ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae096
Nataliya Teteneva, Ananda Sanches-Medeiros, Victor Sourjik
{"title":"Genome-wide screen of genetic determinants that govern Escherichia coli growth and persistence in lake water.","authors":"Nataliya Teteneva, Ananda Sanches-Medeiros, Victor Sourjik","doi":"10.1093/ismejo/wrae096","DOIUrl":"10.1093/ismejo/wrae096","url":null,"abstract":"<p><p>Although enteric bacteria normally reside within the animal intestine, the ability to persist extraintestinally is an essential part of their overall lifestyle, and it might contribute to transmission between hosts. Despite this potential importance, few genetic determinants of extraintestinal growth and survival have been identified, even for the best-studied model, Escherichia coli. In this work, we thus used a genome-wide library of barcoded transposon insertions to systematically identify functional clusters of genes that are crucial for E. coli fitness in lake water. Our results revealed that inactivation of pathways involved in maintaining outer membrane integrity, nucleotide biosynthesis, and chemotaxis negatively affected E. coli growth or survival in this extraintestinal environment. In contrast, inactivation of another group of genes apparently benefited E. coli growth or persistence in filtered lake water, resulting in higher abundance of these mutants. This group included rpoS, which encodes the general stress response sigma factor, as well as genes encoding several other global transcriptional regulators and RNA chaperones, along with several poorly annotated genes. Based on this co-enrichment, we identified these gene products as novel positive regulators of RpoS activity. We further observed that, despite their enhanced growth, E. coli mutants with inactive RpoS had reduced viability in lake water, and they were not enriched in the presence of the autochthonous microbiota. This highlights the duality of the general stress response pathway for E. coli growth outside the host.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11188689/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141318821","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae126
Citlali Fonseca-García, Dean Pettinga, Andrew Wilson, Joshua R Elmore, Ryan McClure, Jackie Atim, Julie Pedraza, Robert Hutmacher, Halbay Turumtay, Yang Tian, Aymerick Eudes, Henrik V Scheller, Robert G Egbert, Devin Coleman-Derr
{"title":"Defined synthetic microbial communities colonize and benefit field-grown sorghum.","authors":"Citlali Fonseca-García, Dean Pettinga, Andrew Wilson, Joshua R Elmore, Ryan McClure, Jackie Atim, Julie Pedraza, Robert Hutmacher, Halbay Turumtay, Yang Tian, Aymerick Eudes, Henrik V Scheller, Robert G Egbert, Devin Coleman-Derr","doi":"10.1093/ismejo/wrae126","DOIUrl":"10.1093/ismejo/wrae126","url":null,"abstract":"<p><p>The rhizosphere constitutes a dynamic interface between plant hosts and their associated microbial communities. Despite the acknowledged potential for enhancing plant fitness by manipulating the rhizosphere, the engineering of the rhizosphere microbiome through inoculation has posed significant challenges. These challenges are thought to arise from the competitive microbial ecosystem where introduced microbes must survive, and the absence of adaptation to the specific metabolic and environmental demands of the rhizosphere. Here, we engineered a synthetic rhizosphere community (SRC1) with the anticipation that it would exhibit a selective advantage in colonizing the host Sorghum bicolor, thereby potentially fostering its growth. SRC1 was assembled from bacterial isolates identified either for their potential role in community cohesion through network analysis or for their ability to benefit from host-specific exudate compounds. The growth performance of SRC1 was assessed in vitro on solid media, in planta under gnotobiotic laboratory conditions, and in the field. Our findings reveal that SRC1 cohesion is most robust when cultivated in the presence of the plant host under laboratory conditions, with lineages being lost from the community when grown either in vitro or in a native field setting. We establish that SRC1 effectively promotes the growth of both above- and below-ground plant phenotypes in both laboratory and native field contexts. Furthermore, in laboratory conditions, these growth enhancements correlate with the transcriptional dampening of lignin biosynthesis in the host. Collectively, these results underscore the potential utility of synthetic microbial communities for modulating crop performance in controlled and native environments alike.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11410050/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565019","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae127
Zhe Pan, Yanhong Chen, Mi Zhou, Tim A McAllister, Tom N Mcneilly, Le Luo Guan
{"title":"Linking active rectal mucosa-attached microbiota to host immunity reveals its role in host-pathogenic STEC O157 interactions.","authors":"Zhe Pan, Yanhong Chen, Mi Zhou, Tim A McAllister, Tom N Mcneilly, Le Luo Guan","doi":"10.1093/ismejo/wrae127","DOIUrl":"10.1093/ismejo/wrae127","url":null,"abstract":"<p><p>The rectal-anal junction (RAJ) is the major colonization site of Shiga toxin-producing Escherichia coli (STEC) O157 in beef cattle, leading to transmission of this foodborne pathogen from farms to food chains. To date, there is limited understanding regarding whether the mucosa-attached microbiome has a profound impact on host-STEC interactions. In this study, the active RAJ mucosa-attached microbiota and its potential role in host immunity-STEC commensal interactions were investigated using RAJ mucosal biopsies collected from calves orally challenged with two STEC O157 strains with or without functional stx2a (stx2a+ or stx2a-). The results revealed that shifts of microbial diversity, topology, and assembly patterns were subjected to stx2a production post-challenge and Paeniclostridium and Gallibacterium were the keystone taxa for both microbial interactions and assembly. Additional mucosal transcriptome profiling showed stx2a-dependent host immune responses (i.e. B- and T-cell signaling and antigen processing and presentation) post-challenge. Further integrated analysis revealed that mucosa-attached beneficial microbes (i.e. Provotella, Faecalibacterium, and Dorea) interacted with host immune genes pre-challenge to maintain host homeostasis; however, opportunistic pathogenic microbes (i.e. Paeniclostridium) could interact with host immune genes after the STEC O157 colonization and interactions were stx2a-dependent. Furthermore, predicted bacterial functions involved in pathogen (O157 and Paeniclostridium) colonization and metabolism were related to host immunity. These findings suggest that during pathogen colonization, host-microbe interactions could shift from beneficial to opportunistic pathogenic bacteria driven and be dependent on the production of particular virulence factors, highlighting the potential regulatory role of mucosa-attached microbiota in affecting pathogen-commensal host interactions in calves with STEC O157 infection.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11304501/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141565021","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Anaerobic ammonium oxidation coupled to iron(III) reduction catalyzed by a lithoautotrophic nitrate-reducing iron(II) oxidizing enrichment culture.","authors":"Hong-Bin Zhang, He-Fei Wang, Jia-Bo Liu, Zhen Bi, Ruo-Fei Jin, Tian Tian","doi":"10.1093/ismejo/wrae149","DOIUrl":"10.1093/ismejo/wrae149","url":null,"abstract":"<p><p>The last two decades have seen nitrogen/iron-transforming bacteria at the forefront of new biogeochemical discoveries, such as anaerobic ammonium oxidation coupled to ferric iron reduction (feammox) and lithoautotrophic nitrate-reducing ferrous iron-oxidation (NRFeOx). These emerging findings continue to expand our knowledge of the nitrogen/iron cycle in nature and also highlight the need to re-understand the functional traits of the microorganisms involved. Here, as a proof-of-principle, we report compelling evidence for the capability of an NRFeOx enrichment culture to catalyze the feammox process. Our results demonstrate that the NRFeOx culture predominantly oxidizes NH4+ to nitrogen gas, by reducing both chelated nitrilotriacetic acid (NTA)-Fe(III) and poorly soluble Fe(III)-bearing minerals (γ-FeOOH) at pH 4.0 and 8.0, respectively. In the NRFeOx culture, Fe(II)-oxidizing bacteria of Rhodanobacter and Fe(III)-reducing bacteria of unclassified_Acidobacteriota coexisted. Their relative abundances were dynamically regulated by the supplemented iron sources. Metagenomic analysis revealed that the NRFeOx culture contained a complete set of denitrifying genes along with hao genes for ammonium oxidation. Additionally, numerous genes encoding extracellular electron transport-associated proteins or their homologs were identified, which facilitated the reduction of extracellular iron by this culture. More broadly, this work lightens the unexplored potential of specific microbial groups in driving nitrogen transformation through multiple pathways and highlights the essential role of microbial iron metabolism in the integral biogeochemical nitrogen cycle.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11366258/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141856963","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae158
Elizabeth Connors, Avishek Dutta, Rebecca Trinh, Natalia Erazo, Srishti Dasarathy, Hugh Ducklow, J L Weissman, Yi-Chun Yeh, Oscar Schofield, Deborah Steinberg, Jed Fuhrman, Jeff S Bowman
{"title":"Microbial community composition predicts bacterial production across ocean ecosystems.","authors":"Elizabeth Connors, Avishek Dutta, Rebecca Trinh, Natalia Erazo, Srishti Dasarathy, Hugh Ducklow, J L Weissman, Yi-Chun Yeh, Oscar Schofield, Deborah Steinberg, Jed Fuhrman, Jeff S Bowman","doi":"10.1093/ismejo/wrae158","DOIUrl":"10.1093/ismejo/wrae158","url":null,"abstract":"<p><p>Microbial ecological functions are an emergent property of community composition. For some ecological functions, this link is strong enough that community composition can be used to estimate the quantity of an ecological function. Here, we apply random forest regression models to compare the predictive performance of community composition and environmental data for bacterial production (BP). Using data from two independent long-term ecological research sites-Palmer LTER in Antarctica and Station SPOT in California-we found that community composition was a strong predictor of BP. The top performing model achieved an R2 of 0.84 and RMSE of 20.2 pmol L-1 hr-1 on independent validation data, outperforming a model based solely on environmental data (R2 = 0.32, RMSE = 51.4 pmol L-1 hr-1). We then operationalized our top performing model, estimating BP for 346 Antarctic samples from 2015 to 2020 for which only community composition data were available. Our predictions resolved spatial trends in BP with significance in the Antarctic (P value = 1 × 10-4) and highlighted important taxa for BP across ocean basins. Our results demonstrate a strong link between microbial community composition and microbial ecosystem function and begin to leverage long-term datasets to construct models of BP based on microbial community composition.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11385589/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141894774","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae153
Su Ding, F A Bastiaan von Meijenfeldt, Nicole J Bale, Jaap S Sinninghe Damsté, Laura Villanueva
{"title":"Production of structurally diverse sphingolipids by anaerobic marine bacteria in the euxinic Black Sea water column.","authors":"Su Ding, F A Bastiaan von Meijenfeldt, Nicole J Bale, Jaap S Sinninghe Damsté, Laura Villanueva","doi":"10.1093/ismejo/wrae153","DOIUrl":"10.1093/ismejo/wrae153","url":null,"abstract":"<p><p>Microbial lipids, used as taxonomic markers and physiological indicators, have mainly been studied through cultivation. However, this approach is limited due to the scarcity of cultures of environmental microbes, thereby restricting insights into the diversity of lipids and their ecological roles. Addressing this limitation, here we apply metalipidomics combined with metagenomics in the Black Sea, classifying and tentatively identifying 1623 lipid-like species across 18 lipid classes. We discovered over 200 novel, abundant, and structurally diverse sphingolipids in euxinic waters, including unique 1-deoxysphingolipids with long-chain fatty acids and sulfur-containing groups. Sphingolipids were thought to be rare in bacteria and their molecular and ecological functions in bacterial membranes remain elusive. However, genomic analysis focused on sphingolipid biosynthesis genes revealed that members of 38 bacterial phyla in the Black Sea can synthesize sphingolipids, representing a 4-fold increase from previously known capabilities and accounting for up to 25% of the microbial community. These sphingolipids appear to be involved in oxidative stress response, cell wall remodeling, and are associated with the metabolism of nitrogen-containing molecules. Our findings underscore the effectiveness of multi-omics approaches in exploring microbial chemical ecology.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11334938/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141903450","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae164
Daniel Méndez-Sánchez, Anna Schrecengost, Johana Rotterová, Kateřina Koštířová, Roxanne A Beinart, Ivan Čepička
{"title":"Methanogenic symbionts of anaerobic ciliates are host and habitat specific.","authors":"Daniel Méndez-Sánchez, Anna Schrecengost, Johana Rotterová, Kateřina Koštířová, Roxanne A Beinart, Ivan Čepička","doi":"10.1093/ismejo/wrae164","DOIUrl":"10.1093/ismejo/wrae164","url":null,"abstract":"<p><p>The association between anaerobic ciliates and methanogenic archaea has been recognized for over a century. Nevertheless, knowledge of these associations is limited to a few ciliate species, and so the identification of patterns of host-symbiont specificity has been largely speculative. In this study, we integrated microscopy and genetic identification to survey the methanogenic symbionts of 32 free-living anaerobic ciliate species, mainly from the order Metopida. Based on Sanger and Illumina sequencing of the 16S rRNA gene, our results show that a single methanogenic symbiont population, belonging to Methanobacterium, Methanoregula, or Methanocorpusculum, is dominant in each host strain. Moreover, the host's taxonomy (genus and above) and environment (i.e. endobiotic, marine/brackish, or freshwater) are linked with the methanogen identity at the genus level, demonstrating a strong specificity and fidelity in the association. We also established cultures containing artificially co-occurring anaerobic ciliate species harboring different methanogenic symbionts. This revealed that the host-methanogen relationship is stable over short timescales in cultures without evidence of methanogenic symbiont exchanges, although our intraspecific survey indicated that metopids also tend to replace their methanogens over longer evolutionary timescales. Therefore, anaerobic ciliates have adapted a mixed transmission mode to maintain and replace their methanogenic symbionts, allowing them to thrive in oxygen-depleted environments.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11378729/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142009830","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae219
Raquel Peixoto, Christian R Voolstra, Lisa Y Stein, Philip Hugenholtz, Joana Falcao Salles, Shady A Amin, Max Häggblom, Ann Gregory, Thulani P Makhalanyane, Fengping Wang, Nadège Adoukè Agbodjato, Yinzhao Wang, Nianzhi Jiao, Jay T Lennon, Antonio Ventosa, Patrik M Bavoil, Virginia Miller, Jack A Gilbert
{"title":"Microbial solutions must be deployed against climate catastrophe.","authors":"Raquel Peixoto, Christian R Voolstra, Lisa Y Stein, Philip Hugenholtz, Joana Falcao Salles, Shady A Amin, Max Häggblom, Ann Gregory, Thulani P Makhalanyane, Fengping Wang, Nadège Adoukè Agbodjato, Yinzhao Wang, Nianzhi Jiao, Jay T Lennon, Antonio Ventosa, Patrik M Bavoil, Virginia Miller, Jack A Gilbert","doi":"10.1093/ismejo/wrae219","DOIUrl":"10.1093/ismejo/wrae219","url":null,"abstract":"","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":"18 1","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11552515/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142631859","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae090
Gao Chen, Yi Yang, Jun Yan, Frank E Löffler
{"title":"Metabolite cross-feeding enables concomitant catabolism of chlorinated methanes and chlorinated ethenes in synthetic microbial assemblies.","authors":"Gao Chen, Yi Yang, Jun Yan, Frank E Löffler","doi":"10.1093/ismejo/wrae090","DOIUrl":"10.1093/ismejo/wrae090","url":null,"abstract":"<p><p>Isolate studies have been a cornerstone for unraveling metabolic pathways and phenotypical (functional) features. Biogeochemical processes in natural and engineered ecosystems are generally performed by more than a single microbe and often rely on mutualistic interactions. We demonstrate the rational bottom-up design of synthetic, interdependent co-cultures to achieve concomitant utilization of chlorinated methanes as electron donors and organohalogens as electron acceptors. Specialized anaerobes conserve energy from the catabolic conversion of chloromethane or dichloromethane to formate, H2, and acetate, compounds that the organohalide-respiring bacterium Dehalogenimonas etheniformans strain GP requires to utilize cis-1,2-dichloroethenene and vinyl chloride as electron acceptors. Organism-specific qPCR enumeration matched the growth of individual dechlorinators to the respective functional (i.e. dechlorination) traits. The metabolite cross-feeding in the synthetic (co-)cultures enables concomitant utilization of chlorinated methanes (i.e. chloromethane and dichloromethane) and chlorinated ethenes (i.e. cis-1,2-dichloroethenene and vinyl chloride) without the addition of an external electron donor (i.e. formate and H2). The findings illustrate that naturally occurring chlorinated C1 compounds can sustain anaerobic food webs, an observation with implications for the development of interdependent, mutualistic communities, the sustenance of microbial life in oligotrophic and energy-deprived environments, and the fate of chloromethane/dichloromethane and chlorinated electron acceptors (e.g. chlorinated ethenes) in pristine environments and commingled contaminant plumes.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11170663/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141181371","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Role of Type VI secretion system in pathogenic remodeling of host gut microbiota during Aeromonas veronii infection.","authors":"Xiaoli Jiang, Hanzeng Li, Jiayue Ma, Hong Li, Xiang Ma, Yanqiong Tang, Juanjuan Li, Xue Chi, Yong Deng, Sheng Zeng, Zhu Liu","doi":"10.1093/ismejo/wrae053","DOIUrl":"10.1093/ismejo/wrae053","url":null,"abstract":"<p><p>Intestinal microbial disturbance is a direct cause of host disease. The bacterial Type VI secretion system (T6SS) often plays a crucial role in the fitness of pathogenic bacteria by delivering toxic effectors into target cells. However, its impact on the gut microbiota and host pathogenesis is poorly understood. To address this question, we characterized a new T6SS in the pathogenic Aeromonas veronii C4. First, we validated the secretion function of the core machinery of A. veronii C4 T6SS. Second, we found that the pathogenesis and colonization of A. veronii C4 is largely dependent on its T6SS. The effector secretion activity of A. veronii C4 T6SS not only provides an advantage in competition among bacteria in vitro, but also contributes to occupation of an ecological niche in the nutritionally deficient and anaerobic environment of the host intestine. Metagenomic analysis showed that the T6SS directly inhibits or eliminates symbiotic strains from the intestine, resulting in dysregulated gut microbiome homeostasis. In addition, we identified three unknown effectors, Tse1, Tse2, and Tse3, in the T6SS, which contribute to T6SS-mediated bacterial competition and pathogenesis by impairing targeted cell integrity. Our findings highlight that T6SS can remodel the host gut microbiota by intricate interplay between T6SS-mediated bacterial competition and altered host immune responses, which synergistically promote pathogenesis of A. veronii C4. Therefore, this newly characterized T6SS could represent a general interaction mechanism between the host and pathogen, and may offer a potential therapeutic target for controlling bacterial pathogens.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11014884/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140295078","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}