Citation: | ZAN Zi-Ye, ZHU Wen-Huan, LI Ming, ZOU Hong, WANG Gui-Tang, WU Shan-Gong. COMPARATIVE STUDY ON INTESTINAL MICROBIOTA OF CRAYFISH (PROCAMBARUS CLARKII) IN DIFFERENT CULTURE MODELS[J]. ACTA HYDROBIOLOGICA SINICA. DOI: 10.7541/2025.2024.0388 |
The red swamp crayfish (Procambarus clarkii) is the most extensively farmed crustacean in China. The intestinal microbiota plays a crucial role in host physiological functions. However, it remains unclear whether there are differences in intestinal microbiota structure and function among different culture models of crayfish. In this study, we utilized Illumina MiSeq high-throughput sequencing technology to analyze the intestinal microbiota of crayfish under different cultivation models: rice-crayfish co-culture (RC), single-crayfish pond culture (SC), and mixed-crayfish pond culture (MC). We also analyzed water physicochemical factors and further explored the relationship between intestinal microbiota and physicochemical factors in the water. The results revealed that: Species composition analysis showed that at phylum level, the intestinal microbiota composition was consistent across three culture models, with Tenericutes, Proteobacteria, and Firmicutes as the absolute dominant groups. At genus level, there were some differences among different culture models, with Bacillus having the highest relative abundance in RC group, Lactococcus dominated in SC group, and Aeromonas was most abundant in MC group. Diversity analysis showed that the species richness and diversity of intestinal bacteria in group MC were the highest, and there were significant differences in the community structure of intestinal bacteria of crayfish under three culture models. Functional prediction showed that Vitamin Biosynthetic metabolic pathway was significantly enriched in RC group, while lactose degradation and galactose degradation metabolic pathways were prominent in SC group. In the MC group, pathways related to fatty acid and lipid degradation, CMP-pseudaminate biosynthesis, and superpathway of lipopolysaccharide biosynthesis metabolic pathways were significantly enriched. Network analysis showed that the cooperative relationship accounted for 83.76% of the interactions within the intestinal microbiota, with Erysipelotrichaceae and Sphingomonas bacteria were the main nodes of the network. Furthermore, the abundance of Lactobacillus in the gut was significantly positively correlated with TP concentration and negatively correlated with NH+4 concentration in the water. In conclusion, the intestinal microbiota of crayfish includes core microbial groups mainly composed of Tenericutes, Proteobacteria and Firmicutes in the gut of crayfish, which remain stable across different culture models. However, there are notable variations in both community structure and metabolic function of intestinal bacteria among the three models. These findings enhance our understanding of crayfish intestinal microbiota and provide a theoretical basis for the screening of intestinal probiotics and their application in production practice.
[1] |
刘其根, 李应森, 陈蓝荪. 克氏原螯虾的生物学 [J]. 水产科技情报, 2008, 35(1): 21-23.]
Liu Q G, Li Y S, Chen L S. Ecological culture of red swamp crawfish Procambarus clarkii (Ⅰ) [J]. Fisheries Science & Technology Information, 2008, 35(1): 21-23. [
|
[2] |
Li Y, Guo X, Cao X, et al. Population genetic structure and post-establishment dispersal patterns of the red swamp crayfish Procambarus clarkii in China [J]. PLoS One, 2012, 7(7): e40652. doi: 10.1371/journal.pone.0040652
|
[3] |
任妮, 戴红君, 张琤琤, 等. 我国克氏原螯虾产业调查分析与发展对策建议 [J]. 江苏农业科学, 2021, 49(19): 241-246.]
Ren N, Dai H J, Zhang C C, et al. Investigation and analysis of China’s crayfish industry and suggestions for development [J]. Jiangsu Agricultural Sciences, 2021, 49(19): 241-246. [
|
[4] |
徐加涛, 阎斌伦, 徐国成. 克氏原螯虾产业发展背景、现状与展望 [J]. 水产科技情报, 2011, 38(4): 172-176.]
Xu J T, Yan B L, Xu G C. Development background, present situation and prospect of Procambarus clarkii industry [J]. Fisheries Science & Technology Information, 2011, 38(4): 172-176. [
|
[5] |
Yi S, Li Y, Shi L, et al. Characterization of population genetic structure of red swamp crayfish, Procambarus clarkii, in China [J]. Scientific Reports, 2018, 8(1): 5586. doi: 10.1038/s41598-018-23986-z
|
[6] |
但启明. 两种养殖模式对克氏原螯虾食性和肌肉品质的影响 [D]. 武汉: 华中农业大学, 2023: 1.]
Dan Q M. Effects of two kinds of breeding systems on feeding habits and meat quality of Procambarus clarkii [D]. Wuhan: Huazhong Agricultural University, 2023: 1. [
|
[7] |
全国水产技术推广总站, 中国水产学会. 中国小龙虾产业发展报告(2024) [J]. 中国水产, 2024(7): 14-20.]
National Fisheries Technology Extension Center, China Society of Fisheries. China crayfish industry development report (2024) [J]. China Fisheries, 2024(7): 14-20. [
|
[8] |
陆海莉, 陈小琳, 陈青春, 等. 稻虾生态种养模式下克氏原螯虾养殖优化决策模型 [J]. 水产养殖, 2023, 44(12): 62-64.]
Lu H L, Chen X L, Chen Q C, et al. Optimal decision-making model of Procambarus clarkii culture under the ecological breeding mode of rice and shrimp [J]. Journal of Aquaculture, 2023, 44(12): 62-64. [
|
[9] |
奚业文. 低洼稻田稻虾连作、共作生态试验技术分析 [J]. 基层农技推广, 2014, 2(10): 30-33.]
Xi Y W. Analysis on ecological experiment technology of rice and shrimp continuous cropping and co-cropping in low-lying paddy fields [J]. Primary Agricultural Technology Extension, 2014, 2(10): 30-33. [
|
[10] |
陈松文, 江洋, 汪金平, 等. 湖北省稻虾模式发展现状与对策分析 [J]. 华中农业大学学报, 2020, 39(2): 1-7.]
Chen S W, Jiang Y, Wang J P, et al. Situation and countermeasures of integrated rice-crayfish farming in Hubei Province [J]. Journal of Huazhong Agricultural University, 2020, 39(2): 1-7. [
|
[11] |
花友亮, 朱宏元, 宋长太. 池塘主养小龙虾生产模式与技术 [J]. 农村新技术, 2022(7): 32-33.]
Hua Y L, Zhu H Y, Song C T. Production mode and technology of crayfish in pond [J]. New Rural Technology, 2022(7): 32-33. [
|
[12] |
顾明. 小龙虾池塘生态养殖技术 [J]. 现代农业科技, 2021(18): 202-203, 207.]
Gu M. Ecological culture technology of crayfish pond [J]. Modern Agricultural Science and Technology, 2021(18): 202-203, 207. [
|
[13] |
宋亮, 张建平, 韩晓磊, 等. 克氏原螯虾养殖现状及对策 [J]. 常熟理工学院学报, 2011, 25(2): 85-87,91.]
Song L, Zhang J P, Han X L, et al. Analysis of breeding situation and countermeasures of Procambarus clarkia [J]. Journal of Changshu Institute of Technology, 2011, 25(2): 85-87,91. [
|
[14] |
张聪. 河蟹与小龙虾池塘高效混养技术 [J]. 渔业致富指南, 2024(9): 39-43.]
Zhang C. Efficient polyculture technology of river crab and crayfish in pond [J]. Fishery Guide to be Rich, 2024(9): 39-43. [
|
[15] |
Gomaa E Z. Human gut microbiota/microbiome in health and diseases: a review [J]. Antonie Van Leeuwenhoek, 2020, 113(12): 2019-2040. doi: 10.1007/s10482-020-01474-7
|
[16] |
Heintz-Buschart A, Wilmes P. Human gut microbiome: function matters [J]. Trends in Microbiology, 2018, 26(7): 563-574. doi: 10.1016/j.tim.2017.11.002
|
[17] |
Hanning I, Diaz-Sanchez S. The functionality of the gastrointestinal microbiome in non-human animals [J]. Microbiome, 2015(3): 51. doi: 10.1186/s40168-015-0113-6
|
[18] |
Roeselers G, Mittge E K, Stephens W Z, et al. Evidence for a core gut microbiota in the zebrafish [J]. The ISME Journal, 2011, 5(10): 1595-1608. doi: 10.1038/ismej.2011.38
|
[19] |
Abid A, Davies S J, Waines P, et al. Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity [J]. Fish & Shellfish Immunology, 2013, 35(6): 1948-1956.
|
[20] |
Nayak S K. Role of gastrointestinal microbiota in fish [J]. Aquaculture Research, 2010, 41(11): 1553-1573. doi: 10.1111/j.1365-2109.2010.02546.x
|
[21] |
Dawood M A O. Nutritional immunity of fish intestines: important insights for sustainable aquaculture [J]. Reviews in Aquaculture, 2021, 13(1): 642-663. doi: 10.1111/raq.12492
|
[22] |
Tzuc J T, Escalante D R, Rojas Herrera R, et al. Microbiota from Litopenaeus vannamei: digestive tract microbial community of Pacific white shrimp (Litopenaeus vannamei) [J]. SpringerPlus, 2014(3): 280. doi: 10.1186/2193-1801-3-280
|
[23] |
王金星. 对虾等甲壳类动物肠道与血淋巴菌群的组成、功能与动态平衡调控 [J]. 微生物学报, 2018, 58(5): 760-772.]
Wang J X. The gut and hemolymph microbiotas of crustacean, composition, functions, and homeostatic regulation [J]. Acta Microbiologica Sinica, 2018, 58(5): 760-772. [
|
[24] |
Rungrassamee W, Klanchui A, Maibunkaew S, et al. Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure [J]. Journal of Invertebrate Pathology, 2016(133): 12-19. doi: 10.1016/j.jip.2015.11.004
|
[25] |
Zhu J, Dai W, Qiu Q, et al. Contrasting ecological processes and functional compositions between intestinal bacterial community in healthy and diseased shrimp [J]. Microbial Ecology, 2016, 72(4): 975-985. doi: 10.1007/s00248-016-0831-8
|
[26] |
冯光志, 石慧, 刘博, 等. 小龙虾肠道产纤维素酶细菌的分离与鉴定 [J]. 生物技术通报, 2020, 36(2): 65-70.]
Feng G Z, Shi H, Liu B, et al. Screening and identification of cellulase-producing strains isolated from crayfish intestine [J]. Biotechnology Bulletin, 2020, 36(2): 65-70. [
|
[27] |
Xu Y, Li Y, Xue M, et al. Effects of dietary Saccharomyces cerevisiae YFI-SC2 on the growth performance, intestinal morphology, immune parameters, intestinal microbiota, and disease resistance of crayfish (Procambarus clarkia) [J]. Animals, 2021, 11(7): 1963. doi: 10.3390/ani11071963
|
[28] |
中国环境监督总站, 辽宁省环境监测中心站. HJ 494-2009, 水质. 采样技术指导 [S]. 行业标准-环保. 2000: 1-3.]
China National Environmental Monitoring Centre, Liaoning Provincial Environmental Monitoring Center Station. HJ 494-2009, Water quality, Guidance on Sampling Techniques [S]. Industry Standard-Environmental Protection. 2000: 1-3. [
|
[29] |
Wanyan R, Pan M, Mai Z, et al. Distribution and influencing factors of antibiotic resistance genes of crayfish (Procambarus clarkii) intestine in main crayfish breeding provinces in China [J]. Science of the Total Environment, 2023(857): 159611. doi: 10.1016/j.scitotenv.2022.159611
|
[30] |
Callahan B J, McMurdie P J, Rosen M J, et al. DADA2: High-resolution sample inference from Illumina amplicon data [J]. Nature Methods, 2016, 13(7): 581-583. doi: 10.1038/nmeth.3869
|
[31] |
DeSantis T Z, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB [J]. Applied and Environmental Microbiology, 2006, 72(7): 5069-5072. doi: 10.1128/AEM.03006-05
|
[32] |
Bokulich N A, Kaehler B D, Rideout J R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin [J]. Microbiome, 2018, 6(1): 90. doi: 10.1186/s40168-018-0470-z
|
[33] |
Bolyen E, Rideout J R, Dillon M R, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 [J]. Nature Biotechnology, 2019, 37(8): 852-857. doi: 10.1038/s41587-019-0209-9
|
[34] |
McArdle B H, Anderson M J. Fitting multivariate models to community data: a comment on distance-based redundancy analysis [J]. Ecology, 2001, 82(1): 290-297. doi: 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
|
[35] |
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation [J]. Genome Biology, 2011, 12(6): R60. doi: 10.1186/gb-2011-12-6-r60
|
[36] |
Douglas G M, Maffei V J, Zaneveld J R, et al. PICRUSt2 for prediction of metagenome functions [J]. Nature Biotechnology, 2020, 38(6): 685-688. doi: 10.1038/s41587-020-0548-6
|
[37] |
Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks [J]. Proceedings of the International AAAI Conference on Web and Social Media, 2009, 3(1): 361-362. doi: 10.1609/icwsm.v3i1.13937
|
[38] |
Team R C. R: A language and environment for statistical computing [CP]. R foundation for statistical computing, Vienna, Austria, 2022, URL https://www.R-project.org/.12c.
|
[39] |
Wu S, Wang G, Angert E R, et al. Composition, diversity, and origin of the bacterial community in grass carp intestine [J]. PLoS One, 2012, 7(2): e30440. doi: 10.1371/journal.pone.0030440
|
[40] |
Sanna S, Kurilshikov A, van der Graaf A, et al. Challenges and future directions for studying effects of host genetics on the gut microbiome [J]. Nature Genetics, 2022, 54(2): 100-106. doi: 10.1038/s41588-021-00983-z
|
[41] |
王飞飞, 王夏雯, 金倩, 等. 稻虾模式下克氏原螯虾组织及其养殖环境菌群多样性 [J]. 青岛农业大学学报(自然科学版), 2021, 38(2): 91-97.]
Wang F F, Wang X W, Jin Q, et al. The microbial community diversity in the tissues of Procambarus clarkii and its aquacultural environment in integrated crayfish-rice cultivation model [J]. Journal of Qingdao Agricultural University (Natural Science), 2021, 38(2): 91-97. [
|
[42] |
Shui Y, Guan Z B, Liu G F, et al. Gut microbiota of red swamp crayfish Procambarus clarkii in integrated crayfish-rice cultivation model [J]. AMB Express, 2020, 10(1): 5. doi: 10.1186/s13568-019-0944-9
|
[43] |
Chen H, Liu F, Ouyang M, et al. Differences in intestinal microbial composition between red claw crayfish (Cherax quadricarinatus) and red swamp crayfish (Procambarus clarkii) cultured in pond [J]. Fishes, 2022, 7(5): 241. doi: 10.3390/fishes7050241
|
[44] |
Li Y, Zhou F, Tang Y, et al. Variation in bacterial communities among stress-sensitive and stress-tolerant black tiger shrimp (Penaeus monodon) individuals [J]. Aquaculture Research, 2021, 52(5): 2146-2159. doi: 10.1111/are.15067
|
[45] |
董学兴, 吕林兰, 赵卫红, 等. 不同养殖模式下罗氏沼虾肠道菌群结构特征及其与环境因子的关系 [J]. 上海海洋大学学报, 2019, 28(4): 501-510.]
Dong X X, Lü L L, Zhao W H, et al. Effects of different cultural patterns on microbial communities in the intestine of Macrobrachium rosenbergii and interactions with environment factors [J]. Journal of Shanghai Ocean University, 2019, 28(4): 501-510. [
|
[46] |
赵月季, 郭海朋, 张德民. 不同养殖模式对凡纳滨对虾肠道微生物群落的影响 [J]. 水产学报, 2021, 45(2): 221-234.]
Zhao Y J, Guo H P, Zhang D M. Effects of different culture patterns on the intestinal microbiota of Litopenaeus vannamei [J]. Journal of Fisheries of China, 2021, 45(2): 221-234. [
|
[47] |
Dong J, Li X, Zhang R, et al. Comparative analysis of the intestinal bacterial community and expression of gut immunity genes in the Chinese mitten crab (Eriocheir sinensis) [J]. AMB Express, 2018, 8(1): 192. doi: 10.1186/s13568-018-0722-0
|
[48] |
Wang Y, Huang J M, Zhou Y L, et al. Phylogenomics of expanding uncultured environmental Tenericutes provides insights into their pathogenicity and evolutionary relationship with Bacilli [J]. BMC Genomics, 2020, 21(1): 408. doi: 10.1186/s12864-020-06807-4
|
[49] |
Wang Y, Wang C, Chen Y, et al. Microbiome analysis reveals microecological balance in the emerging rice-crayfish integrated breeding mode [J]. Frontiers in Microbiology, 2021(12): 669570. doi: 10.3389/fmicb.2021.669570
|
[50] |
邓祥宜, 李池茜, 张涵池, 等. 养殖塘和市售小龙虾肠道细菌多样性的比较 [J]. 微生物学杂志, 2021, 41(3): 44-52.]
Deng X Y, Li C X, Zhang H C, et al. Comparison of intestinal bacterial diversity of crawfish (Procambarus clarkii) from culture ponds and markets [J]. Journal of Microbiology, 2021, 41(3): 44-52. [
|
[51] |
谢梦琪, 张诗雨, 许荔立, 等. 不同性别和生长阶段对克氏原螯虾肠道菌群多样性的影响 [J]. 水生生物学报, 2021, 45(6): 1243-1254.]
Xie M Q, Zhang S Y, Xu L L, et al. The intestinal microbiota diversities of Procambarus clarkia at different sexes and growth stages [J]. Acta Hydrobiologica Sinica, 2021, 45(6): 1243-1254. [
|
[52] |
Zhang Z, Liu J, Jin X, et al. Developmental, dietary, and geographical impacts on gut microbiota of red swamp crayfish (Procambarus clarkii) [J]. Microorganisms, 2020, 8(9): 1376. doi: 10.3390/microorganisms8091376
|
[53] |
Xie M, Zhang S, Xu L, et al. Comparison of the intestinal microbiota during the different growth stages of red swamp crayfish (Procambarus clarkii) [J]. Frontiers in Microbiology, 2021(12): 696281. doi: 10.3389/fmicb.2021.696281
|
[54] |
Wang J, Ye J, Zhang Z, et al. Comparison of the nutrient value, nonspecific immunity, and intestinal microflora of red swamp crayfish (Procambarus clarkii) in different culture modes [J]. Aquaculture Reports, 2023(31): 101683. doi: 10.1016/j.aqrep.2023.101683
|
[55] |
Gao Q, Luo J, Liu P, et al. Characteristics of intestinal microbiota in male morphotypes of the giant freshwater prawn Macrobrachium rosenbergii [J]. Aquaculture, 2022(555): 738200. doi: 10.1016/j.aquaculture.2022.738200
|
[56] |
张美玲, 单承杰, 杜震宇. 益生菌与鱼类肠道健康研究进展 [J]. 水产学报, 2021, 45(1): 147-157.]
Zhang M L, Shan C J, Du Z Y. Research advances on probiotics and fish gut health [J]. Journal of Fisheries of China, 2021, 45(1): 147-157. [
|
[57] |
Wang A, Zhang Z, Ding Q, et al. Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish [J]. Gut Microbes, 2021, 13(1): 1-15.
|
[58] |
Holt C C, Bass D, Stentiford G D, et al. Understanding the role of the shrimp gut microbiome in health and disease [J]. Journal of Invertebrate Pathology, 2021(186): 107387. doi: 10.1016/j.jip.2020.107387
|
[59] |
张立强, 李媛, 邓平, 等. 健康和患病克氏原螯虾肠道微生物群落结构和多样性分析 [J]. 水产科技情报, 2020, 47(1): 37-40.]
Zhang L Q, Li Y, Deng P, et al. Characterizing the composition and biodiversity of intestinal microbiota between healthy and sick Procambarus Clarkii [J]. Fisheries Science & Technology Information, 2020, 47(1): 37-40. [
|
[60] |
马小荣, 薛晖, 唐建清. 克氏原螯虾致病性嗜水气单胞菌的分离鉴定及药敏试验 [J]. 水产养殖, 2012, 33(8): 45-47.] doi: 10.3969/j.issn.1004-2091.2012.08.021
Ma X R, Xue H, Tang J Q. Isolation, identification and drug sensitivity test of pathogenic Aeromonas hydrophila from Procambarus clarkii [J]. Journal of Aquaculture, 2012, 33(8): 45-47. [ doi: 10.3969/j.issn.1004-2091.2012.08.021
|
[61] |
曹海鹏, 温乐夫, 杨移斌, 等. 克氏原螯虾源致病性豚鼠气单胞菌的分离及其生物学特性 [J]. 水生生物学报, 2014, 38(6): 1047-1053.]
Cao H P, Wen L F, Yang Y B, et al. Isolation and biological characteristics of an Aeromonas caviae pathogen from Procambarus clarkii [J]. Acta Hydrobiologica Sinica, 2014, 38(6): 1047-1053. [
|
[62] |
胡骞, 胡瑞雪, 金玉立, 等. 克氏原螯虾源维氏气单胞菌的分离鉴定及组织病理学观察 [J]. 水生生物学报, 2020, 44(4): 811-818.]
Hu Q, Hu R X, Jin Y L, et al. Isolation, identification and pathohistological observation of Aeromonas veronii from Procambarus clarkii [J]. Acta Hydrobiologica Sinica, 2020, 44(4): 811-818. [
|
[63] |
殷文健, 何俊, 李佳佳, 等. 池塘和稻田养殖环境下克氏原螯虾肠道菌群结构特征及其影响因素 [J]. 饲料研究, 2023, 46(10): 58-65.]
Yin W J, He J, Li J J, et al. Structural characteristics and influencing factors of intestinal microflora of Procrayfish clarkii in ponds and rice fields [J]. Feed Research, 2023, 46(10): 58-65. [
|
[64] |
石玉, 冯光志, 何立超. 克氏原螯虾肠道菌群的结构、功能及其影响因素 [J]. 中国酿造, 2023, 42(11): 28-33.]
Shi Y, Feng G Z, He L C. Structure, function and influencing factors of intestinal microflora from Procambarus clarkii [J]. China Brewing, 2023, 42(11): 28-33. [
|
[65] |
Olesen J M, Bascompte J, Dupont Y L, et al. The modularity of pollination networks [J]. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(50): 19891-19896.
|
[66] |
Newman M E J. Modularity and community structure in networks [J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(23): 8577-8582.
|
[67] |
Zhou J, Luo J, Yang S, et al. Different responses of microbiota across intestinal tract to Enterococcus faecium HDRsEf1 and their correlation with inflammation in weaned piglets [J]. Microorganisms, 2021, 9(8): 1767. doi: 10.3390/microorganisms9081767
|
[68] |
Rimoldi S, Finzi G, Ceccotti C, et al. Butyrate and taurine exert a mitigating effect on the inflamed distal intestine of European sea bass fed with a high percentage of soybean meal [J]. Fisheries and Aquatic Sciences, 2016(19): 40. doi: 10.1186/s41240-016-0041-9
|
[69] |
Estensoro I, Ballester-Lozano G, Benedito-Palos L, et al. Dietary butyrate helps to restore the intestinal status of a marine teleost (Sparus aurata) fed extreme diets low in fish meal and fish oil [J]. PLoS One, 2016, 11(11): e0166564. doi: 10.1371/journal.pone.0166564
|
[70] |
Shao Y, Zhong H, Mao X, et al. Biochar-immobilized Sphingomonas sp. and Acinetobacter sp. isolates to enhance nutrient removal: potential application in crab aquaculture [J]. Aquaculture Environment Interactions, 2020(12): 251-262. doi: 10.3354/aei00364
|
[71] |
Benson A K, Kelly S A, Legge R, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors [J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(44): 18933-18938.
|
[72] |
Van Doan H, Hoseinifar S H, Ringø E, et al. Host-associated probiotics: a key factor in sustainable aquaculture [J]. Reviews in Fisheries Science & Aquaculture, 2020, 28(1): 16-42.
|