Regulatory network of nucleotide second messenger in Pseudomonas aeruginosa PFL-P1 and intercellular signaling molecules for functional amyloid fibrillation in biofilm and stress response.

IF 3.4 4区 生物学 Q3 MICROBIOLOGY
Swetambari Kumari, Surajit Das
{"title":"Regulatory network of nucleotide second messenger in Pseudomonas aeruginosa PFL-P1 and intercellular signaling molecules for functional amyloid fibrillation in biofilm and stress response.","authors":"Swetambari Kumari, Surajit Das","doi":"10.1016/j.resmic.2025.104350","DOIUrl":null,"url":null,"abstract":"<p><p>Biofilm formation is governed by quorum sensing (QS) and intracellular signaling, with cyclic di-GMP (c-di-GMP) acting as a key regulator that modulates biofilm stability in response to environmental cues. The present study aims to explore the regulatory network between QS, c-di-GMP signaling, and amyloid production in the marine biofilm-forming bacterium Pseudomonas aeruginosa PFL-P1 under various physicochemical stressors. P. aeruginosa PFL-P1 demonstrated adaptability to diverse conditions typical of marine habitats, attributed to the activity of diguanylate cyclase (dgc86) and phosphodiesterase (pde94) genes regulating c-di-GMP turnover. Gene expression analysis revealed a coordinated regulatory network during biofilm development, with significant upregulation of dgc86, pde94, fapC (functional amyloid synthesis), lasI, rhlI (QS), and nahAc [polycyclic aromatic hydrocarbon (PAH) degradation] at 48 h, indicating a mature biofilm. Under acidic condition (pH 4), all genes except pde94 exhibited an adaptive response (p<0.0001). Salinity ≤1 % enhanced gene expression, whereas salinity ≥5 % suppressed it due to osmotic stress (p<0.0001). At 40 °C, dgc86 (p=0.0457) and fapC (p=0.0444) were upregulated, promoting biofilm stability. Pyrene exposure induced significant upregulation of dgc86, lasI, rhlI, and nahAc (p<0.05), enhancing biofilm formation and PAH degradation while downregulating pde94. Supplementation with C4-HSL and 3OC12-HSL upregulated these genes, reinforcing the role of QS in biofilm regulation. Terrein, a QS and c-di-GMP inhibitor downregulated fapC and nahAc, disrupting biofilm formation and PAH degradation. The strong correlation between c-di-GMP levels, amyloid production, and its high binding affinity to FapC (-11.8 kcal/mol) suggests a dual role for c-di-GMP as a signaling molecule and molecular chaperone in amyloid assembly.</p>","PeriodicalId":21098,"journal":{"name":"Research in microbiology","volume":" ","pages":"104350"},"PeriodicalIF":3.4000,"publicationDate":"2025-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Research in microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.resmic.2025.104350","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Biofilm formation is governed by quorum sensing (QS) and intracellular signaling, with cyclic di-GMP (c-di-GMP) acting as a key regulator that modulates biofilm stability in response to environmental cues. The present study aims to explore the regulatory network between QS, c-di-GMP signaling, and amyloid production in the marine biofilm-forming bacterium Pseudomonas aeruginosa PFL-P1 under various physicochemical stressors. P. aeruginosa PFL-P1 demonstrated adaptability to diverse conditions typical of marine habitats, attributed to the activity of diguanylate cyclase (dgc86) and phosphodiesterase (pde94) genes regulating c-di-GMP turnover. Gene expression analysis revealed a coordinated regulatory network during biofilm development, with significant upregulation of dgc86, pde94, fapC (functional amyloid synthesis), lasI, rhlI (QS), and nahAc [polycyclic aromatic hydrocarbon (PAH) degradation] at 48 h, indicating a mature biofilm. Under acidic condition (pH 4), all genes except pde94 exhibited an adaptive response (p<0.0001). Salinity ≤1 % enhanced gene expression, whereas salinity ≥5 % suppressed it due to osmotic stress (p<0.0001). At 40 °C, dgc86 (p=0.0457) and fapC (p=0.0444) were upregulated, promoting biofilm stability. Pyrene exposure induced significant upregulation of dgc86, lasI, rhlI, and nahAc (p<0.05), enhancing biofilm formation and PAH degradation while downregulating pde94. Supplementation with C4-HSL and 3OC12-HSL upregulated these genes, reinforcing the role of QS in biofilm regulation. Terrein, a QS and c-di-GMP inhibitor downregulated fapC and nahAc, disrupting biofilm formation and PAH degradation. The strong correlation between c-di-GMP levels, amyloid production, and its high binding affinity to FapC (-11.8 kcal/mol) suggests a dual role for c-di-GMP as a signaling molecule and molecular chaperone in amyloid assembly.

铜绿假单胞菌核苷酸第二信使PFL-P1和细胞间信号分子对生物膜和应激反应中功能性淀粉样蛋白颤动的调控网络。
生物膜的形成是由群体感应(QS)和细胞内信号传导控制的,环二gmp (c-di-GMP)作为一个关键的调节剂,在响应环境信号的情况下调节生物膜的稳定性。本研究旨在探讨海洋生物膜形成细菌铜绿假单胞菌PFL-P1在不同理化应激条件下QS、c-di-GMP信号通路与淀粉样蛋白生成之间的调控网络。P. aeruginosa PFL-P1表现出对多种典型海洋栖息地条件的适应性,这归因于调节c-di-GMP周转的二胍酸环化酶(dgc86)和磷酸二酯酶(pde94)基因的活性。基因表达分析显示,在生物膜发育过程中存在一个协调的调控网络,在48 h时dgc86、pde94、fapC(功能性淀粉样蛋白合成)、lasI、rhlI (QS)和nahAc(多环芳烃(PAH)降解)显著上调,表明生物膜已经成熟。在酸性条件下(pH 4),除pde94外,其他基因均表现出适应性反应(p
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Research in microbiology
Research in microbiology 生物-微生物学
CiteScore
4.10
自引率
3.80%
发文量
54
审稿时长
16 days
期刊介绍: Research in Microbiology is the direct descendant of the original Pasteur periodical entitled Annales de l''Institut Pasteur, created in 1887 by Emile Duclaux under the patronage of Louis Pasteur. The Editorial Committee included Chamberland, Grancher, Nocard, Roux and Straus, and the first issue began with Louis Pasteur''s "Lettre sur la Rage" which clearly defines the spirit of the journal:"You have informed me, my dear Duclaux, that you intend to start a monthly collection of articles entitled "Annales de l''Institut Pasteur". You will be rendering a service that will be appreciated by the ever increasing number of young scientists who are attracted to microbiological studies. In your Annales, our laboratory research will of course occupy a central position, but the work from outside groups that you intend to publish will be a source of competitive stimulation for all of us."That first volume included 53 articles as well as critical reviews and book reviews. From that time on, the Annales appeared regularly every month, without interruption, even during the two world wars. Although the journal has undergone many changes over the past 100 years (in the title, the format, the language) reflecting the evolution in scientific publishing, it has consistently maintained the Pasteur tradition by publishing original reports on all aspects of microbiology.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信
小红书