微生物多样性在实验进化的合成群落中得以维持。

IF 5 2区 生物学 Q1 MICROBIOLOGY
mSystems Pub Date : 2024-10-15 DOI:10.1128/msystems.01053-24
Zahraa Al-Tameemi, Alejandra Rodríguez-Verdugo
{"title":"微生物多样性在实验进化的合成群落中得以维持。","authors":"Zahraa Al-Tameemi, Alejandra Rodríguez-Verdugo","doi":"10.1128/msystems.01053-24","DOIUrl":null,"url":null,"abstract":"<p><p>Microbial communities are incredibly diverse. Yet, the eco-evolutionary processes originating and maintaining this diversity remain understudied. Here, we investigate the patterns of diversification for <i>Pseudomonas putida</i> evolving in isolation and with <i>Acinetobacter johnsonii</i> leaking resources used by <i>P. putida</i>. We experimentally evolved four experimental replicates in monoculture and co-culture for 200 generations. We observed that <i>P. putida</i> diversified into two distinct morphotypes that differed from their ancestor by single-point mutations. One of the most prominent mutations hit the <i>fleQ</i> gene encoding the master regulator of flagella and biofilm formation. We experimentally confirmed that <i>fleQ</i> mutants were unable to swim and formed less biofilm than their ancestor, but they also produced higher yields. Interestingly, the <i>fleQ</i> genotype and other mutations swept to fixation in monocultures but not in co-cultures. In co-cultures, the two lineages stably coexisted for approximately 150 generations. We hypothesized that <i>A. johnsonii</i> modulates the coexistence of the two lineages through frequency-dependent selection. However, invasion experiments with two genotypes in monoculture and co-culture did not support this hypothesis. Finally, we conducted an evolutionary \"replay\" experiment to assess whether the presence or absence of <i>A. johnsonii</i> influenced the coexistence of morphotypes at the population level. Interestingly, <i>A. johnsonii</i> had a stabilizing effect on the co-culture. Overall, our study suggests that interspecies interactions play an important role in shaping patterns of diversification in microbial communities.</p><p><strong>Importance: </strong>In nature, bacteria live in microbial communities and interact with other species, for example, through the exchange of resources leaked into the external environment (i.e., cross-feeding interactions). The role that these cross-feeding interactions play in shaping patterns of diversification remains understudied. Using a simple bacterial system in which one species cross-feeds resources to a second species (commensal species), we showed that the commensal species diversified into two subpopulations that persisted only when the cross-feeder partner was present. We further observed loss-of-function mutations in flagellar genes that were fixed in monocultures but not in co-cultures. Our findings suggest that cross-feeding species influence patterns of diversification of other species. Given that nutrient leakage is pervasive in microbial communities, the findings from this study have the potential to extend beyond our specific bacterial system. Importantly, our study has contributed to answering the larger question of whether species evolved differently in isolation versus when interacting with other species.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":null,"pages":null},"PeriodicalIF":5.0000,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Microbial diversification is maintained in an experimentally evolved synthetic community.\",\"authors\":\"Zahraa Al-Tameemi, Alejandra Rodríguez-Verdugo\",\"doi\":\"10.1128/msystems.01053-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Microbial communities are incredibly diverse. Yet, the eco-evolutionary processes originating and maintaining this diversity remain understudied. Here, we investigate the patterns of diversification for <i>Pseudomonas putida</i> evolving in isolation and with <i>Acinetobacter johnsonii</i> leaking resources used by <i>P. putida</i>. We experimentally evolved four experimental replicates in monoculture and co-culture for 200 generations. We observed that <i>P. putida</i> diversified into two distinct morphotypes that differed from their ancestor by single-point mutations. One of the most prominent mutations hit the <i>fleQ</i> gene encoding the master regulator of flagella and biofilm formation. We experimentally confirmed that <i>fleQ</i> mutants were unable to swim and formed less biofilm than their ancestor, but they also produced higher yields. Interestingly, the <i>fleQ</i> genotype and other mutations swept to fixation in monocultures but not in co-cultures. In co-cultures, the two lineages stably coexisted for approximately 150 generations. We hypothesized that <i>A. johnsonii</i> modulates the coexistence of the two lineages through frequency-dependent selection. However, invasion experiments with two genotypes in monoculture and co-culture did not support this hypothesis. Finally, we conducted an evolutionary \\\"replay\\\" experiment to assess whether the presence or absence of <i>A. johnsonii</i> influenced the coexistence of morphotypes at the population level. Interestingly, <i>A. johnsonii</i> had a stabilizing effect on the co-culture. Overall, our study suggests that interspecies interactions play an important role in shaping patterns of diversification in microbial communities.</p><p><strong>Importance: </strong>In nature, bacteria live in microbial communities and interact with other species, for example, through the exchange of resources leaked into the external environment (i.e., cross-feeding interactions). The role that these cross-feeding interactions play in shaping patterns of diversification remains understudied. Using a simple bacterial system in which one species cross-feeds resources to a second species (commensal species), we showed that the commensal species diversified into two subpopulations that persisted only when the cross-feeder partner was present. We further observed loss-of-function mutations in flagellar genes that were fixed in monocultures but not in co-cultures. Our findings suggest that cross-feeding species influence patterns of diversification of other species. Given that nutrient leakage is pervasive in microbial communities, the findings from this study have the potential to extend beyond our specific bacterial system. Importantly, our study has contributed to answering the larger question of whether species evolved differently in isolation versus when interacting with other species.</p>\",\"PeriodicalId\":18819,\"journal\":{\"name\":\"mSystems\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":5.0000,\"publicationDate\":\"2024-10-15\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"mSystems\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/msystems.01053-24\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSystems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msystems.01053-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

微生物群落的多样性令人难以置信。然而,对产生和维持这种多样性的生态进化过程的研究仍然不足。在这里,我们研究了假单胞菌(Pseudomonas putida)单独进化和与约翰逊不动杆菌(Acinetobacter johnsonii)共同进化的多样化模式。我们在单培养和共培养中对四个实验重复体进行了 200 代的实验进化。我们观察到,普氏无针杆菌通过单点突变分化成两种不同的形态。其中一个最突出的突变涉及到编码鞭毛和生物膜形成主调控因子的 fleQ 基因。我们通过实验证实,fleQ 突变体无法游泳,形成的生物膜也比祖先少,但产量也更高。有趣的是,在单培养基中,fleQ 基因型和其他突变体都能横扫固定,但在共培养中却不能。在共培养物中,两个品系稳定共存了大约 150 代。我们假设约翰逊酵母菌通过频率选择调节了两个品系的共存。然而,在单培养和共培养中对两个基因型进行的入侵实验并不支持这一假设。最后,我们进行了一次进化 "重放 "实验,以评估约翰逊蛙的存在或不存在是否会在种群水平上影响形态的共存。有趣的是,A. johnsonii 对共生有稳定作用。总之,我们的研究表明,种间相互作用在塑造微生物群落的多样化模式方面发挥着重要作用:重要意义:在自然界中,细菌生活在微生物群落中,并与其他物种相互作用,例如,通过交换泄漏到外部环境中的资源(即交叉觅食相互作用)。这些交叉觅食相互作用在形成多样化模式方面所起的作用仍未得到充分研究。我们使用了一个简单的细菌系统,其中一个物种向第二个物种(共生物种)交叉馈送资源,结果表明,共生物种的多样化分为两个亚群,只有当交叉馈送伙伴存在时,这两个亚群才会持续存在。我们还观察到鞭毛基因的功能缺失突变,这些突变在单培养物中固定,而在共培养物中则不固定。我们的研究结果表明,异食物种会影响其他物种的多样化模式。鉴于营养物质泄漏在微生物群落中普遍存在,本研究的发现有可能超越我们特定的细菌系统。重要的是,我们的研究有助于回答一个更大的问题,即物种在与世隔绝的情况下与在与其他物种相互作用的情况下是否会有不同的进化。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Microbial diversification is maintained in an experimentally evolved synthetic community.

Microbial communities are incredibly diverse. Yet, the eco-evolutionary processes originating and maintaining this diversity remain understudied. Here, we investigate the patterns of diversification for Pseudomonas putida evolving in isolation and with Acinetobacter johnsonii leaking resources used by P. putida. We experimentally evolved four experimental replicates in monoculture and co-culture for 200 generations. We observed that P. putida diversified into two distinct morphotypes that differed from their ancestor by single-point mutations. One of the most prominent mutations hit the fleQ gene encoding the master regulator of flagella and biofilm formation. We experimentally confirmed that fleQ mutants were unable to swim and formed less biofilm than their ancestor, but they also produced higher yields. Interestingly, the fleQ genotype and other mutations swept to fixation in monocultures but not in co-cultures. In co-cultures, the two lineages stably coexisted for approximately 150 generations. We hypothesized that A. johnsonii modulates the coexistence of the two lineages through frequency-dependent selection. However, invasion experiments with two genotypes in monoculture and co-culture did not support this hypothesis. Finally, we conducted an evolutionary "replay" experiment to assess whether the presence or absence of A. johnsonii influenced the coexistence of morphotypes at the population level. Interestingly, A. johnsonii had a stabilizing effect on the co-culture. Overall, our study suggests that interspecies interactions play an important role in shaping patterns of diversification in microbial communities.

Importance: In nature, bacteria live in microbial communities and interact with other species, for example, through the exchange of resources leaked into the external environment (i.e., cross-feeding interactions). The role that these cross-feeding interactions play in shaping patterns of diversification remains understudied. Using a simple bacterial system in which one species cross-feeds resources to a second species (commensal species), we showed that the commensal species diversified into two subpopulations that persisted only when the cross-feeder partner was present. We further observed loss-of-function mutations in flagellar genes that were fixed in monocultures but not in co-cultures. Our findings suggest that cross-feeding species influence patterns of diversification of other species. Given that nutrient leakage is pervasive in microbial communities, the findings from this study have the potential to extend beyond our specific bacterial system. Importantly, our study has contributed to answering the larger question of whether species evolved differently in isolation versus when interacting with other species.

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
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.
×
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