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Effect of larval nutrition on the hemolymph protein composition during metamorphosis of Anastrepha obliqua

Published online by Cambridge University Press:  24 February 2022

Olivia Rincón-Betancurt
Affiliation:
Universidad Autónoma de Chiapas, Blvd. Príncipe Akishino S/N, Solidaridad 2000. Tapachula, Chiapas, 30798, México Programa Moscamed SADER-SENASICA, Camino a los Cacahotales S/N, Metapa de Domínguez, Chiapas, 30860, México
Marysol Aceituno-Medina*
Affiliation:
Universidad Autónoma de Chiapas, Blvd. Príncipe Akishino S/N, Solidaridad 2000. Tapachula, Chiapas, 30798, México Programa Moscamed SADER-SENASICA, Camino a los Cacahotales S/N, Metapa de Domínguez, Chiapas, 30860, México
Luz Verónica García-Fajardo
Affiliation:
El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto km 2.5, Tapachula, Chiapas, 30700 México
Emilio Hernández
Affiliation:
Universidad Autónoma de Chiapas, Blvd. Príncipe Akishino S/N, Solidaridad 2000. Tapachula, Chiapas, 30798, México Programa Moscamed SADER-SENASICA, Camino a los Cacahotales S/N, Metapa de Domínguez, Chiapas, 30860, México
*
Author for correspondence: Marysol Aceituno-Medina, Email: [email protected]

Abstract

Few studies have focused on how nutrition affects the bioavailability and investment of protein during the metamorphosis of tephritids. Our study allowed us to observe how the type and particle size of the bulking agent affected the protein composition in the hemolymph of the larva and adult of Anastrepha obliqua. Results indicated that, true protein bioavailability and protein profile was greatly modified by the bulking agent and its particle size. The physical structure of the food matrix affected the content of crude fiber (F), crude protein (P), F/P ratio, non-protein nitrogen, ammoniacal nitrogen, and α-amylase and trypsin inhibitors. Results from SDS-PAGE revealed 45 fractions with well-defined bands ranging from ~28 to ~401 kDa in larvae and adults, we found the main differences between the samples from different food matrices within the 75–100 kDa range. Hemolymph of adults from the coarse coconut fiber food matrix treatment showed a single band with a molecular weight close to 250 kDa, probably associated with a storage protein such as lipophorins. The food matrix with a coarse bulking agent had a high concentration of ammoniacal nitrogen, suggesting high microbial activity. In conclusion, the particle size of the bulking agent of the food matrix changes the bioavailability of protein in hemolymph in the adult regardless of the total concentration of protein. Also, when the particle size of the bulking agent favored the F/P ratio, higher larval density resulted in higher individual larval weight, larval yield, and adult emergence.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Aceituno-Medina, M and Hernández, H (2020) Dietas artificiales: evolución, retos y tendencias. In Montoya, P, Toledo, J and Hernandez, E (eds), Moscas de la Fruta: Fundamentos Y Procedimientos Para su Manejo. Ciudad de México: S y G editors, pp. 421448.Google Scholar
Aceituno-Medina, M, Rivera-Ciprian, JP and Hernández, E (2017) Influence of pupation substrate on mass production and fitness of adult Anastrepha obliqua Macquart (Diptera: Tephritidae) for Sterile Insect Technique application. Journal of Economic Entomology 110, 23972405.CrossRefGoogle ScholarPubMed
Aceituno-Medina, M, Rincón-Betancurt, O, Martínez-Salgado, RT and Hernández, E (2019) A novel, low-cost coconut fiber larval diet for mass rearing Anastrepha (Diptera: Tephritidae). Journal of Economic Entomology 20, 18.Google Scholar
Ademiluyi, AO, Oboh, G, Boligon, AA and Athayde, ML (2014) Effect of fermented soybean condiment supplemented diet on α-amylase and α-glucosidase activities in Streptozotocin-induced diabetic rats. Journal of Functional Foods 9, 19.CrossRefGoogle Scholar
Aguila, JR, Hoshizaki, DK and Gibbs, AG (2016) Contribution of larval nutrition to adult reproduction in Drosophila melanogaster. The Journal of Experimental Biology 216, 399406.Google Scholar
Aguilera, JM (2019) The food matrix: implications in processing, nutrition and health. Critical Reviews in Food Science and Nutrition 59, 36123629.CrossRefGoogle ScholarPubMed
Andersen, LH, Kristensen, TN, Loeschcke, V, Toft, S and Mayntz, D (2010) Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosophila melanogaster. Journal of Insect Physiology 56, 336340.CrossRefGoogle ScholarPubMed
AOAC (1990) Method 984.13 Cooper Catalyst Kjeldhal Method. Official Methods of Analysis of AOAC International. Arlington, Virginia. USA.Google Scholar
ASTM (1974) Standards for Bomb Calorimetry and Combustion Methods, American Society for Testing and Materials, Philadelphia, PA. USA.Google Scholar
Ben-Yosef, M, Pasternak, Z, Jurkevitch, E and Yuval, B (2014) Symbiotic bacteria enable olive flies (Bactrocera oleae) to exploit intractable sources of nitrogen. Journal of Evolutionary Biology 27, 26952705.CrossRefGoogle ScholarPubMed
Ben-Yosef, M, Pasternak, Z, Jurkevitch, E and Yuval, B (2015) Symbiotic bacteria enable olive fly larvae to overcome host defenses. Royal Society Open Science 2, 150170.CrossRefGoogle Scholar
Borzoui, E, Nouri-Ganbalani, G and Naseri, B (2017) In vitro and in vivo effects of α-amylase inhibitor from Avena sativa seeds on life history and physiological characteristics of Sitotroga cerealella (Lepidoptera: Gelechiidae). Journal of Insect Science 17, 17.CrossRefGoogle Scholar
Brock, HW and Roberts, DB (1981) Quantitative in situ hybridization reveals extent of sequence homology between related DNA sequences in Drosophila melanogaster. Chromosoma (Berl.) 83, 159168.CrossRefGoogle ScholarPubMed
Capuano, E, Oliviero, T, Fogliano, V and Pellegrini, N (2018) Role of the food matrix and digestion on calculation of the actual energy content of food. Nutrition Reviews 76, 274289.CrossRefGoogle ScholarPubMed
Carbonell-Capella, JM, Buniowska, M, Barba, FJ, Esteve, MJ and Frigola, A (2014) Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables: a review. Comprehensive Reviews in Food Science and Food Safety 13, 155171.CrossRefGoogle ScholarPubMed
Chrysanthis, G, Kaliafas, A and Mintzas, A (1994) Biosynthesis and tissue distribution of four major larval serum proteins during development of Ceratitis capitata (Diptera). Insect Biochemistry Molecular Biology 24, 811818.CrossRefGoogle Scholar
Chrysanthis, G, Marmaras, VJ and Christodoulou, C (1981) Major haemolymph proteins in Ceratitis capitata: biosynthesis and secretion during development. Wilhelm Roux's Archives of Developmental Biology 190, 3339.CrossRefGoogle ScholarPubMed
Cohen, AC (2004) Insect Diets: Science and Technology. Boca Raton, FL: CRC. Pressl.Google Scholar
Cohen, AC (2015) Insect Diets: Science and Technology. Boca Raton, FL: CRC. Press.CrossRefGoogle Scholar
Crawley, MJ (2013) The R Book. West Sussex, UK: John Wiley & Sons.Google Scholar
Crowe, KM (2013) Designing functional foods with bioactive polyphenols: highlighting lessons learned from original plant matrices. Journal of Human Nutrition & Food Science 1, 1018.Google Scholar
Darragh, AJ and Hodgkinson, SM (2000) Quantifying the digestibility of dietary protein. Journal of Nutrition 130, 1850S1856S.CrossRefGoogle ScholarPubMed
Dzionek, A, Wojcieszyńska, D and Guzik, U (2016) Natural carriers in bioremediation: a review. Electronic Journal of Biotechnology 23, 2836.CrossRefGoogle Scholar
FAO/IAEA/USDA (2014) Product Quality Control and Shipping Procedures for Sterile Mass-Reared Tephritid Fruit Flies.Manual, v.5.0. Joint FAO/IAEA, Vienna, Austria.Google Scholar
Frias, BED, Barbosa, CD and Lourenço, AP (2016) Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie 47, 1525.CrossRefGoogle Scholar
Fundo, JF, Quintas, MAC and Silva, CLM (2015) Molecular dynamics and structure in physical properties and stability of food systems. Food Engineering Reviews 7, 384392.CrossRefGoogle Scholar
Green, PW, Simmonds, MS and Blaney, WM (2002) Does the size of larval groups influence the effect of metabolic inhibitors on the development of Phormia regina (Diptera: Calliphoridae) larvae? European Journal of Entomology 99, 1922.CrossRefGoogle Scholar
Hahn, DA (2005) Larval nutrition affects lipid storage and growth, but not protein or carbohydrate storage in newly eclosed adults of the grasshopper Schistocerca americana. Journal of Insect Physiology 51, 12101219.CrossRefGoogle ScholarPubMed
Handke, B, Poernbacher, I, Goetze, S, Ahrens, CH, Omasits, U, Marty, F and Lehner, CF (2013) The hemolymph proteome of fed and starved Drosophila larvae. PLoS One 8, e67208.CrossRefGoogle ScholarPubMed
Hernández, E, Ruiz-Montoya, L, Toledo, J, Montoya, P, Liedo, P, Aceituno-Medina, M and Perales, H (2018) A comparison of sexual competitiveness and demographic traits of Anastrepha obliqua (Macquart) (Diptera: Tephritidae) among fruit-associated populations. Bulletin of Entomological Research 109, 333341.CrossRefGoogle ScholarPubMed
Hirayama, C, Konno, KT and Shinbo, H (1996) Utilization of ammonia as a nitrogen source in the Silkworm, Bombyx mori. Journal of Insect Physiology 42, 983988.CrossRefGoogle Scholar
Hyun, TK, Song, SC, Song, C-K and Kim, J-S (2015) Nutritional and nutraceutical characteristics of Sageretia theezans fruit. Journal of Food and Drug Analysis 23, 742749.CrossRefGoogle ScholarPubMed
Joye, I (2019) Protein digestibility of cereal products. Foods (basel, Switzerland) 8, 199.Google ScholarPubMed
Kakade, ML, Rackis, JJ, McGhee, JE and Puski, G (1974) Determination of trypsin inhibitor activity of soy products: a collaborative analysis of an improved procedure. Cereal Chemistry 51, 376382.Google Scholar
Kansal, R, Gupta, RN, Koundal, KR, Kuhar, K and Gupta, VK (2008) Purification, characterization and evaluation of insecticidal potential of trypsin inhibitor from mungbean (Vigna radiata L. Wilczek) seeds. Acta Physiologiae Plantarum 30, 761768.CrossRefGoogle Scholar
Keebaugh, ES, Yamada, R, Obadia, B, Ludington, WB and Ja, WW (2018) Microbial quantity impacts Drosophila nutrition, development, and lifespan. iScience 4, 247259.CrossRefGoogle ScholarPubMed
Laemmli, UK (1970) Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature 227, 680685.CrossRefGoogle ScholarPubMed
Lawrence, PK and Koundal, KR (2002) Plant protease inhibitors in control of phytophagous insects. Electronic Journal of Biotechnology 5, 93109.CrossRefGoogle Scholar
Lazarevíc, J and Janković-Tomanić, M (2015) Dietary and phylogenetic correlates of digestive trypsin activity in insect pests. Entomologia Experimentalis et Applicata 157, 123151.CrossRefGoogle Scholar
Levenbook, L (1985) Insect storage proteins. In Kerkut, GA and Gilbert, LI (eds), Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford, UK: Pergamon Press, pp. 307346.Google Scholar
Littlefair, JE and Knell, RJ (2016) Within- and trans-generational effects of variation in dietary macronutrient content on life-history traits in the moth Plodia interpunctella. PLoS ONE 11, e0168869.CrossRefGoogle ScholarPubMed
Matveev, YI, Grinberg, VY and Tolstoguzov, VB (2000) The plasticizing effect of water on proteins, polysaccharides and their mixtures. Glassy state of biopolymers, food and seeds. Food Hydrocolloids 14, 425437.CrossRefGoogle Scholar
Mintzas, AC and Rina, MD (1986) Isolation and characterization of three major larval serum proteins of the Mediterranean fruit fly Ceratitis capitata (Diptera). Insect Biochemistry 16, 825835.CrossRefGoogle Scholar
Nash, WJ and Chapman, T (2014) Effect of dietary components on larval life history characteristics in the medfly (Ceratitis capitata: Diptera,Tephritidae). PLoS ONE 9, e86029.CrossRefGoogle Scholar
Nestel, D, Nemny-Lavy, E and Chang, CL (2004) Lipid and protein loads in pupating larvae and emerging adult as affected by the composition of a Mediterranean fruit fly (Ceratitis capitata) meridic larval diets. Archives of Insect Biochemistry and Physiology 56, 97109.CrossRefGoogle Scholar
Nguyen, KT, Kim, JM, Park, SE and Hwang, CS (2019) N-terminal methionine excision of proteins creates tertiary destabilizing N-degrons of the Arg/N-end rule pathway. Journal of Biological Chemistry 294, 44644476.CrossRefGoogle ScholarPubMed
NMX-Y-094-SCFI (2012) Crude fiber determination in finished feeds and ingredients-test method. Secretaria de Economia. Ciudad de México, México.Google Scholar
NMX-Y-346-SCFI (2007) Determination of non-protein nitrogen in ingredients and foods finished for consumption animal –test method. Secretaria de Economia, Ciudad de México, México.Google Scholar
NOM-242-SSA1 (2009) Productos y servicios. Productos de la pesca frescos, refrigerados, congelados y procesados. Especificaciones sanitarias y métodos de prueba. Secretaria de Economia. Ciudad de México, México.Google Scholar
Orozco-Dávila, D, Quintero, L, Hernandez, E, Solis, E, Artiaga, T, Hernandez, R, Ortega, C and Montoya, P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. Pests in méxico – a review. Entomologia Experimentalis et Applicata 164, 176187.CrossRefGoogle Scholar
Palma, L, Fernandez-Bayo, J, Niemeier, D, Pitesky, M and VanderGheynst, JS (2019) Managing high fiber food waste for the cultivation of black soldier fly larvae. Science of Food 3, 15.Google ScholarPubMed
Parada, J and Aguilera, M (2007) Food microestructure affects the bioavailability of several nutrients. Journal of Food Science 72, 2132.CrossRefGoogle Scholar
Polloni, YJ and Telles, MDC (1989) Anastrepha obliqua oviposition capacity in laboratory- 1. Effects of population density. pp. 169–178 in Cavalloro R. (ed.). Fruit flies of economic importance 87, Proceedings of the CEC/IOBC International Symposium. Rome 7–10 April 1987. The Netherlands. A.A. Balkena, Rotterdam.Google Scholar
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.Rproject.org/ (accessed on 10 April 2021).Google Scholar
Rina, MD and Mintzas, AC (1988) Biosynthesis and regulation of two vitellogenins in the fat body and ovaries of Ceratitis capitata (Diptera). Roux s Archives of Developmental Biology 197, 167174.CrossRefGoogle Scholar
Rincón-Betancurt, O, Aceituno-Medina, M, García-Fajardo, LV and Hernández, E (2020) Big particles, best nutrition? Absorption and excretion of protein by Anastrepha obliqua larvae (Diptera: Tephritidae). Bulletin of Entomological Research 111, 210216. doi: 10.1017/S0007485320000577CrossRefGoogle Scholar
Samtiya, M, Aluko, RE and Dhewa, T (2020) Plant food anti-nutritional factors and their reduction strategies: an overview. Food Production, Processing and Nutrition 2, 114. doi: 10.1186/s43014-020-0020-5.CrossRefGoogle Scholar
Smith, P, Krohn, R, Hermanson, G, Mallia, A, Gartner, F, Frovenzano, M, Fujimoto, E, Goeke, N, Olson, J and Klenk, C (1985) Measurement of protein using bicinchoninic acid. Analytical Biochemistry 19, 7685.CrossRefGoogle Scholar
Sun, X, Zhang, Y, Li, J, Asham, N, Sun, H, Zhao, J, Wu, Z and He, S (2019) Effects of particle size on physicochemical and functional properties of superfine black kidney bean (Phaseolus vulgaris L.) powder. Peer J 7, e6369.CrossRefGoogle ScholarPubMed
Tabunoki, H, Dittmer, NT, Gorman, MJ and Kanost, MR (2019) Development of a new method for collecting hemolymph and measuring phenoloxidase activity in Tribolium castaneum. BMC Research Notes 12, 7.CrossRefGoogle ScholarPubMed
Telang, A, Buck, NA and Wheeler, DE (2002) Response of storage protein levels to variation in dietary protein levels. Journal of Insect Physiology 48, 10211029.CrossRefGoogle ScholarPubMed
Van Dung, D, Shang, W and Yao, W (2014) Effect of crude protein levels in concentrate and concentrate levels in diet on In vitro fermentation. Asian-Australasian Journal of Animal Sciences 27, 797805.CrossRefGoogle ScholarPubMed
Wong, S, Batt, B and Robertson, H (2000) Microassay for rapid screening of alfa-amylase activity. The Journal of Agricultural and Food Chemistry 48, 45404543.CrossRefGoogle Scholar
Zhang, Y, Dong, Z, Wang, D, Wu, Y, Song, Q, Gu, P, Zhao, P and Xia, Q (2014) Proteomics of larval hemolymph in Bombyx mori reveals various nutrient-storage and immunity related proteins. Amino Acids 46, 10211031. doi: 10.1007/s00726-014-1665-7CrossRefGoogle ScholarPubMed
Zhao, A, Li, Y, Leng, C, Wang, P and Li, Y (2019) Inhibitory effect of protease inhibitors on larval midgut protease activities and the performance of Plutella xylostella (Lepidoptera: Plutellidae). Frontiers in Physiology 9, 1963.CrossRefGoogle Scholar