Abstract
Intestinal microbiota play an important role in the intestinal immunity and nutrient absorption, even muscle nutritional components, and the composition and function were affected by environment. In this study, the intestinal microbiota and immune enzyme, nutritional flavor of muscle of crayfish in rice field, and pond cultivation model were compared in summer and autumn. The results of Shannon diversity and Chao 1 index of intestinal microbiota based on 16S sequencing analysis showed that the diversity and abundance in autumn were higher than in summer. And the diversity and abundance of intestinal microbiota of different model in the same season were different. Four dominant phyla (relative abundance > 5% at least in one sample) of the intestinal microbiota were Bacteroidetes, Firmicutes, Proteobacteria, and Tenericutes. From summer to autumn, the intestinal immune enzyme activity of crayfish in both models showed a decreasing trend. In summer, the activity of catalase and alkaline phosphatase of crayfish cultured in the pond was significantly higher than that in rice field (P < 0.05). In autumn, the activity of catalase and lysozyme of crayfish cultured in rice field was significantly higher than that in pond (P < 0.05). The contents of umami and sweetish amino acids of muscle were higher in rice field than in pond, and the percentage of glutamic acid and alanine was significantly higher in rice field than in pond (P < 0.05). Thus, rice field model can make crayfish a more stable intestinal environment and a better intestinal immune enzyme activity and muscular flavor.
Key points
• The intestinal microbiota of crayfish in rice field had tended to stabilize from summer to autumn.
• The crayfish had better nutrient absorption and stronger immune abilities in the rice field.
• The crayfish cultured in rice field had higher overall umami concentration than in pond.
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References
Alava VR, Quinitio ET, de Pedro JB, Priolo FMP, Orozco ZGA, Wille M (2007) Lipids and fatty acids in wild and pond-reared mud crab Scylla serrata (Forsskål) during ovarian maturation and spawning. Aquac Res 38(14):1468–1477. https://doi.org/10.1111/j.1365-2109.2007.01793.x
Apitanyasai K, Noonin C, Tassanakajon A, Söderhäll I, Söderhäll K (2016) Characterization of a hemocyte homeostasis-associated-like protein (HHAP) in the freshwater crayfish Pacifastacus leniusculus. Fish Shellfish Immunol 58:429–435. https://doi.org/10.1016/j.fsi.2016.09.038
Barbaresi S, Santini G, Tricarico E, Gherardi F (2004) Ranging behaviour of the invasive crayfish, Procambarus clarkii (Girard). J Nat Hist 38(22):2821–2832. https://doi.org/10.1080/00222930410001663308
Blandford MI, Taylor-Brown A, Schlacher TA, Nowak B, Polkinghorne A (2018) Epitheliocystis in fish: an emerging aquaculture disease with a global impact. Transbound Emerg Dis 65:1436–1446. https://doi.org/10.1111/tbed.12908
Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3(3):263–269. https://doi.org/10.1016/s1369-5274(00)00087-4
Chen D-W, Zhang M (2007) Non-volatile taste active compounds in the meat of Chinese mitten crab (Eriocheir sinensis). Food Chem 104(3):1200–1205. https://doi.org/10.1016/j.foodchem.2007.01.042
Dearing MD, Kohl KD (2017) Beyond fermentation: other important services provided to endothermic herbivores by their gut microbiota. Integr Comp Biol 57(4):723–731. https://doi.org/10.1093/icb/icx020
Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastro Hepat 9(10):577–589. https://doi.org/10.1038/nrgastro.2012.156
Gao S, Pan L, Huang F, Song M, Tian C, Zhang M (2018) Metagenomic insights into the structure and function of intestinal microbiota of the farmed Pacific white shrimp (Litopenaeus vannamei). Aquaculture. 499:109–118. https://doi.org/10.1016/j.aquaculture.2018.09.026
Geraylou Z, Rurangwa E, Wiele TVD, Courtin CM, Delcour JA, Buyse J, Ollevier F (2014) Fermentation of arabinoxylan-oligosaccharides, oligofructose and their monomeric sugars by hindgut bacteria from siberian sturgeon andafrican catfish in batch culture in vitro. J Aquac Res Development 03(3). https://doi.org/10.4172/2155-9546.1000230
Gong S, Lv J, Sun R, Li L, He X (2008) Studies on the reproductive biology of procambarus kirschner. Freshwater fisheries, 38(06):23–25+30
Guo H, Qi M, Hu ZJ, Liu Q (2020) Optimization of the rice-fish coculture in Qingtian, China: 1. Effects of rice spacing on the growth of the paddy fish and the chemical composition of both rie and fish. Aquaculture 522:735106. https://doi.org/10.1016/j.aquaculture.2020.735106
Iwashita MKP, Nakandakare IB, Terhune JS, Wood T, Ranzani-Paiva MJT (2015) Dietary supplementation with Bacillus subtilis, Saccharomyces cerevisiae and Aspergillus oryzae enhance immunity and disease resistance against Aeromonas hydrophila and Streptococcus iniae infection in juvenile tilapia Oreochromis niloticus. Fish Shellfish Immunol 43(1):60–66. https://doi.org/10.1016/j.fsi.2014.12.008
Li Y, Guo X, Cao X, Deng W, Luo W, Wang W (2012) Population genetic structure and post-establishment dispersal patterns of the red swamp crayfish Procambarus Clarkii in China. PLoS One 7(7):e40652. https://doi.org/10.1371/journal.pone.0040652
Meng X, Li W, Nie G (2019) Research progress on influencing factors of fish intestinal flora. J Fish China 43(01):143–155. https://doi.org/10.11964/jfc.20181011476
Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302(1–2):1–18. https://doi.org/10.1016/j.aquaculture.2010.02.007
Mitra A, Mukhopadhyay PK, Homechaudhuri S (2014) Understanding probiotic potentials of bacillus bacterial population isolated from Chitala chitala (Osteoglossiformes; Notopteridae) by comparing the enzyme activity in vitro. J Pure Appl Zool 2:120–127
Mouchet MA, Bouvier C, Bouvier T, Troussellier M, Escalas A, Mouillot D (2011) Genetic difference but functional similarity among fish gut bacterial communities through molecular and biochemical fingerprints. FEMS Microbiol Ecol 79(3):568–580. https://doi.org/10.1111/j.1574-6941.2011.01241.x
Nguyen DDL, Ngoc HH, Dijoux D, Loiseau G, Montet D (2008) Determination of fish origin by using 16S rDNA fingerprinting of bacterial communities by PCR-DGGE: an application on Pangasius fish from Viet Nam. Food Control 19(5):454–460. https://doi.org/10.1016/j.foodcont.2007.05.006
Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz JL (2010) Host–microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3(4):355–360. https://doi.org/10.1038/mi.2010.12
Ren WZ, Hu LL, Guo L, Zhang J, Tang L, Zhang ET, Zhang JE, Luo SM, Tang JJ, Chen X (2017) Preservation of the genetic diversity of a local common carp in the agricultural heritage rice-fish system. Proc Natl Acad Sci U S A 115(3):E546–E554. https://doi.org/10.1073/pnas.1709582115
Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A (2017) Proteobacteria: a common factor in human diseases. Biomed Res Int 2017:1–7. https://doi.org/10.1155/2017/9351507
Shao L, Wang C, He J, Wu X, Cheng Y (2013) Hepatopancreas and gonad quality of Chinese mitten crabs fattened with natural and formulated diets. J Food Qual 36(3):217–227. https://doi.org/10.1111/jfq.12030
She L (2018) Biological characteristics of crayfish and their main breeding patterns [J]. Hubei Agric Sci (1):75–78. https://doi.org/10.14088/j.cnki.issn0439-8114.2018.17.019
Sugita H, Miyajima C, Deguchi Y (1991) The vitamin B 12-producing ability of the intestinal micromicrobiota of freshwater fish. Aquaculture 92:267–276
Sun Y, Yang H, Ma R, Lin W (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(5):803–809. https://doi.org/10.1016/j.fsi.2010.07.018
Tang L, Yang J, Lin Y, Yao J (2018) Analysis of muscle nutrient composition of procambarus kirschner cultured in rice field in Guizhou province. Fisheries in Hebei Province, 297(09), 19-23+49. CNKI:SUN:HBYU.0.2018-09-003
Tao H, Du B, Wang H, Dong H, Yu D, Ren L, Sima Y, Xu S (2018) Intestinal microbiome affects the distinctive flavor of Chinese mitten crabs in commercial farms. Aquaculture 483:38–45. https://doi.org/10.1016/j.aquaculture.2017.09.031
Tilg H, Moschen AR (2014) Relevance of TNF-α gene polymorphisms in nonalcoholic fatty liver disease. Expert Rev Gastroent 5(2):155–158. https://doi.org/10.1586/egh.11.17
Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2008) A core gut microbiome in obese and lean twins. Nature 457(7228):480–484. https://doi.org/10.1038/nature07540
Uddin N, Al-Harbi AH (2012) Bacterial flora of polycultured common carp (Cyprinus carpio) and African catfish (Clarias gariepinus). Int Aquat Res 4(1):10. https://doi.org/10.1186/2008-6970-4-10
Wan NF, Li SX, Li T, Cavalieri A, Weiner J, Zheng XQ, Ji ZY, Zhang JQ, Zhang HL, Zhang H, Bai NL, Chen YJ, Zhang HY, Tao XB, Zhang HL, Lv WG, Jiang JX, Li B (2019) Ecological intenfification of rice production through rice-fish co-culture. J Clean Prod 234:1002–1012. https://doi.org/10.1016/j.jclepro.2019.06.238
Wang S, He Y, Wang Y, Tao N, Wu X, Wang X, Qiu W, Ma M (2016) Comparison of flavour qualities of three sourced Eriocheir sinensis. Food Chem 200:24–31. https://doi.org/10.1016/j.foodchem.2015.12.093
Wang Y, Wang B, Liu M, Jiang K, Wang M, Wang L (2018) Aflatoxin B1 (AFB1) induced dysregulation of intestinal microbiota and damage of antioxidant system in pacific white shrimp ( Litopenaeus vannamei ). Aquaculture 495:940–947. https://doi.org/10.1016/j.aquaculture.2018.06.065
Wu X, Cheng Y, Sui L, Yang X, Nan T, Wang J (2007) Biochemical composition of pond-reared and lake-stocked Chinese mitten crab Eriocheir sinensis (H. Milne-Edwards) broodstock. Aquac Res 38(14):1459–1467. https://doi.org/10.1111/j.1365-2109.2007.01728.x
Wu X, Cheng Y, Zeng C, Wang C, Yang X (2010) Reproductive performance and offspring quality of wild-caught and pond-reared swimming crab Portunus trituberculatus broodstock. Aquaculture 301(1–4):78–84. https://doi.org/10.1016/j.aquaculture.2010.01.016
Xia Z, Zhang J, Zhou Y, Peng L, Zheng D, Xia H (2020) Analysis on the status quo of crayfish quality safety standards in China. Modern Food Technol 36(03):310–318. https://doi.org/10.13982/j.mfst.1673-9078.2020.3.041
Yang S, Duan Y, Zhang J, Zhou J, Liu Y, Du J, Zhao L, Du Z, Han S (2017) Observational comparisons of intestinal microbiota characterizations, immune enzyme activities, and muscle amino acid compositions of loach in paddy fields and ponds in Sichuan Province. Appl Microbiol Biotechnol 101(11):4775–4789. https://doi.org/10.1007/s00253-017-8167-y
Yang S, Luo J, Long Y, Du J, Xu G, Zhao L, Du Z, Luo W, Wang Y, He Z (2019) Mixed diets reduce the oxidative stress of common carp (Cyprinus carpio): based on MicroRNA sequencing. Front Physiol 10. https://doi.org/10.3389/fphys.2019.00631
Zhang JY, Zhao YL, Ding YT, Gao F, Lv F (2018) Relationships of lipid oxidation and protein oxidation with flavor characteristics of meat products. J Nucl Agric Sci 32(7):1417–1424. https://doi.org/10.11869/j.issn.100-8551.2018.07.1417
Zhuang K, Wu N, Wang X, Wu X, Wang S, Long X, Wei X (2016) Effects of 3 feeding modes on the volatile and nonvolatile compounds in the edible tissues of female Chinese mitten crab (Eriocheir sinensis). J Food Sci 81(4):S968–S981. https://doi.org/10.1111/1750-3841.13229
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This research was supported by the multiple fishery and agricultural comprehensive culture technology and model (2019YFD0900305). It was also supported by the Special Fund for Agro-scientific Research in the Public Interest (201203081).
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Q. Liu, S. Yang, and Y.N. Long conceived and designed the experiments. S. Yang and J. Zhou supported the fund. Y.N. Long, L. Xu, Z.J. Du, and B. Li performed the experiments. L.L. Zhao, S. Yang, and Y.N. Long performed data analysis. Y.N. Long, W. Luo, J. Luo, and Q. Liu contributed to sample collection. Q. Liu and Y.N. Long wrote the paper. L.L. Zhao and S. Yang assisted with writing and proofreading. All authors read and approved the manuscript.
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The experiment was permitted by the Institutional Animal Care and Use Committee of the Sichuan Agricultural University.
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Liu, Q., Long, Y., Li, B. et al. Rice-shrimp culture: a better intestinal microbiota, immune enzymatic activities, and muscle relish of crayfish (Procambarus clarkii) in Sichuan Province. Appl Microbiol Biotechnol 104, 9413–9420 (2020). https://doi.org/10.1007/s00253-020-10797-4
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DOI: https://doi.org/10.1007/s00253-020-10797-4