Interspecies synergistic interactions mediated by cofactor exchange enhance stress tolerance by inducing biofilm formation.

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-09-17 Epub Date: 2024-08-27 DOI:10.1128/msystems.00884-24
Lvjing Wang, Xiaoyu Wang, Hao Wu, Haixia Wang, Zhenmei Lu
{"title":"Interspecies synergistic interactions mediated by cofactor exchange enhance stress tolerance by inducing biofilm formation.","authors":"Lvjing Wang, Xiaoyu Wang, Hao Wu, Haixia Wang, Zhenmei Lu","doi":"10.1128/msystems.00884-24","DOIUrl":null,"url":null,"abstract":"<p><p>Metabolic exchange plays a crucial role in shaping microbial community interactions and functions, including the exchange of small molecules such as cofactors. Cofactors are fundamental to enzyme catalytic activities; however, the role of cofactors in microbial stress tolerance is unclear. Here, we constructed a synergistic consortium containing two strains that could efficiently mineralize di-(2-ethylhexyl) phthalate under hyperosmotic stress. Integration of transcriptomic analysis, metabolic profiling, and a genome-scale metabolic model (GEM) facilitated the discovery of the potential mechanism of microbial interactions. Multi-omics analysis revealed that the vitamin B<sub>12</sub>-dependent methionine-folate cycle could be a key pathway for enhancing the hyperosmotic stress tolerance of synergistic consortium. Further GEM simulations revealed interspecies exchange of S-adenosyl-L-methionine and riboflavin, cofactors needed for vitamin B<sub>12</sub> biosynthesis, which was confirmed by <i>in vitro</i> experiments. Overall, we proposed a new mechanism of bacterial hyperosmotic stress tolerance: bacteria might promote the production of vitamin B<sub>12</sub> to enhance biofilm formation, and the species collaborate with each other by exchanging cofactors to improve consortium hyperosmotic stress tolerance. These findings offer new insights into the role of cofactors in microbial interactions and stress tolerance and are potentially exploitable for environmental remediation.</p><p><strong>Importance: </strong>Metabolic interactions (also known as cross-feeding) are thought to be ubiquitous in microbial communities. Cross-feeding is the basis for many positive interactions (e.g., mutualism) and is a primary driver of microbial community assembly. In this study, a combination of multi-omics analysis and metabolic modeling simulation was used to reveal the metabolic interactions of a synthetic consortium under hyperosmotic stress. Interspecies cofactor exchange was found to promote biofilm formation under hyperosmotic stress. This provides a new perspective for understanding the role of metabolic interactions in microbial communities to enhance environmental adaptation, which is significant for improving the efficiency of production activities and environmental bioremediation.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":null,"pages":null},"PeriodicalIF":5.0000,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11406921/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSystems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msystems.00884-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/8/27 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Metabolic exchange plays a crucial role in shaping microbial community interactions and functions, including the exchange of small molecules such as cofactors. Cofactors are fundamental to enzyme catalytic activities; however, the role of cofactors in microbial stress tolerance is unclear. Here, we constructed a synergistic consortium containing two strains that could efficiently mineralize di-(2-ethylhexyl) phthalate under hyperosmotic stress. Integration of transcriptomic analysis, metabolic profiling, and a genome-scale metabolic model (GEM) facilitated the discovery of the potential mechanism of microbial interactions. Multi-omics analysis revealed that the vitamin B12-dependent methionine-folate cycle could be a key pathway for enhancing the hyperosmotic stress tolerance of synergistic consortium. Further GEM simulations revealed interspecies exchange of S-adenosyl-L-methionine and riboflavin, cofactors needed for vitamin B12 biosynthesis, which was confirmed by in vitro experiments. Overall, we proposed a new mechanism of bacterial hyperosmotic stress tolerance: bacteria might promote the production of vitamin B12 to enhance biofilm formation, and the species collaborate with each other by exchanging cofactors to improve consortium hyperosmotic stress tolerance. These findings offer new insights into the role of cofactors in microbial interactions and stress tolerance and are potentially exploitable for environmental remediation.

Importance: Metabolic interactions (also known as cross-feeding) are thought to be ubiquitous in microbial communities. Cross-feeding is the basis for many positive interactions (e.g., mutualism) and is a primary driver of microbial community assembly. In this study, a combination of multi-omics analysis and metabolic modeling simulation was used to reveal the metabolic interactions of a synthetic consortium under hyperosmotic stress. Interspecies cofactor exchange was found to promote biofilm formation under hyperosmotic stress. This provides a new perspective for understanding the role of metabolic interactions in microbial communities to enhance environmental adaptation, which is significant for improving the efficiency of production activities and environmental bioremediation.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
由辅助因子交换介导的种间协同作用通过诱导生物膜的形成增强了应激耐受性。
代谢交换在形成微生物群落相互作用和功能方面起着至关重要的作用,其中包括小分子(如辅助因子)的交换。辅助因子是酶催化活性的基础;然而,辅助因子在微生物胁迫耐受性中的作用尚不清楚。在这里,我们构建了一个包含两种菌株的协同菌群,它们能在高渗透胁迫下高效矿化邻苯二甲酸二(2-乙基己基)酯。整合转录组分析、代谢分析和基因组尺度代谢模型(GEM)有助于发现微生物相互作用的潜在机制。多组学分析表明,依赖于维生素 B12 的蛋氨酸-叶酸循环可能是增强协同菌群高渗胁迫耐受性的关键途径。进一步的 GEM 模拟揭示了维生素 B12 生物合成所需的辅助因子 S-腺苷-L-蛋氨酸和核黄素的种间交换,体外实验也证实了这一点。总之,我们提出了细菌耐高渗胁迫的新机制:细菌可能会促进维生素 B12 的生成以增强生物膜的形成,而菌种之间则通过交换辅助因子来提高联合体的耐高渗胁迫能力。这些发现为了解辅助因子在微生物相互作用和应激耐受性中的作用提供了新的视角,并有可能用于环境修复:重要意义:代谢相互作用(也称为交叉供食)被认为在微生物群落中无处不在。交叉取食是许多积极互动(如互惠)的基础,也是微生物群落组合的主要驱动力。本研究结合多组学分析和代谢模型模拟,揭示了高渗透胁迫下合成联合体的代谢相互作用。研究发现,种间辅助因子交换可促进高渗透压下生物膜的形成。这为理解微生物群落中的代谢相互作用在增强环境适应性方面的作用提供了一个新的视角,对提高生产活动和环境生物修复的效率具有重要意义。
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 去求助
来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
期刊最新文献
Effect of combined probiotics and doxycycline therapy on the gut-skin axis in rosacea. Stable, multigenerational transmission of the bean seed microbiome despite abiotic stress. Antimicrobial and antibiofilm activity of human recombinant H1 histones against bacterial infections. Gut and oral microbial compositional differences in women with breast cancer, women with ductal carcinoma in situ, and healthy women. Metagenomic sequencing of CRISPRs as a new marker to aid in personal identification with low-biomass samples.
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1