Lan Yang, Zhihao Wu, Tian-Yu Ma, Hui Zeng, Ming Chen, Yong-An Zhang, Yang Zhou
{"title":"鉴定参与无乳链球菌应激耐受性和毒力的分子伴侣 ClpB。","authors":"Lan Yang, Zhihao Wu, Tian-Yu Ma, Hui Zeng, Ming Chen, Yong-An Zhang, Yang Zhou","doi":"10.1186/s13567-024-01318-6","DOIUrl":null,"url":null,"abstract":"<p><p>Bacterial ClpB is an ATP-dependent disaggregate that belongs to the Hsp100/Clp family and facilitates bacterial survival under hostile environmental conditions. Streptococcus agalactiae, which is regarded as the major bacterial pathogen of farmed Nile tilapia (Oreochromis niloticus), is known to cause high mortality and large economic losses. Here, we report a ClpB homologue of S. agalactiae and explore its functionality. S. agalactiae with a clpB deletion mutant (∆clpB) exhibited defective tolerance against heat and acidic stress, without affecting growth or morphology under optimal conditions. Moreover, the ΔclpB mutant exhibited reduced intracellular survival in RAW264.7 cells, diminished adherence to the brain cells of tilapia, increased sensitivity to leukocytes from the head kidney of tilapia and whole blood killing, and reduced mortality and bacterial loads in a tilapia infection assay. Furthermore, the reduced virulence of the ∆clpB mutant was investigated by transcriptome analysis, which revealed that deletion of clpB altered the expression levels of multiple genes that contribute to the stress response as well as certain metabolic pathways. Collectively, our findings demonstrated that ClpB, a molecular chaperone, plays critical roles in heat and acid stress resistance and virulence in S. agalactiae. This finding provides an enhanced understanding of the functionality of this ClpB homologue in gram-positive bacteria and the survival strategy of S. agalactiae against immune clearance during infection.</p>","PeriodicalId":23658,"journal":{"name":"Veterinary Research","volume":"55 1","pages":"60"},"PeriodicalIF":3.7000,"publicationDate":"2024-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11094935/pdf/","citationCount":"0","resultStr":"{\"title\":\"Identification of ClpB, a molecular chaperone involved in the stress tolerance and virulence of Streptococcus agalactiae.\",\"authors\":\"Lan Yang, Zhihao Wu, Tian-Yu Ma, Hui Zeng, Ming Chen, Yong-An Zhang, Yang Zhou\",\"doi\":\"10.1186/s13567-024-01318-6\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Bacterial ClpB is an ATP-dependent disaggregate that belongs to the Hsp100/Clp family and facilitates bacterial survival under hostile environmental conditions. Streptococcus agalactiae, which is regarded as the major bacterial pathogen of farmed Nile tilapia (Oreochromis niloticus), is known to cause high mortality and large economic losses. Here, we report a ClpB homologue of S. agalactiae and explore its functionality. S. agalactiae with a clpB deletion mutant (∆clpB) exhibited defective tolerance against heat and acidic stress, without affecting growth or morphology under optimal conditions. Moreover, the ΔclpB mutant exhibited reduced intracellular survival in RAW264.7 cells, diminished adherence to the brain cells of tilapia, increased sensitivity to leukocytes from the head kidney of tilapia and whole blood killing, and reduced mortality and bacterial loads in a tilapia infection assay. Furthermore, the reduced virulence of the ∆clpB mutant was investigated by transcriptome analysis, which revealed that deletion of clpB altered the expression levels of multiple genes that contribute to the stress response as well as certain metabolic pathways. Collectively, our findings demonstrated that ClpB, a molecular chaperone, plays critical roles in heat and acid stress resistance and virulence in S. agalactiae. This finding provides an enhanced understanding of the functionality of this ClpB homologue in gram-positive bacteria and the survival strategy of S. agalactiae against immune clearance during infection.</p>\",\"PeriodicalId\":23658,\"journal\":{\"name\":\"Veterinary Research\",\"volume\":\"55 1\",\"pages\":\"60\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2024-05-15\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11094935/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Veterinary Research\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://doi.org/10.1186/s13567-024-01318-6\",\"RegionNum\":1,\"RegionCategory\":\"农林科学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"VETERINARY SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Veterinary Research","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1186/s13567-024-01318-6","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"VETERINARY SCIENCES","Score":null,"Total":0}
引用次数: 0
摘要
细菌 ClpB 是一种 ATP 依赖性分解物,属于 Hsp100/Clp 家族,有助于细菌在恶劣的环境条件下生存。众所周知,被认为是尼罗罗非鱼(Oreochromis niloticus)养殖过程中主要细菌病原体的半乳链球菌(Streptococcus agalactiae)会造成很高的死亡率和巨大的经济损失。在此,我们报告了一种 S. agalactiae 的 ClpB 同源物,并探讨了其功能。具有clpB缺失突变体(ΔclpB)的S. agalactiae对热和酸性胁迫的耐受性有缺陷,但不影响其在最佳条件下的生长和形态。此外,ΔclpB 突变体在 RAW264.7 细胞中的胞内存活率降低,对罗非鱼脑细胞的粘附性减弱,对来自罗非鱼头部肾脏的白细胞和全血杀灭的敏感性增加,罗非鱼感染试验中的死亡率和细菌载量降低。此外,我们还通过转录组分析研究了 ∆clpB 突变体毒力降低的情况,结果表明 clpB 的缺失改变了多个基因的表达水平,而这些基因有助于应激反应和某些代谢途径。总之,我们的研究结果表明,ClpB 是一种分子伴侣蛋白,在 S. agalactiae 的抗热和抗酸胁迫以及毒力方面发挥着关键作用。这一发现加深了人们对革兰氏阳性菌中 ClpB 同源物的功能以及 S. agalactiae 在感染期间抵御免疫清除的生存策略的了解。
Identification of ClpB, a molecular chaperone involved in the stress tolerance and virulence of Streptococcus agalactiae.
Bacterial ClpB is an ATP-dependent disaggregate that belongs to the Hsp100/Clp family and facilitates bacterial survival under hostile environmental conditions. Streptococcus agalactiae, which is regarded as the major bacterial pathogen of farmed Nile tilapia (Oreochromis niloticus), is known to cause high mortality and large economic losses. Here, we report a ClpB homologue of S. agalactiae and explore its functionality. S. agalactiae with a clpB deletion mutant (∆clpB) exhibited defective tolerance against heat and acidic stress, without affecting growth or morphology under optimal conditions. Moreover, the ΔclpB mutant exhibited reduced intracellular survival in RAW264.7 cells, diminished adherence to the brain cells of tilapia, increased sensitivity to leukocytes from the head kidney of tilapia and whole blood killing, and reduced mortality and bacterial loads in a tilapia infection assay. Furthermore, the reduced virulence of the ∆clpB mutant was investigated by transcriptome analysis, which revealed that deletion of clpB altered the expression levels of multiple genes that contribute to the stress response as well as certain metabolic pathways. Collectively, our findings demonstrated that ClpB, a molecular chaperone, plays critical roles in heat and acid stress resistance and virulence in S. agalactiae. This finding provides an enhanced understanding of the functionality of this ClpB homologue in gram-positive bacteria and the survival strategy of S. agalactiae against immune clearance during infection.
期刊介绍:
Veterinary Research is an open access journal that publishes high quality and novel research and review articles focusing on all aspects of infectious diseases and host-pathogen interaction in animals.