapadinha – Chapadinha (MA), Brazil. https://orcid.org/0000-0001-5994-8830
Jefferson Costa de Siqueira Universidade Federal do Maranhão, Centro de Ciências de Chapadinha – Chapadinha (MA), Brazil. https://orcid.org/0000-0002-6692-0972
Bruna Tássia Santos Pantoja Universidade Federal do Maranhão, Centro de Ciências de Chapadinha – Chapadinha (MA), Brazil. https://orcid.org/0000-0002-9164-1940
Bernardo Baldisserotto Universidade Federal de Santa Maria, Departamento de Fisiologia e Farmacologia – Santa Maria (RS), Brazil. https://orcid.org/0000-0002-8770-0100
Jane Mello Lopes Universidade Federal do Maranhão, Centro de Ciências de Chapadinha – Chapadinha (MA), Brazil. https://orcid.org/0000-0003-0396-3104

DOI:

https://doi.org/10.20950/1678-2305/bip.2022.48.e745

Keywords:

alternative feeds, 6-dimethylaminopurine, lectins

Abstract

This study investigated the possible antinutritional effects of Parkia platycephala lectin (0, 20, 40, or 60 mg kg^-1 of diet) on tambatinga feeding for 60 days as well as methods of inactivating this protein. Weight gain, specific growth rate, and relative weight gain decreased, and the feed conversion rate increased with the increase in dietary lectin. The hepatic glycogen levels of fish fed 60 mg kg^-1 were higher than those of fish fed 20 and 40 mg kg^-1. Diets containing 40 and 60 mg kg^-1 increased muscle glucose levels compared to the control group. Fish-fed diets containing lectin showed reduced muscle glycogen compared to those receiving the control diet. Fish fed 60 mg kg^-1 presented lower muscle protein levels than those fed 20 mg kg^-1. In vitro tests showed that the hemagglutination activity of lectin was inhibited by d-mannose, d-glucose, and α-methyl-d-mannopyranoside. Thermal treatment at 50–60°C was sufficient to reduce the action of lectin, as well as a pH below and above the 6–7 range. Therefore, the use of P. platycephala meals as a dietary ingredient for tambatinga with no lectin inactivation is not recommended as it can negatively affect the fish’s biochemical parameters and growth. Acid or alkaline solutions can be an alternative for inactivating the protein and improving its use by fish and other animals.

References

Aanyu, M.; Ondhoro, C.C.; Ganda, E.; Kato, D.C.; Basiita, R.K. 2014. Intestine histology, nutrient digestibility and body composition of Nile tilapia (Oreochromis niloticus) fed on diets with both cotton and seed cakes. African Journal of Biotechnology, 13(37): 3831-3839. https://doi.org/10.5897/AJB12.1895

Abafi, J.; Aliyu-Paiko, M.; Adamu, K.M.; King, M.A. 2019. Dietary inclusion of fermented parkia in feeds as an organic strategy to improve feed quality and antioxidant parameters of African catfish (Clarias gariepinus) fingerlings. Asian Journal of Biotechnology and Bioresource Technology, 5: 1-14. https://doi.org/10.9734/ajb2t/2019/v5i330059

Abdul-Qadir, A.M.; Mohammad, A.P.; Adamu, K.M.; Abdurraheem, A.A. 2020. Inclusion of Sargassum muticum and Parkia biglobosa in diets for African Catfish (Clarias gariepinus) elevates feed utilization, growth and immune parameters. African Journal of Agricultural Research, 15(1): 134-139. https://doi.org/10.5897/AJAR2019.14189

Alves, A.A.; Sales, R.O.; Neiva, J.N.M.; Medeiros, A.N.; Braga, A.P.; Azevedo, A.R. 2007. Degradabilidade ruminal in situ de vagens de faveira (Parkia platycephala Benth.) em diferentes tamanhos de partículas. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59(4): 1045-1051. https://doi.org/10.1590/S0102-09352007000400034

Araújo, M.J.; Miranda, H.H.; Marques, C.A.T.; Batista, I.L.; Carvalho, F.J.V.; Jácome, D.L.S.; Edvan, R.L.; Silva, T.P.D.; Bezerra, L.R.; Lima, A.G.V.O.; Oliveira, R.L. 2019. Eﬀect of replacing ground corn with Parkia platycephala pod meal on the performance of lactating Anglo-Nubian goats. Animal Feed Science and Technology, 258: 114313. https://doi.org/10.1016/j.anifeedsci.2019.114313

Batista, K.L.R.; Silva, C.R.; Santos, V.F.; Silva, R.C.; Roma, R.R.; Santos, A.L.E.; Pereira, R.O.; Delatorre, P.; Rocha, B.A.M.; Soares, A.M.S.; Costa-Júnior, L.M.; Teixeira, C.S. 2018. Structural analysis and anthelmintic activity of Canavalia brasiliensis lectin reveal molecular correlation between the carbohydrate recognition domain and glycans of Haemonchus contortus. Molecular & Biochemical Parasitology, 225: 67-72. https://doi.org/10.1016/j.molbiopara.2018.09.002

Bidinotto, P.M.; Moraes, G.; Souza, R.H.S. 1997. Hepatic glycogen and glucose in eight tropical freshwater teleost fish: A procedure for field determinations of micro samples. Boletim Técnico do CEPTA, 10: 53-60.

Cavada, B.S.; Santos, C.F.; Grangeiro, T.B.; Silva, L.I.M.M.; Campos, M.J.O.; Souza, F.A.M.; Calvette, J.J. 1997. Isolation and partial characterization of a lectin from Parkia platycephala Benth seeds. Physiology and Molecular Biology of Plants, 3: 109-115.

Cook, J.T.; Mcniven, M.A.; Richardson, G.F.; Sutterlin, A.M. 2000. Growth rate, body composition and feed digestibility/conversion of growth enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture, 188(1-2): 15-32. https://doi.org/10.1016/S0044-8486(00)00331-8

Del Sol, F.G.; Nagano, C.S.; Cavada, B.S.; Calvette, J.J. 2005. The ﬁrst crystal structure of a mimosoideae lectin reveals a novel quaternary arrangement of a widespread domain. Journal of Molecular Biology, 353(3): 574-583. https://doi.org/10.1016/j.jmb.2005.08.055

Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28(3): 350-356. https://doi.org/10.1021/ac60111a017

Harrower, J.R.; Brown, C.H. 1972. Blood lactic acid—a micromethod adapted to field collection of microliter samples. Journal of Applied Physiology, 32(5): 709-711. https://doi.org/10.1152/jappl.1972.32.5.709

Hart, S.D.; Bharadwaj, A.S.; Brown, P.B. 2010. Soybean lectins and trypsin inhibitors, but not oligosaccharides or the interactions of factors, impact weight gain of rainbow trout (Oncorhynchus mykiss). Aquaculture, 306(1-4): 310-314. https://doi.org/10.1016/j.aquaculture.2010.03.027

Hashimoto, D.T.; Mendonça, F.F.; Senhorini, J.A.; Oliveira, C.; Foresti, F.; Porto-Foresti, F. 2011. Molecular diagnostic methods for identifying Serrasalmid fish (Pacu, Pirapitinga, and Tambaqui) and their hybrids in the Brazilian aquaculture industry. Aquaculture, 321(1-2): 49-53. https://doi.org/10.1016/j.aquaculture.2011.08.018

Lopes, J.M.; Marques, N.C.; Santos, M.D.M.C.; Souza, C.F.; Baldissera, M.D.; Carvalho, R.C.; Santos, L.L.; Pantoja, B.T.S.; Heinzmann, B.M.; Baldisserotto, B. 2020. Dietary limon Citrus × latifolia fruit peel essential oil improves antioxidant capacity of tambaqui (Colossoma macropomum) juveniles. Aquaculture Research, 51(12): 4852-4862. https://doi.org/10.1111/are.14771

Lowry, O.H.; Rosebrough, N.J.; Farra, L.; Randall, R.J. 1951. Protein measurement with the Folin Phenol Reagent. Journal of Biological Chemistry, 193(1): 265-275.

Makkar, H.P.S. 2016. State-of-the-art on detoxification of Jatropha curcas products aimed for use as animal and fish feed: A review. Animal Feed Science and Technology, 222: 87-99. https://doi.org/10.1016/j.anifeedsci.2016.09.013

Martins, G.P.; Pezzato, L.E.; Guimarães, I.G.; Padovani, C.R.; Mazini, B.S.M.; Barros, M.M. 2017. Antinutritional factors of raw soybean on growth and haematological responses of Nile tilapia. Boletim do Instituto de Pesca, 43(3): 322-333. https://doi.org/10.20950/1678-2305.2017v43n3p322

Michael, K.G.; Mathias, A.I. 2020. Growth performance of Clarias gariepinus fed locust bean meal (Parkia biglobosa) supplemented diets. International Journal of Fisheries and Aquatic Studies, 8(1): 266-270.

Mohan, V.R.; Tresina, P.S.; Daffodil, E.D. 2016. Antinutritional factors in legume seeds: Characteristics and determination. In: Caballero, B.; Finglas, P.; Toldrá, F. (eds). The encyclopedia of food and health. Oxford: Academic Press, p. 211-220.

Moreira, R.A.; Perrone, J.C. 1977. Purification and partial characterization of a lectin from Phaseolus vulgaris. Plant Physiology, 59(5): 783-787. https://doi.org/10.1104%2Fpp.59.5.783

Musa, S.O.; Tiamiyu, L.O.; Solomon, S.G.; Ayuba, V.O.; Okomoda, V.T. 2018. Nutritional value of hydrothermally processed Jatropha curcas kernel and its effect on growth and hematological parameters of Clarias gariepinus fingerlings (Burchell, 1982). Aquaculture Reports, 10: 32-38. https://doi.org/10.1016/j.aqrep.2018.04.001

Oishi, C.A.; Nwanna, L.W.; Pereira Filho, M. 2010. Optimum dietary protein requirement for Amazonian Tambaqui, Colossoma macropomum Cuvier, 1818, fed fish meal free diets. Acta Amazonica, 40(4): 757-762. https://doi.org/10.1590/S0044-59672010000400017

Popova, A.; Mihaylova, D. 2019. Antinutrients in plant-based foods: a review. Open Biotechnology Journal, 13: 68-76. https://doi.org/10.2174/1874070701913010068

Pretto, A.; Silva, L.P.; Corrêia, V.; Martinelli, S.G. 2020. Effect of feeding crude or treated tung meal (Aleurites fordii) in the diet of Rhamdia quelen on growth, digestive enzymes and biochemical parameters. Ciência Animal Brasileira, 21: 46276. https://doi.org/10.1590/1809-6891v21e-46276

Prophet, E.B.; Mills, B.; Arrington, J.B.; Sobin, L.H. 1992. Laboratory methods in histotechnology. Washington, D.C.: American Registry of Pathology, Armed Forces Institute of Pathology. 279 p.

Ribeiro, P.F.; Leite, L.A.; Quaresma, F.S.; Farias, W.R.L.; Sampaio, A.H. 2019. Dietary supplementation with Arthrospira platensis in tambatinga (Colossoma macropomum × Piaractus brachypomus). Ciência Agronômica, 50: 600-608. https://doi.org/10.5935/1806-6690.20190071

Santos, A.L.E.; Leite, G.O.; Carneiro, R.F.; Roma, R.R.; Santos, V.F.; Santos, M.H.C.; Pereira, R.O.; Silva, R.C.; Nagano, C.S.; Sampaio, A.H.; Rocha, B.A.M.; Delatorre, P.; Campos, A.R.; Teixeira, C.S. 2019. Puriﬁcation and biophysical characterization of a mannose/N-acetyl-D-glucosamine-speciﬁc lectin from Machaerium acutifolium and its eﬀect on inhibition of orofacial pain via TRPV1 receptor. Archives of Biochemistry and Biophysics, 664: 149-156. https://doi.org/10.1016/j.abb.2019.02.009

Silva, R.R.S.; Silva, C.R.; Santos, V.F.; Barbosa, C.R.S.; Muniz, D.F.; Santos, A.L.E.; Santos, M.H.C.; Rocha, B.A.M.; Batista, K.L.R.; Costa-Júnior, L.M.; Coutinho, H.D.M.; Teixeira, C.S. 2019. Parkia platycephala lectin enhances the antibiotic activity against multi-resistant bacterial strains and inhibits the development of Haemonchus contortus. Microbial Pathogenesis, 135: 103629. https://doi.org/10.1016/j.micpath.2019.103629

Soares, K.J.A.; Ribeiro, F.; Bomfim, M.A.D.; Marchão, R.S. 2017. Valor nutricional de alimentos alternativos para tambaqui (Colossoma macropomum). Archivos de Zootecnia, 66(256): 491-498. https://doi.org/10.21071/az.v66i256.2764

Von Danwitz, A.; Schulz, C. 2020. Effects of dietary rapeseed glucosinolates, sinapic acid and phytic acid on feed intake, growth performance and fish health in turbot (Psetta maxima L.). Aquaculture, 516: 734624. https://doi.org/10.1016/j.aquaculture.2019.734624

Welengane, E.; Sado, R.Y.; Bicudo, A.J.A. 2019. Protein‐sparing effect by dietary lipid increase in juveniles of the hybrid fish tambatinga (Colossoma macropomum × Piaractus brachypomus). Aquaculture Nutrition, 25(6): 1272-1280. https://doi.org/10.1111/anu.12941

Xiang, Y.; Song, M.; Wei, Z.; Tong, J.; Zhang, L.; Xiao, L.; Ma, Z.; Wang, Y. 2011. A jacalin- related lectin-like gene in wheat is a component of the plant defence system. Journal of Experimental Botany, 62(15): 5471-5483. https://doi.org/10.1093/jxb/err226