Abstract
As a kind of green and high quality feed, fermented feed has the activity of promoting growth and improving immunity in aquaculture. The aim of this study was to develop a new liquid fermented feed for the culture of sea cucumber Apostichopus japonicus and evaluate its nutritional value and function. After the commercial feed of the sea cucumber was fermented by Corynebacterium glutamicum, the contents of crude protein, free amino acids, palmitoleic acid, linoleic acid, arachidonic acid, and the total content of polyunsaturated fatty acids were significantly increased. By feeding the fermented food, the weight gain rate, special growth rate and feed conversion rate of the sea cucumber were significantly increased, and the mortality rate was significantly reduced in the challenge test. The cellulase activity in the gut of the sea cucumber fed with the fermented feed was significantly increased, while the activities of alkaline phosphatase, acid phosphatase, total nitric oxide synthase, catalase, and lysozyme in the coelomic fluid were significantly increased. The fermented feed changed the gut microbiota of the sea cucumber and significantly reduced the relative abundance of Vibrio, which was the main pathogen causing skin ulcer syndrome. Transcriptome analysis revealed 4492 differentially expressed genes that can be enriched in biological processes such as immune system processes and immune responses, and affect the growth performance and immune regulation of the sea cucumber through metabolic pathways such as ribosomal biogenesis. Further gene expression analysis showed that the upregulation of genes such as NFκBI, TLR, TLR3, TRAF6, MyD88, and p38 activated the TLR signaling pathway and enhances the immune response of the sea cucumber. Therefore, C. glutamicum fermented feed can promote the growth of the sea cucumber, enhance non-specific immunity, and resist pathogen infection, making it a highly promising feed for application.
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References
Bao PY, Li XY, Xu YP (2018) An evaluation on the ratio of plant to animal protein in the diet of juvenile sea cucumber (Apostichopus japonicus): growth, nutrient digestibility and nonspecific immunity. J Ocean Univ China 17(6):1479–1486. https://doi.org/10.1007/s11802-018-3725-1
Callewaert L, Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci 35(1):127–160. https://doi.org/10.1007/s12038-010-0015-5
Deng H, He C, Zhou Z, Liu C, Tan K, Wang N, Jiang B, Gao X, Liu W (2009) Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture 287(1):18–27. https://doi.org/10.1016/j.aquaculture.2008.10.015
Dossou S, Koshio S, Ishikawa M, Yokoyama S, Dawood MAO, El Basuini MF, Olivier A, Zaineldin AI (2018) Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish Shellfish Immunol 75:253–262. https://doi.org/10.1016/j.fsi.2018.01.032
Dou HX, Wu SJ (2023) Dietary fulvic acid supplementation improves the growth performance and immune response of sea cucumber (Apostichopus japonicas). Fish Shellfish Immunol 135:108662. https://doi.org/10.1016/j.fsi.2023.108662
Feng ZF, Song XJ, Zhao LT, Zhu W (2020) Isolation of probiotics and their effects on growth, antioxidant and non-specific immunity of sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 106:1087–1094. https://doi.org/10.1016/j.fsi.2020.08.049
Gao F (2010) Physiology of sea cucumber. In: Ke Y, Wang C, Liao Y (eds) Study on sea cucumbers. China Ocean University Press, Qingdao, pp 65–82
Gao L, He C, Bao X, Tian M, Ma Z (2017a) Transcriptome analysis of the sea cucumber (Apostichopus japonicus) with variation in individual growth. PLoS ONE 12(7):e0181471. https://doi.org/10.1371/journal.pone.0181471
Gao ML, Hou HM, Zhang GL, Liu Y, Sun LM (2017b) Bacterial diversity in the intestine of sea cucumber Stichopus japonicus. Iran J Fish Sci 16(1):318–325
Han X (2018) Study on dietary optimum methionine, valine and isoleucine requirements of juvenile sea cucumber Apostichopus japonicus Selenka. Dissertation, Shanghai Ocean University
Hou SY, ** ZW, Jiang WW, Chi L, **a B, Chen JH (2019) Physiological and immunological responses of sea cucumber Apostichopus japonicus during desiccation and subsequent resubmersion. PeerJ 7:e7427. https://doi.org/10.7717/peerj.7427
Kumar N (2021a) Dietary riboflavin enhances immunity and anti-oxidative status against arsenic and high temperature in Pangasianodon hypophthalmus. Aquaculture 533:736209. https://doi.org/10.1016/j.aquaculture.2020.736209
Kumar V (2021b) Chapter 7 - Ribosomal biogenesis in eukaryotes. In Kumar V (Ed.), Emerging concepts in ribosome structure, biogenesis, and function (pp. 129–150). Academic Press. https://doi.org/10.1016/B978-0-12-816364-1.00011-1
Li Z, Ren HY, Li Q, Murtaza B, Li XY, Zhang JC, Xu YP (2020) Exploring the effects of phage cocktails in preventing Vibrio infections in juvenile sea cucumber (Apostichopus japonicus) farming. Aquaculture 515:734599. https://doi.org/10.1016/j.aquaculture.2019.734599
Li BS, Han XJ, Wang JY, Song ZD, Sun YZ, Wang SX, Huang BS (2021) Optimal dietary methionine requirement for juvenile sea cucumber Apostichopus japonicus selenka. Aquacult Res 52(4):1348–1358. https://doi.org/10.1111/are.14989
Li C, **ng X, Qi HQ, Liu Y, Jian FJ, Wang JH (2022) The arachidonic acid and its metabolism pathway play important roles for Apostichopus japonicus infected by Vibrio splendens. Fish Shellfish Immunol 125:152–160. https://doi.org/10.1016/j.fsi.2022.05.012
Liao ZH, Ibarra-Arana MJ, Chen JC, Huang HT, Lin YJ, Nan FH (2021) The effects of dietary supplement of Ulva fasciata, fermented soybean and probiotics on the growth of Apostichopus japonicus. Aquacul Nutr 27(5):1363–1369. https://doi.org/10.1111/anu.13274
Liu B, Zhou W, Wang H, Li C, Wang L, Li Y, Wang J (2020) Bacillus baekryungensis MS1 regulates the growth, non-specific immune parameters and gut microbiota of the sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 102:133–139. https://doi.org/10.1016/j.fsi.2020.04.023
Liu Y, Liu Q, Bai Q, Wang L, Li C, Li Y, Liu B (2023) Effects of dietary Bacillus baekryungensis on body wall nutrients, digestion and immunity of the sea cucumber Apostichopus japonicus. Fish Sci 89(2):233–241. https://doi.org/10.1007/s12562-022-01665-3
Lu Y, Li CH, Wang DQ, Su XR, ** CH, Li Y, Li TW (2013) Characterization of two negative regulators of the Toll-like receptor pathway in Apostichopus japonicus: Inhibitor of NF-kappa B and Toll-interacting protein. Fish Shellfish Immunol 35(5):1663–1669. https://doi.org/10.1016/j.fsi.2013.08.014
Mugwanya M, Dawood MAO, Kimera F, Sewilam H (2023) Replacement of fish meal with fermented plant proteins in the aquafeed industry: A systematic review and meta-analysis. Rev Aquacult 15(1):62–88. https://doi.org/10.1111/raq.12701
Nugraha TA, Isnansetyo A, Triyanto DM (2022) Fermented earthworms as a feed additive enhances non-specific immune response in catfish (Clarias gariepinus). Aquacult Int 30(1):211–226. https://doi.org/10.1007/s10499-021-00794-3
Qi HQ, Liu Y, Jian FJ, **ng X, Wang JH, Li C (2022) Effects of dietary arachidonic acid (ARA) on immunity, growth and fatty acids of Apostichopus japonicus. Fish Shellfish Immunol 127:901–909. https://doi.org/10.1016/j.fsi.2022.07.037
Ray D, Anand U, Jha NK, Korzeniewska E, Bontempi E, Proćków J, Dey A (2022) The soil bacterium, Corynebacterium glutamicum, from biosynthesis of value-added products to bioremediation: A master of many trades. Environ Res 213:113622. https://doi.org/10.1016/j.envres.2022.113622
Ren Y, Zhang JL, Wang YN, Chen J, Liang CL, Li RJ, Li Q (2020) Non-specific immune factors differences in coelomic fluid from polian vesicle and coelom of Apostichopus japonicus, and their early response after evisceration. Fish Shellfish Immunol 98:160–166. https://doi.org/10.1016/j.fsi.2019.12.094
Sharifian M, Hajimoradloo A, Ghorbani R, Hoseinifar SH (2017) Effects of dietary retinol acetate on growth performance, skin mucus immune responses and haematological parameters of Caspian roach (Rutilus caspicus). Aquacul Nutr 23(5):893–898. https://doi.org/10.1111/anu.12456
Shi C, Zhang Y, Yin Y, Wang C, Lu Z, Wang F, Feng J, Wang Y (2017) Amino acid and phosphorus digestibility of fermented corn-soybean meal mixed feed with Bacillus subtilis and Enterococcus faecium fed to pigs. J Anim Sci 95(9):3996–4004. https://doi.org/10.2527/jas2017.1516
Song ZD, Li PY, Wang JY, Huang BS, Li BS, Wang SX, Zhang Y, Gong XP, Li XL, Tan Q (2016) Effects of seaweed replacement by hydrolyzed soybean meal on growth, metabolism, oxidation resistance and body composition of sea cucumber Apostichopus japonicus. Aquaculture 463:135–144. https://doi.org/10.1016/j.aquaculture.2016.05.020
Sugiharto S, Ranjitkar S (2019) Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Anim Nutr 5(1):1–10. https://doi.org/10.1016/j.aninu.2018.11.001
Wang J, Ren TJ, Han YZ, Zhao Y, Liao ML, Wang FQ, Jiang ZQ (2015) Effects of dietary vitamin C supplementation on lead-treated sea cucumbers, Apostichopus japonicus. Ecotoxicol Environ Saf 118:21–26. https://doi.org/10.1016/j.ecoenv.2015.04.009
Wang JH, Guo H, Zhang TR, Wang H, Liu BN, **ao S (2017) Growth performance and digestion improvement of juvenile sea cucumber Apostichopus japonicus fed by solid-state fermentation diet. Aquacult Nutr 23(6):1312–1318. https://doi.org/10.1111/anu.12506
Wang GY, Meng ZQ, Chen L, Jiang JH, Feng YL, Zhang BS (2020) Effects of kelp residues fermented with probiotics on the culture of sea cucumber. Apostichopus Japonicus Aquacult Res 51(3):1133–1142. https://doi.org/10.1111/are.14460
Wen B, Gao QF, Dong SL, Hou YR, Yu HB, Li WD (2016) Effects of dietary inclusion of benthic matter on feed utilization, digestive and immune enzyme activities of sea cucumber Apostichopus japonicus (Selenka). Aquaculture 458:1–7. https://doi.org/10.1016/j.aquaculture.2016.01.028
Yang L, Zeng X, Qiao S (2021) Advances in research on solid-state fermented feed and its utilization: The pioneer of private customization for intestinal microorganisms. Anim Nutr 7(4):905–916. https://doi.org/10.1016/j.aninu.2021.06.002
Yi H, Bai Q, Li Y, Zhan H, Liu Y, Liu B, Wang J (2022) Sporosarcina aquimarina MS4 regulates the digestive enzyme activities, body wall nutrients, gut microbiota, and metabolites of Apostichopus japonicus. Fishes 7:134. https://doi.org/10.3390/fishes7030134
Yu H, Gao Q, Dong S, Lan Y, Ye Z, Wen B (2016) Regulation of dietary glutamine on the growth, intestinal function, immunity and antioxidant capacity of sea cucumber Apostichopus japonicus (Selenka). Fish Shellfish Immunol 50:56–65. https://doi.org/10.1016/j.fsi.2016.01.024
Zhang ED, Dong SL, Wang F, Tian XL, Gao QF (2018) Effects of L-tryptophan on the growth, intestinal enzyme activities and non-specific immune response of sea cucumber (Apostichopus japonicus Selenka) exposed to crowding stress. Fish Shellfish Immunol 75:158–163. https://doi.org/10.1016/j.fsi.2018.01.009
Zhang MZ, Pan LQ, Fan DP, He JJ, Su C, Gao S, Zhang MY (2021) Study of fermented feed by mixed strains and their effects on the survival, growth, digestive enzyme activity and intestinal flora of Penaeus vannamei. Aquaculture 530:735703. https://doi.org/10.1016/j.aquaculture.2020.735703
Zhang P, Tan P, Zhang L, Zhu WL, Chen RY, Wang LG, Xu DD (2023) A comparative study on growth performance, body composition, and liver tissue metabolism rearing on soybean lecithin-enriched Artemia Nauplii and microdiet in rock bream (Oplegnathus fasciatus) larvae. Aquacult Nutr 2023:5545898. https://doi.org/10.1155/2023/5545898
Zhao YC, Zhang WB, Xu W, Mai KS, Zhang YJ, Liufu ZG (2012) Effects of potential probiotic Bacillus subtilis T13 on growth, immunity and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 32(5):750–755. https://doi.org/10.1016/j.fsi.2012.01.027
Zhao LT, Feng ZF, Lu N, Yang SH, Zhu W (2019) Effects of dietary n-3 PUFA supplements on composition of n-3 PUFA and expression of fatty acid elongase 5 (AJELOVL5) in sea cucumber. Apostichopus Japonicus Aquacult Res 50(1):209–218. https://doi.org/10.1111/are.13885
Zhuo LC, Chen CF, Lin YH (2021) Dietary supplementation of fermented lemon peel enhances lysozyme activity and susceptibility to Photobacterium damselae for orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol 117:248–252. https://doi.org/10.1016/j.fsi.2021.08.015
Acknowledgements
This work was supported by Open Foundation of Dalian **shiwan Laboratory (2024015), the Research Project of Applied Basic Research Program of Department of Science & Technology of Liaoning Province (2022JH2/101300137), and Open Fund of Key Laboratory of Biotechnology and Bioresources Utilization (Dalian Minzu University), Ministry of Education (KF2022007), China.
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Jiarong Cui: methodology, formal analysis. **aofei Tan: software, data curation. Zixuan Xu: writing—original draft preparation, validation. **nyu Sun: investigation. Liang Wang: funding acquisition. Honglei Zhan: resources. Yujia Liu: visualization. Ying Li: conceptualization, funding acquisition. Bingnan Liu: conceptualization, writing—original draft preparation, project administration.
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Cui, J., Tan, X., Xu, Z. et al. Evaluation of growth, immune characteristics and gut microbiota of juvenile sea cucumber Apostichopus japonicus fed with fermented feed from Corynebacterium glutamicum. Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01490-8
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DOI: https://doi.org/10.1007/s10499-024-01490-8