粪肠球菌抑制铜绿假单胞菌烷基喹诺酮类药物的反应。

IF 5.1 1区 生物学 Q1 MICROBIOLOGY
mBio Pub Date : 2025-02-05 Epub Date: 2024-12-27 DOI:10.1128/mbio.03320-24
Maggie M Fink, Abigail A Weaver, Dharmeshkumar Parmar, Jon E Paczkowski, Lingyun Li, Maggie K Klaers, Ella A Junker, Elizabeth A Jarocki, Jonathan V Sweedler, Joshua D Shrout
{"title":"粪肠球菌抑制铜绿假单胞菌烷基喹诺酮类药物的反应。","authors":"Maggie M Fink, Abigail A Weaver, Dharmeshkumar Parmar, Jon E Paczkowski, Lingyun Li, Maggie K Klaers, Ella A Junker, Elizabeth A Jarocki, Jonathan V Sweedler, Joshua D Shrout","doi":"10.1128/mbio.03320-24","DOIUrl":null,"url":null,"abstract":"<p><p>The bacterium <i>Pseudomonas aeruginosa</i> is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While <i>P. aeruginosa</i> is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in polymicrobial infections where multiple species survive. For example, in prosthetic joint infections, <i>P. aeruginosa</i> can be identified along with other pathogenic bacteria including <i>Staphylococcus aureus</i>, <i>Enterococcus faecalis</i>, and <i>Corynebacterium striatum</i>. Here, we have explored the survival and behavior of such microbes and find that <i>E. faecalis</i> readily survives culturing with <i>P. aeruginosa</i> while other tested species do not. In each of the tested conditions, <i>E. faecalis</i> growth remained unchanged by the presence of <i>P. aeruginosa</i>, indicating a unique mutualistic interaction between the two species. We find that <i>E. faecalis</i> proximity leads <i>P. aeruginosa</i> to attenuate competitive behaviors as exemplified by reduced production of <i>Pseudomonas</i> quinolone signal and pyocyanin. Reduced alkyl quinolones are important to <i>E. faecalis</i> as these will grow in supernatant from a quinolone mutant but not <i>P. aeruginosa</i> wild-type in planktonic culture. The reduced pyocyanin production of <i>P. aeruginosa</i> is attributable to production of ornithine by <i>E. faecalis</i>, which we recapitulate by adding exogenous ornithine to <i>P. aeruginosa</i> monocultures. Similarly, co-culture with an ornithine-deficient strain of <i>E. faecalis</i> leads <i>P. aeruginosa</i> to yield near monoculture amounts of pyocyanin. Here, we directly demonstrate how notorious pathogens such as <i>P. aeruginosa</i> might persist in polymicrobial infections under the influence of metabolites produced by other bacterial species.</p><p><strong>Importance: </strong>While we now appreciate that many infections are polymicrobial, we understand little of the specific actions between a given set of microbes to enable combinatorial survival and pathogenesis. The bacteria <i>Pseudomonas aeruginosa</i> and <i>Enterococcus faecalis</i> are both prevalent pathogens in wound, urinary tract, and bacteremic infections. While <i>P. aeruginosa</i> often kills other species in standard laboratory culture conditions, we present here that <i>E. faecalis</i> can be reliably co-cultured with <i>P. aeruginosa</i>. We specifically detail that ornithine produced by <i>E. faecalis</i> reduces the <i>Pseudomonas</i> quinolone signal response of <i>P. aeruginosa</i>. This reduction of the <i>Pseudomonas</i> quinolone signal response aids <i>E. faecalis</i> growth.</p>","PeriodicalId":18315,"journal":{"name":"mBio","volume":" ","pages":"e0332024"},"PeriodicalIF":5.1000,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11796420/pdf/","citationCount":"0","resultStr":"{\"title\":\"<i>Pseudomonas aeruginosa</i> alkyl quinolone response is dampened by <i>Enterococcus faecalis</i>.\",\"authors\":\"Maggie M Fink, Abigail A Weaver, Dharmeshkumar Parmar, Jon E Paczkowski, Lingyun Li, Maggie K Klaers, Ella A Junker, Elizabeth A Jarocki, Jonathan V Sweedler, Joshua D Shrout\",\"doi\":\"10.1128/mbio.03320-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The bacterium <i>Pseudomonas aeruginosa</i> is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While <i>P. aeruginosa</i> is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in polymicrobial infections where multiple species survive. For example, in prosthetic joint infections, <i>P. aeruginosa</i> can be identified along with other pathogenic bacteria including <i>Staphylococcus aureus</i>, <i>Enterococcus faecalis</i>, and <i>Corynebacterium striatum</i>. Here, we have explored the survival and behavior of such microbes and find that <i>E. faecalis</i> readily survives culturing with <i>P. aeruginosa</i> while other tested species do not. In each of the tested conditions, <i>E. faecalis</i> growth remained unchanged by the presence of <i>P. aeruginosa</i>, indicating a unique mutualistic interaction between the two species. We find that <i>E. faecalis</i> proximity leads <i>P. aeruginosa</i> to attenuate competitive behaviors as exemplified by reduced production of <i>Pseudomonas</i> quinolone signal and pyocyanin. Reduced alkyl quinolones are important to <i>E. faecalis</i> as these will grow in supernatant from a quinolone mutant but not <i>P. aeruginosa</i> wild-type in planktonic culture. The reduced pyocyanin production of <i>P. aeruginosa</i> is attributable to production of ornithine by <i>E. faecalis</i>, which we recapitulate by adding exogenous ornithine to <i>P. aeruginosa</i> monocultures. Similarly, co-culture with an ornithine-deficient strain of <i>E. faecalis</i> leads <i>P. aeruginosa</i> to yield near monoculture amounts of pyocyanin. Here, we directly demonstrate how notorious pathogens such as <i>P. aeruginosa</i> might persist in polymicrobial infections under the influence of metabolites produced by other bacterial species.</p><p><strong>Importance: </strong>While we now appreciate that many infections are polymicrobial, we understand little of the specific actions between a given set of microbes to enable combinatorial survival and pathogenesis. The bacteria <i>Pseudomonas aeruginosa</i> and <i>Enterococcus faecalis</i> are both prevalent pathogens in wound, urinary tract, and bacteremic infections. While <i>P. aeruginosa</i> often kills other species in standard laboratory culture conditions, we present here that <i>E. faecalis</i> can be reliably co-cultured with <i>P. aeruginosa</i>. We specifically detail that ornithine produced by <i>E. faecalis</i> reduces the <i>Pseudomonas</i> quinolone signal response of <i>P. aeruginosa</i>. This reduction of the <i>Pseudomonas</i> quinolone signal response aids <i>E. faecalis</i> growth.</p>\",\"PeriodicalId\":18315,\"journal\":{\"name\":\"mBio\",\"volume\":\" \",\"pages\":\"e0332024\"},\"PeriodicalIF\":5.1000,\"publicationDate\":\"2025-02-05\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11796420/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"mBio\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/mbio.03320-24\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/12/27 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"mBio","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/mbio.03320-24","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/12/27 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

铜绿假单胞菌是一种机会致病菌,可引起肺部、皮肤、伤口、关节、尿路和眼睛感染。虽然已知铜绿假单胞菌对其他细菌物种表现出强大的竞争反应,但这种细菌经常在多微生物感染中被发现,其中多个物种存活。例如,在假体关节感染中,铜绿假单胞菌可与其他致病菌包括金黄色葡萄球菌、粪肠球菌和纹状棒状杆菌一起被鉴定出来。在这里,我们探索了这些微生物的生存和行为,发现粪肠杆菌很容易与铜绿假单胞菌一起培养,而其他被测试的物种则没有。在每一种测试条件下,粪肠杆菌的生长在铜绿假单胞菌的存在下保持不变,表明这两个物种之间存在独特的互惠相互作用。我们发现粪肠杆菌的接近导致铜绿假单胞菌的竞争行为减弱,例如喹诺酮假单胞菌信号和pyocyanin的产生减少。还原烷基喹诺酮类药物对粪肠杆菌很重要,因为它们会在喹诺酮类药物突变体的上清中生长,而不是浮游培养的铜绿假单胞菌野生型上清。铜绿假单胞菌的pyocyanin产量的减少是由于E. faecalis产生鸟氨酸,我们通过在单株铜绿假单胞菌中添加外源鸟氨酸来概括。同样,与缺乏鸟氨酸的粪肠球菌共同培养,铜绿假单胞菌产生接近单一培养量的pyocyanin。在这里,我们直接证明了臭名昭著的病原体,如铜绿假单胞菌,在其他细菌种类产生的代谢物的影响下,如何在多微生物感染中持续存在。重要性:虽然我们现在认识到许多感染是多微生物的,但我们对一组给定微生物之间的特定作用知之甚少,这些作用使组合生存和发病机制成为可能。铜绿假单胞菌和粪肠球菌都是伤口、尿路和细菌性感染的常见病原体。虽然铜绿假单胞菌在标准的实验室培养条件下经常杀死其他物种,但我们在这里提出,粪肠杆菌可以可靠地与铜绿假单胞菌共培养。我们特别详细说明了粪肠杆菌产生的鸟氨酸降低了铜绿假单胞菌的喹诺酮类假单胞菌的信号反应。这种喹诺酮假单胞菌信号反应的减少有助于粪肠杆菌的生长。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Pseudomonas aeruginosa alkyl quinolone response is dampened by Enterococcus faecalis.

The bacterium Pseudomonas aeruginosa is an opportunistic pathogen that can cause lung, skin, wound, joint, urinary tract, and eye infections. While P. aeruginosa is known to exhibit a robust competitive response toward other bacterial species, this bacterium is frequently identified in polymicrobial infections where multiple species survive. For example, in prosthetic joint infections, P. aeruginosa can be identified along with other pathogenic bacteria including Staphylococcus aureus, Enterococcus faecalis, and Corynebacterium striatum. Here, we have explored the survival and behavior of such microbes and find that E. faecalis readily survives culturing with P. aeruginosa while other tested species do not. In each of the tested conditions, E. faecalis growth remained unchanged by the presence of P. aeruginosa, indicating a unique mutualistic interaction between the two species. We find that E. faecalis proximity leads P. aeruginosa to attenuate competitive behaviors as exemplified by reduced production of Pseudomonas quinolone signal and pyocyanin. Reduced alkyl quinolones are important to E. faecalis as these will grow in supernatant from a quinolone mutant but not P. aeruginosa wild-type in planktonic culture. The reduced pyocyanin production of P. aeruginosa is attributable to production of ornithine by E. faecalis, which we recapitulate by adding exogenous ornithine to P. aeruginosa monocultures. Similarly, co-culture with an ornithine-deficient strain of E. faecalis leads P. aeruginosa to yield near monoculture amounts of pyocyanin. Here, we directly demonstrate how notorious pathogens such as P. aeruginosa might persist in polymicrobial infections under the influence of metabolites produced by other bacterial species.

Importance: While we now appreciate that many infections are polymicrobial, we understand little of the specific actions between a given set of microbes to enable combinatorial survival and pathogenesis. The bacteria Pseudomonas aeruginosa and Enterococcus faecalis are both prevalent pathogens in wound, urinary tract, and bacteremic infections. While P. aeruginosa often kills other species in standard laboratory culture conditions, we present here that E. faecalis can be reliably co-cultured with P. aeruginosa. We specifically detail that ornithine produced by E. faecalis reduces the Pseudomonas quinolone signal response of P. aeruginosa. This reduction of the Pseudomonas quinolone signal response aids E. faecalis growth.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
mBio
mBio MICROBIOLOGY-
CiteScore
10.50
自引率
3.10%
发文量
762
审稿时长
1 months
期刊介绍: mBio® is ASM''s first broad-scope, online-only, open access journal. mBio offers streamlined review and publication of the best research in microbiology and allied fields.
×
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:481959085
Book学术官方微信