The Impacts and Mechanism of Streptococcus agalactiae on Behavior of GIFT Tilapia (Oreochromis niloticus)
YI Meng-Meng, WANG Miao, LI Zhong-Hui, ZHANG De-Feng, LIU Zhi-Gang, Gao Feng-Ying, LU Mai-Xin*
Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou 510380, China
Abstract:Streptococcus agalactiae infection may cause abnormal behavior of tilapia (Oreochromis niloticus) and seriously endangers the development of the tilapia industry.To investigate the impacts of S.agalactiae on behavior of GIFT tilapia and its mechanism, the qRT-PCR and immunofluorescence were used to examine the concentration of S.agalactiae in the brain and intestine, the behavior changes, as well as the expression of 5-hydroxytryptamine (5-HT) in the cerebellum, intestine and stomach of tilapia infected with by intraperitoneal injection.The results showed that the copies of S.agalactiae in the brain and intestinal tissues of tilapia increased sharply from the 6th and 0 h after pathogen infection respectively, and reached the maximum at 18th h (61.2 copies /mg in the brain and 1 800.5 copies/ mg in the intestine).Furthermore, fish showed abnormal behavior from the 12th h after pathogen challenge, and the abnormal behavior continued until the end of the experiment or the death of the fish.In addition, 5-HT positive reaction was found in the cerebellum, intestine and stomach of tilapia before and after S. agalactiae infection.While the positive reaction of 5-HT in cerebellum and intestine showed a weakening trend with the prolongation of experiment, and the fluorescence intensity of cerebellum and intestine were 9.1 and 6.9 at 18th h, respectively.But the 5-HT positive reaction in stomach increased first and then decreased with experiment went on, reaching a minimum of 3.1 at the end of the experiment.Therefore, it could be speculated that after infection of S.agalactia, tilapia induces abnormal behavior of tilapia by regulating 5-HT in the central nervous system and the peripheral digestive system.The current study researched the abnormal behavior of tilapia after S.agalactiae infection from the perspective of 5-HT, which could provide a new insight into the mechanism of impulsive behavior of fish infected with pathogen.
衣萌萌, 王淼, 李忠徽, 张德锋, 刘志刚, 高风英, 卢迈新. 无乳链球菌感染对吉富罗非鱼行为的影响及其机制[J]. 农业生物技术学报, 2019, 27(5): 799-808.
YI Meng-Meng, WANG Miao, LI Zhong-Hui, ZHANG De-Feng, LIU Zhi-Gang, Gao Feng-Ying, LU Mai-Xin. The Impacts and Mechanism of Streptococcus agalactiae on Behavior of GIFT Tilapia (Oreochromis niloticus). 农业生物技术学报, 2019, 27(5): 799-808.
[1] 段云峰, 吴晓丽, 王涛, 等.2013.五羟色胺和多巴胺与攻击行为的关联研究进展[J].生命科学, 25(10): 1027-1035. (Duan Y F, Wu X L, Wang T, et al.2013.Research progress on the correlations of aggressive behavior with serotonin and dopamine[J].Chinese Bulletin of Life Sciences, 25(10): 1027-1035.) [2] 方静, 樊均德, 陈玥.2012.齐口裂腹鱼脑内5-羟色胺免疫组织化学的定位观察[J].水生生物学报, 36(1): 143-147. (Fang J, Fan J D, Chen Y.2012.The Immunocytochemical study on the distribution of 5-hydroxytryptamine in the brain of Schizothorax prenantia[J].Acta Hydrobiological Sinica.36(1): 143-147.). [3] 黄威权, 方永强, 苏慧慈, 等.1990.文昌鱼体内5-羟色胺免疫组织化学定位的研究[J].科学通报, 35(15): 1187-1189. (Huang W Q, Fang Y Q, Su H C, et al.1990.Immunocytochemical study on the distribution of 5-Hydroxytryptamine in the brain of Branchiostoma belcheri[J].Chinese Science Bulletin, 35(15) :1187-1189.) [4] 阚延胜.2007.罗非鱼消化道5-HT内分泌细胞的免疫组织化学研究[J].安徽农学通报, 13(17): 27-28. (Kan Y S.2007.Studies on immunohistochemistry of 5-HT endocrine cells in the digestive tract of tilapia Mossamblca[J].Anhui Agricultural Science Bulletin, 13(17): 27-28.) [5] 卢迈新.2010.罗非鱼链球菌病研究进展[J].南方水产科学, 6(1): 75-79. (Lu M X.2010.Review of research on streptococcosis in tilapia[J].South China Fisheries Science, 6(1): 75-79.) [6] 卢迈新, 黎炯, 叶星, 等.2010.广东与海南养殖罗非鱼无乳链球菌的分离、鉴定与特性分析[J].微生物学通报, 37(5): 766-774. (Lu M X, Li J, Ye X, et al.2010.Identification and characterizations of Streptococcus agalactiae isolated from tilapia cultured in Guangdong and Hainan provinces[J].Microbiology China, 37(5): 766-774.) [7] 罗佳, 金锋.2014.肠道菌群影响宿主行为的研究进展[J].科学通报, 59(22): 2169-2190. (Luo J, Jin F.2014.Recent advances in understanding the impact of intestinal microbiota on host behavior (in Chinese)[J].Chinese Science Bulletin (Chinese Version), 59(22): 2169-2190.) [8] 燕晋媛.2015.细菌侵染线虫所诱发的逃避和免疫之间消长平衡的分子机制研究[D].博士学位论文, 云南大学, 导师: 黄晓玮.pp.Ⅰ-Ⅱ. (Yan J Y.2015.Molecular mechanism underlying the counter balance between avoidance and immunne response inCaenorhabditis elegans[D].Thesis for Ph.D., Yunnan University, Supervisor: Huang X W, pp.Ⅰ-Ⅱ.) [9] Airhart M J, Lee D H, Wilson T D, et al.2012.Adverse effects of serotonin depletion in developing zebrafish[J].Neurotoxicology & Teratology, 34(1): 152-160. [10] Alzghoul L, Bortolato M, Delis F, et al.2012.Altered cerebellar organization and function in monoamine oxidase A hypomorphic mice[J].Neuropharmacology, 63(7): 1208-1217. [11] Bercik P, Verdu E F, Foster J A, et al.2010.Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice[J].Gastroenterology, 139(6): 2102-2112. [12] Bortolato M, Pivac N, Seler D M, et al.2013.The role of the serotonergic system at the interface of aggression and suicide[J].Neuroscience, 236: 160-185. [13] Goehler L E, Su M P, Opitz N, et al.2008.Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: Possible anatomical substrates for viscerosensory modulation of exploratory behavior[J].Brain Behavior & Immunity, 22(3): 354-366. [14] Hannon J, Hoyer D.2008.Molecular biology of 5-HT receptors[J].Behavioural Brain Research, 195(1): 198-213. [15] Hoover K, Grove M, Gardner M, et al.2011.A gene for an extended phenotype[J].Science, 333(6048): 1401. [16] Lyte M, Li W, Opitz N, et al.2006.Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium[J].Physiology & Behavior, 89(3): 350-357. [17] Nelson R J, Chiavegatto S.2001.Molecular basis of aggression[J].Trends in Neurosciences, 24(12): 713-719. [18] Norton W H J, Folchert A, Bally-Cuif L.2008.Comparative analysis of serotonin receptor (HTR1A/HTR1B families) and transporter (slc6a4a/b) gene expression in the zebrafish brain[J].Journal of Comparative Neurology, 511(4): 521-542. [19] Nowicki M, Tran S, Muraleetharan A, et al.2014.Serotonin antagonists induce anxiolytic and anxiogenic-like behavior in zebrafish in a receptor-subtype dependent manner[J].Pharmacology Biochemistry & Behavior, 126: 170-180. [20] Rapport M M, Green A A, Page I H.1948.Crystalline serotonin[J].Science, 108(2804): 329-330. [21] Rodriguez-Gomez F J, Rendon-Unceta M C, Sarasquete C, et al.2000.Localization of tyrosine hydroxylase-immunoreactivity in the brain of the Senegalese sole, Solea senegalensis[J].Journal of Chemical Neuroanatomy, 19(1): 17-32. [22] Honma S.1970.Presence of monoaminergic neurons in the spinal cord and intestine of the lamprey, Lampetra japonica[J].Archivum Histologicum Japonicum, 32(4): 383-393. [23] Schneider H, Fritzky L, Williams J, et al.2012.Cloning and expression of a zebrafish 5-HT2C receptor gene[J].Gene, 502(2): 108-117. [24] Wang B, Gan Z, Wang Z, et al.2017.Integrated analysis neurimmirs of tilapia (Oreochromis niloticus) involved in immune response to Streptococcus agalactiae, a pathogen causing meningoencephalitis in teleosts[J].Fish & Shellfish Immunology, 61: 44-60. [25] Wang G, Zhang J, Shen Y, et al.2015.Transcriptome analysis of the brain of the silkworm Bombyx mori infected with Bombyx mori nucleopolyhedrovirus: A new insight into the molecular mechanism of enhanced locomotor activity induced by viral infection[J].Journal of Invertebrate Pathology, 128: 37-43. [26] Winberg S, Thörnqvist P O.2016.Role of brain serotonin in modulating fish behavior[J].Current Zoology, 62(3): 317-323. [27] Zhang H, Wen W, Yan J.2017.Application of immunohistochemistry technique in hydrobiological studies[J].Aquaculture and Fisheries, 2: 140-144.