Enhancing biomass and ecological sustainability in rice–fish cocropping systems through the induction of functional microbiota with compound biogenic bait

Abstract

● Compound biological bait can replace commercial bait to ensure fish growth.

● The compound biogenic bait can effectively improve the water and soil environment.

● The key microbiome induced by compound biogenic bait plays an important role.

Traditional commercial aquatic fish bait (CA) is not conducive to the scientific breeding of rice and fish in cocropping systems, and excessive feeding easily causes environmental pollution in rice fields. In this study, an environment-friendly compound biogenic bait (CB) mixed with plant-derived (PB) and animal-derived (AB) baits was proposed. The rice–crucian carp cocropping system was used as the research object, and the soil microorganisms and fish gut microorganisms were sequenced with high throughput, respectively, to verify the effect of CB application and the microbial mechanism underlying its functional effect. The results showed that the AB and PB components in CB maintain the growth of fish by improving the metabolism-related functions of fish gut microbiome and reducing the abundance of intestinal pathogenic bacteria, including Actinomadura. In particular, the PB components induced soil microbiome, such as Pseudonocardia, that participate in soil nutrient cycling and increase dissolved oxygen in water, which is key for improving rice quality and yield. This is the first study to focus on how different bait components drive key microbial communities to regulate animal–plant–environment relationships in the integrated planting and breeding patterns of paddy fields.

Graphical abstract

Keywords

rice soil / rice–fish cocropping / fish bait / high-throughput sequencing / microbial community

References

[1] Ahmad, M.T., Shariff, M., Yusoff, F., Goh, Y.M., Banerjee, S., 2020. Applications of microalga Chlorella vulgaris in aquaculture. Reviews in Aquaculture12, 328–346.

[2] Arias-Jayo, N., Abecia, L., Alonso-Sáez, L., Ramirez-Garcia, A., Rodriguez, A., Pardo, M.A., 2018. High-fat diet consumption induces microbiota dysbiosis and intestinal inflammation in zebrafish. Microbial Ecology76, 1089–1101.

[3] Barbee, G.C., McClain, W.R., Lanka, S.K., Stout, M.J., 2010. Acute toxicity of chlorantraniliprole to non-target crayfish (Procambarus clarkii) associated with rice–crayfish cropping systems. Pest Management Science66, 996–1001.

[4] Borre, Y.E., Moloney, R.D., Clarke, G., Dinan, T.G., Cryan, J.F., 2014. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. In: Lyte, M., Cryan, J.F., eds. Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease. New York: Springer, 373–403

[5] Butt, R.L., Volkoff, H., 2019. Gut microbiota and energy homeostasis in fish. Frontiers in Endocrinology10, 9.

[6] Cani, P.D., Knauf, C., 2016. How gut microbes talk to organs: the role of endocrine and nervous routes. Molecular Metabolism5, 743–752.

[7] Chaparro, J.M., Sheflin, A.M., Manter, D.K., Vivanco, J.M., 2012. Manipulating the soil microbiome to increase soil health and plant fertility. Biology and Fertility of Soils48, 489–499.

[8] Chen, J.Y., Li, Q.Y., Tan, C.Y., Xie, L.Q., Yang, X.J., Zhang, Q.L., Deng, X.Y., 2023. Effects of enrofloxacin's exposure on the gut microbiota of Tilapia fish (Oreochromis niloticus). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics46, 101077.

[9] Cole, J.R., Wang, Q., Fish, J.A., Chai, B.L., McGarrell, D.M., Sun, Y.N., Brown, C.T., Porras-Alfaro, A., Kuske, C.R., Tiedje, J.M., 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research42, D633–D642.

[10] Ding, W.H., Li, N.N., Ren, W.Z., Hu, L.L., Chen, X., Tang, J.J., 2013. Effects of improved traditional rice-fish system productivity on field water environment. Acta Automatica Sinica21, 308–314.

[11] Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics26, 2460–2461.

[12] Fageria, N.K., 2007. Yield physiology of rice. Journal of Plant Nutrition30, 843–879.

[13] Frąc, M., Hannula, S.E., Bełka, M., Jędryczka, M., 2018. Fungal biodiversity and their role in soil health. Frontiers in Microbiology9, 707.

[14] Franchini, P., Fruciano, C., Frickey, T., Jones, J.C., Meyer, A., 2014. The gut microbial community of Midas cichlid fish in repeatedly evolved limnetic-benthic species pairs. PLoS One9, e95027.

[15] Goldstein, E.J.C., Citron, D.M., Peraino, V.A., Cross, S.A., 2003. Desulfovibrio desulfuricans bacteremia and review of human Desulfovibrio infections. Journal of Clinical Microbiology41, 2752–2754.

[16] Halwart, M., Gupta, M.V., 2004. Culture of Fish in Rice Fields. Rome: FAO and The WorldFish Center

[17] Hlordzi, V., Kuebutornye, F.K.A., Afriyie, G., Abarike, E.D., Lu, Y.S., Chi, S.Y., Anokyewaa, M.A., 2020. The use of Bacillus species in maintenance of water quality in aquaculture: a review. Aquaculture Reports18, 100503.

[18] Ju, F., Guo, F., Ye, L., Xia, Y., Zhang, T., 2014. Metagenomic analysis on seasonal microbial variations of activated sludge from a full-scale wastewater treatment plant over 4 years. Environmental Microbiology Reports6, 80–89.

[19] Kim, S.H., Kim, H.C., Choi, S.H., Lee, W.C., Jung, R.H., Hyun, J.H., Kim, S.H., Lee, J.S., 2020. Benthic respiration and nutrient release associated with net cage fish and longline oyster aquaculture in the geoje-tongyeong coastal waters in Korea. Estuaries and Coasts43, 589–601.

[20] Kong, W.W., Huang, S.L., Yang, Z.J., Shi, F.F., Feng, Y.B., Khatoon, Z., 2020. Fish feed quality is a key factor in impacting aquaculture water environment: evidence from incubator experiments. Scientific Reports10, 187.

[21] Kong, W.W., Xu, Q.J., Lyu, H., Kong, J., Wang, X., Shen, B.X., Bi, Y.H., 2023. Sediment and residual feed from aquaculture water bodies threaten aquatic environmental ecosystem: interactions among algae, heavy metals, and nutrients. Journal of Environmental Management326, 116735.

[22] Könönen, E., Wade, W.G., 2015. Actinomyces and related organisms in human infections. Clinical Microbiology Reviews28, 419–442.

[23] Kotani, T., Kawashima, Y., Yurimoto, H., Kato, N., Sakai, Y., 2006. Gene structure and regulation of alkane monooxygenases in propane-utilizing Mycobacterium sp. TY-6 and Pseudonocardia sp. TY-7. Journal of Bioscience and Bioengineering 102, 184–192

[24] Kotrbáček, V., Doubek, J., Doucha, J., 2015. The chlorococcalean alga Chlorella in animal nutrition: a review. Journal of Applied Phycology27, 2173–2180.

[25] Langille, M.G.I., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Vega Thurber, R.L., Knight, R., Beiko, R.G., Huttenhower, C., 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology31, 814–821.

[26] Li, X.D., Dong, S.L., Lei, Y.Z., Li, Y.H., 2007. The effect of stocking density of Chinese mitten crab Eriocheir sinensis on rice and crab seed yields in rice–crab culture systems. Aquaculture273, 487–493.

[27] Lin, S.M., Zhou, X.M., Zhou, Y.L., Kuang, W.M., Chen, Y.J., Luo, L., Dai, F.Y., 2020. Intestinal morphology, immunity and microbiota response to dietary fibers in largemouth bass, Micropterus salmoide. Fish & Shellfish Immunology103, 135–142.

[28] Liu, T., Xu, J.W., Tian, R.Q., Quan, X., 2021a. Enhanced simultaneous nitrification and denitrification via adding N-acyl-homoserine lactones (AHLs) in integrated floating fixed-film activated sludge process. Biochemical Engineering Journal166, 107884.

[29] Liu, Y.X., Qin, Y., Chen, T., Lu, M.P., Qian, X.B., Guo, X.X., Bai, Y., 2021b. A practical guide to amplicon and metagenomic analysis of microbiome data. Protein & Cell12, 315–330.

[30] Liu, Z.J., Zhou, W., Li, S.T., He, P., Liang, G.Q., Lv, J.L., Jin, H., 2015. Assessing soil quality of gleyed paddy soils with different productivities in subtropical China. CATENA133, 293–302.

[31] Louca, S., Parfrey, L.W., Doebeli, M., 2016. Decoupling function and taxonomy in the global ocean microbiome. Science353, 1272–1277.

[32] McIlroy, S.J., Nielsen, P.H., 2014. The family Saprospiraceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F., eds. The Prokaryotes: Other Major Lineages of Bacteria and the Archaea. 4th ed. Berlin, Heidelberg: Springer, 863–889

[33] Meijide, A., Gruening, C., Goded, I., Seufert, G., Cescatti, A., 2017. Water management reduces greenhouse gas emissions in a Mediterranean rice paddy field. Agriculture, Ecosystems & Environment238, 168–178.

[34] Qi, J.B., Gu, X.L., Ma, L.B., Qiao, Z.G., Chen, K., 2013. The research progress on food organism culture and technology utilization in crab seed production in ponds in China. Agricultural Sciences4, 563–569.

[35] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

[36] Radhakrishnan, D.K., Akbarali, I., Schmidt, B.V., John, E.M., Sivanpillai, S., Vasunambesan, S.T., 2020. Improvement of nutritional quality of live feed for aquaculture: an overview. Aquaculture Research51, 1–17.

[37] Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ4, e2584.

[38] Ruddle, K., 1982. Traditional integrated farming systems and rural development: the example of ricefield fisheries in Southeast Asia. Agricultural Administration10, 1–11.

[39] Samat, N.A., Yusoff, F.M., Rasdi, N.W., Karim, M., 2020. Enhancement of live food nutritional status with essential nutrients for improving aquatic animal health: a review. Animals10, 2457.

[40] Shen, Z.Z., Zhong, S.T., Wang, Y.G., Wang, B.B., Mei, X.L., Li, R., Ruan, Y.Z., Shen, Q.R., 2013. Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. European Journal of Soil Biology57, 1–8.

[41] Shi, X., Luo, Z., Chen, F., Wei, C.C., Wu, K., Zhu, X.M., Liu, X., 2017. Effect of fish meal replacement by Chlorella meal with dietary cellulase addition on growth performance, digestive enzymatic activities, histology and myogenic genes’ expression for crucian carp Carassius auratus. Aquaculture Research48, 3244–3256.

[42] Taranu, I., Marin, D.E., Untea, A., Janczyk, P., Motiu, M., Criste, R.D., Souffrant, W.B., 2012. Effect of dietary natural supplements on immune response and mineral bioavailability in piglets after weaning. Czech Journal of Animal Science57, 332–343.

[43] Venkatesh, M., Mukherjee, S., Wang, H., Li, H.W., Sun, K., Benechet, A.P., Qiu, Z.J., Maher, L., Redinbo, M.R., Phillips, R.S., Fleet, J.C., Kortagere, S., Mukherjee, P., Fasano, A., Le Ven, J., Nicholson, J.K., Dumas, M.E., Khanna, K.M., Mani, S., 2014. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity41, 296–310.

[44] Wang, M.L., Xiong, X., Liu, J.J., He, C., Zhao, Q.Y., 2020. Carbon and nitrogen stable isotopes evidence for the environmental impact of the cage fish farm in Poyang Lake, China. Bulletin of Environmental Contamination and Toxicology105, 860–867.

[45] Xi, L.W., Lu, Q.S., Liu, Y.L., Su, J.Z., Chen, W., Gong, Y.L., Han, D., Yang, Y.X., Zhang, Z.M., Jin, J.Y., Liu, H.K., Zhu, X.M., Xie, S.Q., 2022. Effects of fish meal replacement with Chlorella meal on growth performance, pigmentation, and liver health of largemouth bass (Micropterus salmoides). Animal Nutrition10, 26–40.

[46] Xie, J., Hu, L.L., Tang, J.J., Wu, X., Li, N.N., Yuan, Y.G., Yang, H.S., Zhang, J.E., Luo, S.M., Chen, X., 2011. Ecological mechanisms underlying the sustainability of the agricultural heritage rice–fish coculture system. Proceedings of the National Academy of Sciences of the United States of America108, E1381–E1387.

[47] Yan, L., Lim, S.U., Kim, I.H., 2012. Effect of fermented Chlorella supplementation on growth performance, nutrient digestibility, blood characteristics, fecal microbial and fecal noxious gas content in growing pigs. Asian-Australasian Journal of Animal Sciences25, 1742–1747.

[48] Yang, S., Du, J., Luo, J., Zhou, Y., Long, Y., Xu, G., Zhao, L., Du, Z., Yan, T., 2019. Effects of different diets on the intestinal microbiota and immunity of common carp (Cyprinus carpio). Journal of Applied Microbiology127, 1327–1338.

[49] Zhang, Y., Chen, M., Zhao, Y.Y., Zhang, A.Y., Peng, D.H., Lu, F., Dai, C.C., 2021. Destruction of the soil microbial ecological environment caused by the over-utilization of the rice-crayfish co-cropping pattern. Science of the Total Environment788, 147794.

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