Prospection of putative genes for digestive enzymes based on functional genome of the hepatopancreas of Amazon river prawn
Resumo
Over recent years, Macrobrachium amazonicum has become a popular species for shrimp farming due to their fast growth, high survival rates, and marketability. Several studies have focused on the development of new technology for the culture of this species, but many aspects of their nutrition and physiology remain unknown. Thus, the goal of the present study was to obtain transcripts of putative genes encoding digestive enzymes, based on a library of the cDNA from the hepatopancreas of M. amazonicum, sequenced in the Ion TorrentTM platform. We identified fragments of nine genes related to digestive enzymes, acting over proteins, carbohydrates and lipids. Endo and exoproteases were also recorded in the hepatopancreas, indicating adaptation to the digestion of protein-rich foods. Nonetheless, the enzymes involved in the carbohydrate metabolism formed the largest functional group in M. amazonicum, including enzymes related to the digestion of starch, chitin, and cellulose. These findings indicate that the species has a genetic apparatus of a well-adapted omnivorous animal. This information may provide important insights for the selection of ingredients for the formulation of a more appropriate diet to the enzymatic repertoire of M. amazonicum.
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Referências
Anger, K. (2013). Neotropical Macrobrachium (Caridea: Palaemonidae): on the biology, origin, and radiation of freshwater-invading shrimp. Journal of Crustacean Biology, 33(2), 151-183. DOI: https://doi.org/10.1163/1937240X-00002124
Anger, K., & Hayd, L. (2009). From lecithotrophy to planktotrophy : ontogeny of larval feeding in the Amazon River prawn Macrobrachium amazonicum. Aquatic Biology, 7(1-2), 19-30. DOI: https://doi.org/10.3354/ab00180
Aoki, H., Ahsan, M. N., & Watabe, S. (2003). Molecular cloning and characterization of cathepsin B from the hepatopancreas of northern shrimp Pandalus borealis. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 134(4), 681-694. DOI: https://doi.org/10.1016/S1096-4959(03)00023-X
Araújo, M. V. L. F., Silva, K. C. A., Silva, B. B., Ferreira, I. L. S., & Cintra, I. H. A. (2014). Pesca e Procedimentos de captura do camarão-da-amazônia a jusante de uma usina hidrelétrica na amazônia brasileira. Biota Amazônia, 4(2), 102-112. DOI: https://doi.org/10.18561/2179-5746/biotaamazonia.v4n2p102-112
Asaro, A., Del Valle, J. C., & Mañanes, A. A. L. (2011). Amylase, maltase and sucrase activities in hepatopancreas of the euryhaline crab Neohelice granulata (Decapoda: Brachyura: Varunidae): partial characterization and response to low environmental salinity. Scientia Marina, 75(3), 517-524.
Augusto, A., & Valenti, W. C. (2016). Are there any physiological differences between the male morphotypes of the freshwater shrimp Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae)? Journal of Crustacean Biology, 36(5), 716-723. DOI: https://doi.org/10.1163/1937240X-00002467
Berti, P. J., & Storer, A. C. (1995). Alignment/phylogeny of the papain superfamily of cysteine proteases. Journal of Molecular Biology, 246(2), 273-283. DOI: https://doi.org/10.1006/jmbi.1994.0083
Choct, M. (1997). Feed non-starch polysaccharides: chemical structures and nutritional significance. Feed Milling International, 6(1), 13-26.
Collins, P., Williner, V., & Giri, F. (2007). Trophic relationships in crustacean decapods of a river with a floodplain. In A. M. T. Elewa (Ed.), Predation in organisms (p. 59-86). Berlin, DE: Springer Berlin Heidelberg.
Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M., & Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18), 3676. DOI: https://doi.org/10.1093/bioinformatics/bti610
Coulombe, R., Grochulski, P., Sivaraman, J., Ménard, R., Mort, J. S., & Cygler, M. (1996). Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. The EMBO Journal, 15(20), 5492-5503. DOI: https://doi.org/10.1002/j.1460-2075.1996.tb00934.x
Dammannagoda, L. K., Pavasovic, A., Prentis, P. J., Hurwood, D. A., & Mather, P. B. (2015). Expression and characterization of digestive enzyme genes from hepatopancreatic transcripts from redclaw crayfish (Cherax quadricarinatus). Aquaculture Nutrition, 21(6), 868-880. DOI: https://doi.org/10.1111/anu.12211
David, F. S., Proença, D. C., & Valenti, W. C., (2017). Nitrogen budget in integrated aquaculture systems with Nile tilapia and Amazon River prawn. Aquaculture International, 25(1), 1733-1746.
Ding, Z. L., Kong, Y. Q., Li, J. F., Cao, F., Zhang, Y. X., Du, Z. Y., & Ye, J. Y. (2016). Growth and metabolic responses of juvenile Macrobrachium nipponense to different dietary carbohydrate levels. Aquaculture Nutrition, 23(5), 1136-1144. DOI: https://doi.org/10.1111/anu.12482
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41(1), 95-98.
Handford, M. G., Baldwin, T. C., Goubet, F., Prime, T. A., Miles, J., Yu, X., & Dupree, P. (2003). Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta, 218(1), 27-36. DOI: https://doi.org/10.1007/s00425-003-1073-9
Hedstrom, L. (2002). Serine Protease mechanism and specificity. Chemical Reviews, 102(12), 4501-4523. DOI: https://doi.org/10.1021/cr000033x
Hedstrom, L., Szilagyi, L., & Rutter, W. J. J. (1992). Converting trypsin to chymotrypsin: the role of surface loops. Science, 255(5049), 1249-1253. DOI: https://doi.org/10.1126/science.1546324
Heldt, A., Suita, S., Dutra, F. M., Pereira, A. L., & Ballester, E. (2019). Stable isotops as a method for analysis of the contribution of different ditary sources in the production of Macrobrachium amazonicum. Latin American Journal of Aquatic Research, 47(2), 282-29. DOI: https://doi.10.3856/vol47-issue2-fulltext-8
Henry-Silva, G. G., Maia, C. S. P., Moura, R. S. T., Bessa Junior, A. P., & Valenti, W. C. (2015). Integrated multi-trophic culture of Nile tilapia (Oreochromis niloticus) and Amazon river prawn (Macrobrachium amazonicum) in brackish water. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 67(1), 265-273. DOI: https://doi.org/10.1590/1678-6788
Holthuis, L. B. (1952). A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. II - The subfamily Palaemoninae (Occasional paper number 12). Los Angeles, CA: Allan Hancock Foundation Publications.
Hu, K. J., & Leung, P. C. (2004). Shrimp cathepsin L encoded by an intronless gene has predominant expression in hepatopancreas, and occurs in the nucleus of oocyte. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 137(1), 21-33. DOI: https://doi.org/10.1016/j.cbpc.2003.09.010
Hu, K. J., & Leung, P. C. (2007). Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 146(1), 69-80. DOI: https://doi.org/10.1016/j.cbpb.2006.09.010
Ishibashi, S., Brown, M. S., Goldstein, J. L., Gerard, R. D., Hammer, R. E., & Herz, J. (1993). Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. Journal of Clinical Investigation, 92(2), 883-893. DOI: https://doi.org/10.1172/JCI116663
Jiang, H., Cai, Y. M., Chen, L. Q., Zhang, X. W., Hu, S. N., & Wang, Q. (2009). Functional annotation and analysis of expressed sequence tags from the hepatopancreas of mitten crab (Eriocheir sinensis). Marine Biotechnology, 11(1), 317-326. DOI: https://doi.org/10.1007/s10126-008-9146-1
Jiang, K., Zhang, F., Zhang, D., Tao, Q., Zhang, Y., Pi, Y., … Ma, L. (2011). Identification of a trypsin gene from Scylla paramamosain and its expression profiling during larval development. African Journal of Agricultural Research, 6(32), 6613-6621. DOI: https://doi.org/10.5897/ajar11.784
Johnston, D. J. (2003). Ontogenetic changes in digestive enzyme activity of the spiny lobster, Jasus edwardsii (Decapoda; Palinuridae). Marine Biology, 143(1), 1071-1082. DOI: https://doi.org/10.1007/s00227-003-1154-0
Jung, H., Lyons, R. E., Hurwood, D. A., & Mather, P. B. (2013). Genes and growth performance in crustacean species: A review of relevant genomic studies in crustaceans and other taxa. Reviews in Aquaculture, 5(2), 77-110. DOI: https://doi.org/10.1111/raq.12005
Karrer, K. M., Peiffert, S. L., & Ditomas, M. E. (1993). Two distinct gene subfamilies within the family of cysteine protease genes Biochemistry. Proceedings of the National Academy of Sciences of the United States of America, 90(7), 3063-3067. DOI: https://doi: 10.1073/pnas.90.7.3063
Kensley, B., & Walker, I. (1982). Palaemonid Shrimps from the Amazon Basin, Brazil (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 362(1), 1-27. DOI: https://doi.org/10.5479/si.00810282.362
Kimpara, J. M., Rosa, F. R. T., Preto, B. L. & Valenti, W. C. (2011). Limnology of Macrobrachium amazonicum grow-out ponds subject to high inflow of nutrient-rich water and different stocking and harvest management. Aquaculture Research, 42(9), 1289-1297. DOI: https://doi.org/10.1111/j.1365-2109.2010.02717.x
King, A. J., Cragg, S. M., Li, Y., Dymond, J., Guille, M. J., Bowles, D. J., … McQueen-Mason, S. J. (2010). Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes. Proceedings of the National Academy of Sciences of the United States of America, 107(12), 5345-5350.
Le Boulay, C., Van Wormhoudt, A., & Sellos, D. (1995). Molecular cloning and sequencing of two cDNAs encoding cathepsin L-related cysteine proteinase in the nervous system and in the stomach of the Norway lobster (Nephops norvegicus). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 111B(3), 353-359. DOI: https://doi:10.1016/0305-0491(95)00001-o
Leone, F. A., Masui, D. C., Souza Bezerra, T. M., Garçon, D. P., Valenti, W. C., Augusto, A. S., & McNamara, J. C. (2012). Kinetic analysis of gill (Na +,K +)-ATPase activity in selected ontogenetic stages of the Amazon river shrimp, Macrobrachium amazonicum (Decapoda, Palaemonidae): Interactions at ATP- and cation-binding sites. The Journal of Membrane Biology, 245(4), 201-215. DOI: https://doi.org/10.1007/s00232-012-9431-9
Li, W. W., Jin, X. K., He, L., Jiang, H., Gong, Y. N., Xie, Y. N., & Wang, Q. (2010). Molecular cloning, characterization, expression and activity analysis of cathepsin L in Chinese mitten crab, Eriocheir sinensis. Fish & Shellfish Immunology, 29(6), 1010-1018. DOI: https://doi.org/10.1016/j.fsi.2010.08.007
Lima, J. D. F., Garcia, J. D. S., & Silva, T. C. D. (2014). Natural diet and feeding habits of a freshwater prawn (Macrobrachium carcinus: Crustacea, Decapoda) in the estuary of the Amazon River. Acta Amazonica, 44(2), 235-244. DOI: https://doi.org/doi.org/10.1590/S0044-59672014000200009
Maciel, C. R., & Valenti, W. C. (2014a). Assessing the potencial of partil replacing of Artemia by practical inert diet in the larviculture of the Amazon river prawn. Boletim do Instituto de Pesca, 40(1), 69-78.
Maciel, C. R., & Valenti, W. C. (2014b). Effect of tank colour on larval performance of the Amazon River prawn Macrobrachium amazonicum. Aquaculture Research, 45(6), 1041-1050. DOI: https://doi.org/10.1111/are.12048
Marques, H. L. A, & Moraes-Valenti, P. M. C. (2012). Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii (De Man 1879) and the Amazon river prawn Macrobrachium amazonicum (Heller 1862)) in Brazil. Aquaculture Research, 43(7), 984-992. DOI: https://doi.org/10.1111/j.1365-2109.2011.03032.x
Marques, H. L. A., Barros, H. P., Mallasen, M., Boock, M. V., & Moraes-Valenti, P. M. C. (2012). Influence of stocking densities in the nursery phase on the growth of Macrobrachium amazonicum reared in net pens. Aquaculture, 358-359(1), 240-245. DOI: https://doi.org/10.1016/j.aquaculture.2012.06.011
McGrath, M. E. (1999). The lysosomal cysteine proteases. Annual Review of Biophysics and Biomolecular Structure, 28(1), 181-204. DOI: https://doi.org/10.1146/annurev.biophys.28.1.181
Montoya Martinez, C., Carrillo Perez, C., Nolasco Soria, H., Alvarez Gonzalez, A., Carrillo Farnes, O., Civera Cerecedo, R., & Vega Villasante, F. (2018). Evaluation of different maze systems for the determination of feed attractability for longarm river prawn Macrobrachium tenellum. Latin American Journal of Aquatic Research, 46(3), 604-609. DOI: https://doi.org/10.3856/vol46-issue3-fulltext-15
Moraes-Valenti, P., & Valenti, W.C. (2010). Culture of the Amazon river prawn Macrobrachium Amazonicum. In: M. B. New, W.C. Valenti, J.H. Tidwell, L.R. D’Abramo, & M.N. Kutty (Eds.), Freshwater prawns: biology and farming (p. 485-501). Ames, IA : Wiley-Blackwell, Oxford.
Ong, S. S., Bhassu, S., Kwong, Q. B., Mather, P., Simarani, K., & Othman, R. Y. (2016). Identification of a putative cellulase gene in the giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879). Aquaculture Research, 47(11), 3653-3661. DOI: https://doi.org/10.1111/are.12818
Pinto, M. R., Lucena, M. N., Faleiros, R. O., Almeida, E. A., McNamara, J. C., & Leone, F. A. (2016). Effects of ammonia stress in the Amazon river shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Aquatic Toxicology (Amsterdam, Netherlands), 170(1), 13-23. DOI: https://doi.org/10.1016/j.aquatox.2015.10.021
Proespraiwong, P., Tassanakajon, A., & Rimphanitchayakit, V. (2010). Chitinases from the black tiger shrimp Penaeus monodon: Phylogenetics, expression and activities. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 156(2), 86-96. DOI: https://doi.org/10.1016/j.cbpb.2010.02.007
Rivera-Pérez, C., & García-Carreño, F. (2011). Effect of fasting on digestive gland lipase transcripts expression in Penaeus vannamei. Marine Genomics, 4(4), 273-278. DOI: https://doi.org/10.1016/j.margen.2011.07.002
Rodrigues, C. G., Garcia, B. F., Verdegem, M., Santos, M. R., Amorim, R. V., & Valenti, W. C. (2019). Integrated culture of Nile tilapia and Amazon river prawn in stagnant ponds, using nutrient-rich water and substrates. Aquaculture, 503(1), 111-117. DOI: https://doi.org/10.1016/j.aquaculture.2018.12.073
Saborowski, R. (2015). Nutrition and digestion. In E. S., Chang, M. Thiel, The Natural history of the crustacea (Vol. 4 Physiology, p. 285-319). Oxford, UK: University Press.
Salma, U., Uddowla, M. H., Kim, M., Kim, J. M., Kim, B. K., Baek, H. J., … Kim, H. W. (2012). Five hepatopancreatic and one epidermal chitinases from a pandalid shrimp (Pandalopsis japonica): cloning and effects of eyestalk ablation on gene expression. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 161(3), 197-207. DOI: https://doi.org/10.1016/j.cbpb.2011.11.005
Santos, F. M. S, Ribeiro, K., Júnior, A. C. V. F., Júnior, L. B. C., Valenti, W. C., & Bezerra, R. S. (2014). Digestive proteases from wild and farmed male morphotypes of the amazon river prawn (Macrobrachium amazonicum). Journal of Crustacean Biology, 34(2), 189-198. DOI: https://doi.org/10.1163/1937240X-00002215
Shi, X. Z., Ren, Q., Zhao, X. F., & Wang, J. X. (2009). Expression of four trypsin-like serine proteases from the Chinese shrimp, Fenneropenaeus chinensis, as regulated by pathogenic infection. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 153(1), 54-60. DOI: https://doi.org/10.1016/j.cbpb.2009.01.011
Soeiro, R. K. S., Rocha, C. P., Maciel, M., Abrunhosa, F. A., & Maciel, C. R. (2016). Relationship between the coastal origin of the freshwater prawn Macrobrachium amazonicum and salinity levels in the hatchery. Boletim do Instituto de Pesca, 42(3), 691-703. DOI: https://doi.org/10.20950/1678-2305.2016v42n3p691
Stephens, A., Rojo, L., Araujo-Bernal, S., Garcia-Carreño, F., & Muhlia-Almazan, A. (2012). Cathepsin B from the white shrimp Litopenaeus vannamei: cDNA sequence analysis, tissues-specific expression and biological activity. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 161(1), 32-40. DOI: https://doi.org/10.1016/j.cbpb.2011.09.004
Sun, S., Xuan, F., Ge, X., Fu, H., Zhu, J., & Zhang, S. (2014). Identification of differentially expressed genes in hepatopancreas of oriental river prawn, Macrobrachium nipponense exposed to environmental hypoxia. Gene, 534(2), 298-306. DOI: https://doi.org/10.1016/j.gene.2013.10.036
Thongsaiklaing, T., Sehawong, W., Kubera, A., & Ngernsiri, L. (2014). Analysis of the α-amylase gene sequence and the enzyme activity of Indian rock oyster Saccostrea forskali. Fisheries Science, 80(1), 589-601. DOI: https://doi.org/10.1007/s12562-014-0708-z
Van der Maarel, M. J. E. C., Van der Veen, B., Uitdehaag, J. C. M., Leemhuis, H., & Dijkhuizen, L. (2002). Properties and applications of starch-converting enzymes of the a-amylase family. Journal of Biotechnology, 94(2), 137-155. DOI: https://doi.org/10.1016/S0168-1656(01)00407-2
Van Wormhoudt, A. & Sellos, D. (1996). Cloning and Sequencing analysis of three amylase cDNAs in the shrimp Pennaeus vannamei (Crustacea decapoda): evolutionary aspects. Journal of Molecular Evolution, 42(1), 543-551.
Wang, S., Magoulas, C., & Hickey, D. A. (1993). Isolation and characterization of a full-length trypsin-encoding cDNA clone from the Lepidopteran insect, Choristoneura fumiferana. Gene, 136(1-2), 375-376. DOI: https://doi.org/10.1016/0378-1119(93)90501-S
Wang, W., Wu, X., Liu, Z., Zheng, H., & Cheng, Y. (2014) Insights into hepatopancreatic functions for nutrition metabolism and ovarian development in the crab Portunus trituberculatus: gene discovery in the comparative transcriptome of different hepatopancreas stages. PLoS ONE, 9(1), 1-15.
Watanabe, T., Kono, M., Aida, K., & Nagasawa, H. (1998). Purification and molecular cloning of a chitinase expressed in the hepatopancreas of the penaeid prawn Penaeus japonicus. Biochimica et Biophysica Acta, 1382(2), 181-185. DOI: https://doi.org/10.1016/S0167-4838(97)00184-2
Wattanakul, W., Wattanakul, U., Thongprajukaew, K., & Muenpo, C. (2015). Optimal protein replacement of fish meal by mackerel condensate in diet for giant freshwater prawn (Macrobrachium rosenbergii). Aquaculture Research, 48(2), 697-710. DOI: https://doi.org/10.1111/are.12916
Wei, J., Zhang, X., Yu, Y., Li, F., & Xiang, J. (2014). RNA-Seq reveals the dynamic and diverse features of digestive enzymes during early development of Pacific white shrimp Litopenaeus vannamei. Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics, 11(1), 37-44. DOI: https://doi.org/10.1016/j.cbd.2014.07.001
Zhang, S., Jiang, S., Xiong, Y., Fu, H., Sun, S., Qiao, H., … Gong, Y. (2014). Six chitinases from oriental river prawn Macrobrachium nipponense: cDNA characterization, classification and mRNA expression during post-embryonic development and moulting cycle. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 167(1), 30-40. DOI: https://doi.org/10.1016/j.cbpb.2013.09.009
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