Pub Date : 2026-01-16DOI: 10.1128/msystems.01605-25
Delaney G Beals, Dana L Carper, Leah H Hochanadel, Sara S Jawdy, Dawn M Klingeman, Bryan T Piatkowski, David J Weston, Mitchel J Doktycz, Dale A Pelletier
Microbial colonization of plant roots involves strong selective pressures that shape the structure and function of root-associated communities. In particular, the endosphere represents a highly selective environment requiring host entry and in planta persistence. However, strain-specific microbial traits that enable endosphere colonization remain poorly understood. Here, we use a defined, genome-resolved community of 28 Variovorax strains isolated from the roots of Populus deltoides and Populus trichocarpa (poplar trees) to determine which strains partition between rhizosphere and endosphere compartments and to identify the genomic traits associated with endosphere specialization. By combining strain-resolved metagenomic profiling, comparative genomics, and functional assays, we demonstrate that dominant endosphere colonizers are enriched in genes related to nutrient metabolism, redox balance, transcriptional regulation, and a conserved L-fucose utilization pathway experimentally shown to enhance root colonization. Not all strains succeed through the same strategy. Community-wide functional profiling revealed a distinct and reduced set of traits in the endosphere, including orthogroups associated with low-abundance strains that were overlooked in strain-level analyses. These findings reveal that multiple ecological strategies, such as metabolic competition, regulatory adaptation, and niche specialization, can support endosphere colonization. Our results advance the understanding of how bacterial colonization traits are distributed and deployed within a plant microbiome and suggest that host filtering selects for distinct, and sometimes complementary, microbial strategies. This work supports a shift toward mechanistic, genome-resolved models of microbiome assembly and offers a framework for linking microbial function to host colonization success.IMPORTANCEPlants often depend on diverse microbial partners to support their growth, resilience, and adaptation to changing environments. Among these microbes, some bacteria inhabit the rhizosphere (the narrow zone around roots where microbes interact with the plant) while others are able to enter and persist within root tissues. The traits that distinguish these two lifestyles remain poorly understood. In this study, we examined a group of related Variovorax strains from poplar tree root microbiomes to ask why some rhizosphere-associated strains also become successful endosphere colonizers. We found that strains appear to succeed through different strategies: some may benefit from rapid growth on plant-derived carbon sources, while others may rely on stress tolerance or fine-tuned regulation. These results suggest that there is no single path from the rhizosphere into the root interior, but rather multiple strategies shaped by the host environment. Understanding this diversity can inform efforts to design resilient plant-microbe communities.
{"title":"Genomic signatures in <i>Variovorax</i> enabling colonization of the <i>Populus</i> endosphere.","authors":"Delaney G Beals, Dana L Carper, Leah H Hochanadel, Sara S Jawdy, Dawn M Klingeman, Bryan T Piatkowski, David J Weston, Mitchel J Doktycz, Dale A Pelletier","doi":"10.1128/msystems.01605-25","DOIUrl":"https://doi.org/10.1128/msystems.01605-25","url":null,"abstract":"<p><p>Microbial colonization of plant roots involves strong selective pressures that shape the structure and function of root-associated communities. In particular, the endosphere represents a highly selective environment requiring host entry and <i>in planta</i> persistence. However, strain-specific microbial traits that enable endosphere colonization remain poorly understood. Here, we use a defined, genome-resolved community of 28 <i>Variovorax</i> strains isolated from the roots of <i>Populus deltoides</i> and <i>Populus trichocarpa</i> (poplar trees) to determine which strains partition between rhizosphere and endosphere compartments and to identify the genomic traits associated with endosphere specialization. By combining strain-resolved metagenomic profiling, comparative genomics, and functional assays, we demonstrate that dominant endosphere colonizers are enriched in genes related to nutrient metabolism, redox balance, transcriptional regulation, and a conserved L-fucose utilization pathway experimentally shown to enhance root colonization. Not all strains succeed through the same strategy. Community-wide functional profiling revealed a distinct and reduced set of traits in the endosphere, including orthogroups associated with low-abundance strains that were overlooked in strain-level analyses. These findings reveal that multiple ecological strategies, such as metabolic competition, regulatory adaptation, and niche specialization, can support endosphere colonization. Our results advance the understanding of how bacterial colonization traits are distributed and deployed within a plant microbiome and suggest that host filtering selects for distinct, and sometimes complementary, microbial strategies. This work supports a shift toward mechanistic, genome-resolved models of microbiome assembly and offers a framework for linking microbial function to host colonization success.IMPORTANCEPlants often depend on diverse microbial partners to support their growth, resilience, and adaptation to changing environments. Among these microbes, some bacteria inhabit the rhizosphere (the narrow zone around roots where microbes interact with the plant) while others are able to enter and persist within root tissues. The traits that distinguish these two lifestyles remain poorly understood. In this study, we examined a group of related <i>Variovorax</i> strains from poplar tree root microbiomes to ask why some rhizosphere-associated strains also become successful endosphere colonizers. We found that strains appear to succeed through different strategies: some may benefit from rapid growth on plant-derived carbon sources, while others may rely on stress tolerance or fine-tuned regulation. These results suggest that there is no single path from the rhizosphere into the root interior, but rather multiple strategies shaped by the host environment. Understanding this diversity can inform efforts to design resilient plant-microbe communities.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0160525"},"PeriodicalIF":4.6,"publicationDate":"2026-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145989895","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-16DOI: 10.1128/msystems.00801-25
Rebecca S Key, Sacha N Coesel, Mary R Gradoville, Rhonda L Morales, Hanna Farnelid, Jonathan P Zehr, E Virginia Armbrust, Bryndan P Durham
Marine phytoplankton are central to global seascapes, acting as key conduits in element cycling and oceanic food webs. Phytoplankton cell size spans several orders of magnitude (0.2 to >200 µm) and is an important trait that governs metabolism. However, the vast taxonomic diversity within phytoplankton size classes makes it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. To explore phytoplankton biogeography and biogeochemical roles in field populations, we analyzed 3 years of 16S and 18S rRNA gene amplicon sequencing variant (ASV) data alongside biochemical measurements across the dynamic latitudinal gradient of the North Pacific Transition Zone. We identified picophytoplankton community members associated with patterns in net community production (NCP), particulate organic carbon (POC), and particulate organic nitrogen (PON) and uncovered co-occurring species that may influence their growth and abundance. Multivariate linear mixed modeling revealed that the occurrence of chlorophytes explained 22.6% of NCP values, followed by stramenopiles and cyanobacteria. In contrast, POC and PON spatial patterns were best explained by chlorophyte and dinoflagellate spatial patterns. Weighted co-expression network analysis further showed NCP, POC, and PON correlations with a subset of ~40 ASVs belonging to chlorophytes, cyanobacteria, stramenopiles, haptophytes, and dinoflagellates that range in trophic strategy. Association network inference recapitulated these findings and revealed additional co-occurring phytoplankton, grazers, and heterotrophic bacteria. Together, our integrated computational analyses identified key picophytoplankton and co-occurring mixotrophs as major contributors to shaping regional biogeochemical dynamics in the North Pacific Ocean.IMPORTANCEPhytoplankton mediate key biogeochemical processes in dynamic oceanic transition zones. However, their vast cell size range and taxonomic diversity make it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. By integrating molecular and biogeochemical measurements from the North Pacific Transition Zone using combined network and multivariate modeling, we identified specific picophytoplankton strongly linked to community production and organic nutrients levels. These picophytoplankton included specific members of cyanobacteria, pelagophytes, haptophytes, and chlorophytes and formed tight associations with several nano- and pico-sized protistan mixotrophs, highlighting how top-down interactions and microbial consortia shape community structure and elemental fluxes. Our work establishes key microbial players that may control fundamental ecosystem processes like carbon and nitrogen cycling and offers a computational framework to track and identify "microbial neighborhoods" that underpin biogeochemical features of an ecosystem.
{"title":"Picophytoplankton implicated in productivity and biogeochemistry in the North Pacific Transition Zone.","authors":"Rebecca S Key, Sacha N Coesel, Mary R Gradoville, Rhonda L Morales, Hanna Farnelid, Jonathan P Zehr, E Virginia Armbrust, Bryndan P Durham","doi":"10.1128/msystems.00801-25","DOIUrl":"https://doi.org/10.1128/msystems.00801-25","url":null,"abstract":"<p><p>Marine phytoplankton are central to global seascapes, acting as key conduits in element cycling and oceanic food webs. Phytoplankton cell size spans several orders of magnitude (0.2 to >200 µm) and is an important trait that governs metabolism. However, the vast taxonomic diversity within phytoplankton size classes makes it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. To explore phytoplankton biogeography and biogeochemical roles in field populations, we analyzed 3 years of 16S and 18S rRNA gene amplicon sequencing variant (ASV) data alongside biochemical measurements across the dynamic latitudinal gradient of the North Pacific Transition Zone. We identified picophytoplankton community members associated with patterns in net community production (NCP), particulate organic carbon (POC), and particulate organic nitrogen (PON) and uncovered co-occurring species that may influence their growth and abundance. Multivariate linear mixed modeling revealed that the occurrence of chlorophytes explained 22.6% of NCP values, followed by stramenopiles and cyanobacteria. In contrast, POC and PON spatial patterns were best explained by chlorophyte and dinoflagellate spatial patterns. Weighted co-expression network analysis further showed NCP, POC, and PON correlations with a subset of ~40 ASVs belonging to chlorophytes, cyanobacteria, stramenopiles, haptophytes, and dinoflagellates that range in trophic strategy. Association network inference recapitulated these findings and revealed additional co-occurring phytoplankton, grazers, and heterotrophic bacteria. Together, our integrated computational analyses identified key picophytoplankton and co-occurring mixotrophs as major contributors to shaping regional biogeochemical dynamics in the North Pacific Ocean.IMPORTANCEPhytoplankton mediate key biogeochemical processes in dynamic oceanic transition zones. However, their vast cell size range and taxonomic diversity make it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. By integrating molecular and biogeochemical measurements from the North Pacific Transition Zone using combined network and multivariate modeling, we identified specific picophytoplankton strongly linked to community production and organic nutrients levels. These picophytoplankton included specific members of cyanobacteria, pelagophytes, haptophytes, and chlorophytes and formed tight associations with several nano- and pico-sized protistan mixotrophs, highlighting how top-down interactions and microbial consortia shape community structure and elemental fluxes. Our work establishes key microbial players that may control fundamental ecosystem processes like carbon and nitrogen cycling and offers a computational framework to track and identify \"microbial neighborhoods\" that underpin biogeochemical features of an ecosystem.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0080125"},"PeriodicalIF":4.6,"publicationDate":"2026-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145989829","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-15DOI: 10.1128/msystems.01435-25
Yuhao Li, Daniel J Stieh, Lindsay Droit, Andrew HyoungJin Kim, Rachel Rodgers, Kathie A Mihindukulasuriya, Leran Wang, Maria G Pau, Olive Yuan, Herbert W Virgin, Dan H Barouch, Megan T Baldridge, Scott A Handley
Optimization of prophylactic vaccine regimens to elicit strong, long-lasting immunity is an urgent need highlighted by the COVID-19 pandemic. Stronger vaccine immunogenicity is frequently reported in individuals living in high-income countries compared to individuals living in low- and middle-income countries. While numerous host genetic and immune factors may influence vaccine responses, geographic restrictions to vaccine effectiveness may also be influenced by the intestinal microbiota, which modulates host immune systems. However, the potential role of the gut microbiota on responses to HIV-1 vaccines has not yet been explored. We analyzed the bacteriome by targeted 16S sequencing and the virome by virus-like particle sequencing of 154 fecal samples collected from healthy individuals in Uganda, Rwanda, and the United States early (week 2) and late (week 26) after vaccination with multivalent adenovirus serotype 26 (Ad26)-vectored mosaic HIV-1 vaccines. Vaccination did not affect the enteric bacteriome or virome regardless of geographic location. However, geography was the major driver of microbiota differences within this cohort. Differences in overall bacterial and viral diversity and in specific microbial taxa, including Bacteroidota and Bacillota, between participants from the United States and East African countries correlated with differential immune responses, including specific antibody titers, antibody functionality, and cellular immune responses to vaccination regimens. These findings support the microbiota as a putative modifier of vaccine immunogenicity.IMPORTANCEOur research examined how gut bacteria might influence vaccine effectiveness in different parts of the world. We studied adults from the United States, Rwanda, and Uganda who received an experimental HIV vaccine. We found that participants from East Africa had more diverse gut bacteria than those from the United States, but their immune responses to the vaccine were weaker. This is the first study to directly show this relationship between higher gut bacterial diversity and reduced vaccine effectiveness in the same group of people. We also identified specific types of bacteria that were linked to either stronger or weaker immune responses. These findings are particularly relevant now as we use vaccines globally to fight diseases like COVID-19, as they suggest that regional differences in gut bacteria Bacteroidota and Bacillota might help explain why vaccines work better in some places than others. This could inform how we design and test future vaccines.
{"title":"Associations between the microbiome and immune responses to an adenovirus-based HIV-1 candidate vaccine are distinct between African and US cohorts.","authors":"Yuhao Li, Daniel J Stieh, Lindsay Droit, Andrew HyoungJin Kim, Rachel Rodgers, Kathie A Mihindukulasuriya, Leran Wang, Maria G Pau, Olive Yuan, Herbert W Virgin, Dan H Barouch, Megan T Baldridge, Scott A Handley","doi":"10.1128/msystems.01435-25","DOIUrl":"https://doi.org/10.1128/msystems.01435-25","url":null,"abstract":"<p><p>Optimization of prophylactic vaccine regimens to elicit strong, long-lasting immunity is an urgent need highlighted by the COVID-19 pandemic. Stronger vaccine immunogenicity is frequently reported in individuals living in high-income countries compared to individuals living in low- and middle-income countries. While numerous host genetic and immune factors may influence vaccine responses, geographic restrictions to vaccine effectiveness may also be influenced by the intestinal microbiota, which modulates host immune systems. However, the potential role of the gut microbiota on responses to HIV-1 vaccines has not yet been explored. We analyzed the bacteriome by targeted 16S sequencing and the virome by virus-like particle sequencing of 154 fecal samples collected from healthy individuals in Uganda, Rwanda, and the United States early (week 2) and late (week 26) after vaccination with multivalent adenovirus serotype 26 (Ad26)-vectored mosaic HIV-1 vaccines. Vaccination did not affect the enteric bacteriome or virome regardless of geographic location. However, geography was the major driver of microbiota differences within this cohort. Differences in overall bacterial and viral diversity and in specific microbial taxa, including <i>Bacteroidota</i> and <i>Bacillota</i>, between participants from the United States and East African countries correlated with differential immune responses, including specific antibody titers, antibody functionality, and cellular immune responses to vaccination regimens. These findings support the microbiota as a putative modifier of vaccine immunogenicity.IMPORTANCEOur research examined how gut bacteria might influence vaccine effectiveness in different parts of the world. We studied adults from the United States, Rwanda, and Uganda who received an experimental HIV vaccine. We found that participants from East Africa had more diverse gut bacteria than those from the United States, but their immune responses to the vaccine were weaker. This is the first study to directly show this relationship between higher gut bacterial diversity and reduced vaccine effectiveness in the same group of people. We also identified specific types of bacteria that were linked to either stronger or weaker immune responses. These findings are particularly relevant now as we use vaccines globally to fight diseases like COVID-19, as they suggest that regional differences in gut bacteria <i>Bacteroidota</i> and <i>Bacillota</i> might help explain why vaccines work better in some places than others. This could inform how we design and test future vaccines.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0143525"},"PeriodicalIF":4.6,"publicationDate":"2026-01-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145985048","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-12DOI: 10.1128/msystems.01591-25
Emily E Benedict, Wesley Agee, Tiffany Hink, Katelyn L Parrish, Kimberly A Reske, Kate Peacock, Rachel E Bosserman, Alyssa Valencia, Akshay Saluja, Elianora Ovchiyan, Olivia Arter, Kevin Jolani, Erik R Dubberke, Gautam Dantas, Jennie H Kwon
<p><p><i>Escherichia coli</i> is a public health threat capable of causing multiple types of infection, carrying a variety of antimicrobial resistance genes (ARGs), and disseminating ARGs to other microbes. Since ARG-carrying <i>E. coli</i> can exist as a commensal gut microbe, intestinal <i>E. coli</i> in community-associated (CA) members presents an under-appreciated reservoir of ARGs. We cultured 75 CA <i>E. coli</i> isolates from stool of 64 patients lacking inpatient healthcare exposures >24 hours in the previous 12 weeks. Remnant stool submitted to the Barnes-Jewish Hospital (BJH) microbiology laboratory for <i>Clostridioides difficile</i> testing was plated to MacConkey agar with ciprofloxacin and extended-spectrum beta-lactamase (ESBL) Chrome Agar to isolate resistant <i>E. coli</i> colonies, which were whole-genome sequenced. Isolates were compared to ESBL <i>E. coli</i> genomes published by Mahmud et al. (B. Mahmud, M. A. Wallace, K. A. Reske, K. Alvarado, et al., mSystems 7:e00519-22, 2022, https://doi.org/10.1128/msystems.00519-22), which were collected from bloodstream and urinary tract infections. We identified ESBL genes and quinolone resistance elements in <i>E. coli</i> isolates from all patients, 32 (50%) of whom had no recent antibiotic exposure. Sequence type (ST) 131 isolates carried more quinolone resistance elements but fewer ESBL genes than other STs. Eleven patients carried two distinct <i>E. coli</i> lineages simultaneously. CA ESBL <i>E. coli</i> displayed a lower diversity of beta-lactamase genes but similar rates of antibiotic resistance genes compared to ESBL <i>E. coli</i> reported by Mahmud et al. (https://doi.org/10.1128/msystems.00519-22). Carriage of resistance elements without recent antimicrobial exposure suggests the presence of circulating, resistant <i>E. coli</i>. Our results show the continually evolving resistance profile of CA <i>E. coli</i>, demonstrating the importance of characterizing antimicrobial resistance in the community.IMPORTANCEAntimicrobial-resistant <i>Escherichia coli</i> presents a substantial threat to public health, limiting treatment options and potentially horizontally transferring its resistance to other members of the gut microbiome. Resistance to quinolones and beta-lactams, specifically, hinders treatment of urinary tract and gastrointestinal infections, both commonly caused by <i>E. coli</i>. Tracking successful lineages, such as ST131, within the healthcare setting can inform clinicians about resistance patterns among their patients, but this work shows that other STs present an even higher antimicrobial resistance burden than ST131. In addition to monitoring multiple lineages of antimicrobial-resistant <i>E. coli</i>, it is necessary to identify and understand community-associated carriage of this organism, as evidenced by the increasing prevalence of community-associated ESBL <i>E. coli</i> carriage and our specific results showing similar resistance burdens within the clinic
大肠杆菌是一种公共卫生威胁,能够引起多种类型的感染,携带多种抗微生物药物耐药性基因(ARGs),并将ARGs传播给其他微生物。由于携带arg的大肠杆菌可以作为一种共生肠道微生物存在,因此社区相关(CA)成员的肠道大肠杆菌是一个未被充分认识的arg储存库。我们从64例患者的粪便中培养了75株CA E.大肠杆菌,这些患者在过去12周内没有住院医疗保健暴露。将送到美国巴尼斯犹太医院(BJH)微生物实验室进行艰难梭菌检测的残余粪便,用环丙沙星和广谱β -内酰胺酶(ESBL)铬琼脂镀于MacConkey琼脂上,分离耐药大肠杆菌菌落,并对其进行全基因组测序。将分离株与Mahmud等人发表的ESBL大肠杆菌基因组进行比较(B. Mahmud, M. A. Wallace, K. A. Reske, K. Alvarado等,mSystems 7:e00519- 22,2022, https://doi.org/10.1128/msystems.00519-22),这些基因组收集自血液和尿路感染。我们在所有患者的大肠杆菌分离株中发现了ESBL基因和喹诺酮类药物耐药元素,其中32例(50%)近期没有抗生素暴露。序列型(ST 131)分离株携带的喹诺酮类耐药因子较多,而ESBL基因较少。11名患者同时携带两种不同的大肠杆菌谱系。与Mahmud等人报道的ESBL大肠杆菌相比,CA ESBL大肠杆菌显示出较低的β -内酰胺酶基因多样性,但抗生素耐药基因的比例相似(https://doi.org/10.1128/msystems.00519-22)。携带没有最近接触过抗菌素的耐药因子表明存在循环的耐药大肠杆菌。我们的研究结果显示了CA E. coli的持续进化的耐药谱,证明了在社区中表征抗菌素耐药性的重要性。耐药大肠杆菌对公共卫生构成重大威胁,限制了治疗选择,并可能将其耐药性横向转移到肠道微生物组的其他成员。特别是对喹诺酮类药物和β -内酰胺类药物的耐药性,阻碍了泌尿道和胃肠道感染的治疗,这两种感染通常都是由大肠杆菌引起的。在医疗保健环境中跟踪成功的ST131谱系可以告知临床医生其患者的耐药模式,但这项工作表明,其他STs比ST131表现出更高的抗微生物药物耐药性负担。除了监测耐药大肠杆菌的多个谱系外,有必要确定和了解这种有机体的社区相关携带,社区相关ESBL大肠杆菌携带的流行率日益增加,我们的具体结果表明,在诊所和社区中存在类似的耐药负担。这项工作提供了对那些没有大量医疗保健暴露的人的抗菌素耐药大肠杆菌的见解,提供了目前缺乏的以社区为重点的重要监测。
{"title":"Community-associated quinolone-resistant and extended-spectrum beta-lactamase-producing <i>Escherichia coli</i> isolates are similar to clinical infection isolates by sequence type and resistome.","authors":"Emily E Benedict, Wesley Agee, Tiffany Hink, Katelyn L Parrish, Kimberly A Reske, Kate Peacock, Rachel E Bosserman, Alyssa Valencia, Akshay Saluja, Elianora Ovchiyan, Olivia Arter, Kevin Jolani, Erik R Dubberke, Gautam Dantas, Jennie H Kwon","doi":"10.1128/msystems.01591-25","DOIUrl":"https://doi.org/10.1128/msystems.01591-25","url":null,"abstract":"<p><p><i>Escherichia coli</i> is a public health threat capable of causing multiple types of infection, carrying a variety of antimicrobial resistance genes (ARGs), and disseminating ARGs to other microbes. Since ARG-carrying <i>E. coli</i> can exist as a commensal gut microbe, intestinal <i>E. coli</i> in community-associated (CA) members presents an under-appreciated reservoir of ARGs. We cultured 75 CA <i>E. coli</i> isolates from stool of 64 patients lacking inpatient healthcare exposures >24 hours in the previous 12 weeks. Remnant stool submitted to the Barnes-Jewish Hospital (BJH) microbiology laboratory for <i>Clostridioides difficile</i> testing was plated to MacConkey agar with ciprofloxacin and extended-spectrum beta-lactamase (ESBL) Chrome Agar to isolate resistant <i>E. coli</i> colonies, which were whole-genome sequenced. Isolates were compared to ESBL <i>E. coli</i> genomes published by Mahmud et al. (B. Mahmud, M. A. Wallace, K. A. Reske, K. Alvarado, et al., mSystems 7:e00519-22, 2022, https://doi.org/10.1128/msystems.00519-22), which were collected from bloodstream and urinary tract infections. We identified ESBL genes and quinolone resistance elements in <i>E. coli</i> isolates from all patients, 32 (50%) of whom had no recent antibiotic exposure. Sequence type (ST) 131 isolates carried more quinolone resistance elements but fewer ESBL genes than other STs. Eleven patients carried two distinct <i>E. coli</i> lineages simultaneously. CA ESBL <i>E. coli</i> displayed a lower diversity of beta-lactamase genes but similar rates of antibiotic resistance genes compared to ESBL <i>E. coli</i> reported by Mahmud et al. (https://doi.org/10.1128/msystems.00519-22). Carriage of resistance elements without recent antimicrobial exposure suggests the presence of circulating, resistant <i>E. coli</i>. Our results show the continually evolving resistance profile of CA <i>E. coli</i>, demonstrating the importance of characterizing antimicrobial resistance in the community.IMPORTANCEAntimicrobial-resistant <i>Escherichia coli</i> presents a substantial threat to public health, limiting treatment options and potentially horizontally transferring its resistance to other members of the gut microbiome. Resistance to quinolones and beta-lactams, specifically, hinders treatment of urinary tract and gastrointestinal infections, both commonly caused by <i>E. coli</i>. Tracking successful lineages, such as ST131, within the healthcare setting can inform clinicians about resistance patterns among their patients, but this work shows that other STs present an even higher antimicrobial resistance burden than ST131. In addition to monitoring multiple lineages of antimicrobial-resistant <i>E. coli</i>, it is necessary to identify and understand community-associated carriage of this organism, as evidenced by the increasing prevalence of community-associated ESBL <i>E. coli</i> carriage and our specific results showing similar resistance burdens within the clinic","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0159125"},"PeriodicalIF":4.6,"publicationDate":"2026-01-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145952538","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-12DOI: 10.1128/msystems.01305-25
Carlismari O Grundmann, Christopher J Tomo, Julia L Hershelman, Benjamin E Wolfe, Laura M Sanchez
Microbial interactions in cheese rinds influence community structure, food safety, and product quality. But the chemical mechanisms that mediate microbial interactions in cheeses and other fermented foods are generally not known. Here, we investigate how the spoilage mold Aspergillus westerdijkiae chemically inhibits beneficial cheese-rind bacteria using a combination of omics technologies. In cheese-rind community and co-culture experiments, A. westerdijkiae strongly inhibited most cheese-rind community members. In co-culture with Staphylococcus equorum, A. westerdijkiae strongly affected bacterial gene expression, including upregulation of a putative bceAB gene cluster that is associated with resistance to antimicrobial compounds in other bacteria. Mass spectrometry imaging revealed spatially localized production of secondary metabolites, including penicillic acid and ochratoxin B at the fungal-bacterial interface with Brachybacterium alimentarium. Integration of liquid chromatography-tandem mass spectrometry and genome annotations confirmed the presence of additional bioactive metabolites, such as notoamides and circumdatins. Fungal metabolic responses varied by bacterial partner, suggesting species-specific chemical strategies. Notably, penicillic acid levels increased 2.5-fold during interaction with B. alimentarium, and experiments with purified penicillic acid showed inhibition in a dose-dependent manner against this rind bacterium. These findings show that A. westerdijkiae deploys a context-dependent suite of mycotoxins and other metabolites, disrupting microbial community assembly in cheese rinds.IMPORTANCEThis study identifies the chemical mechanisms underlying the negative impacts of Aspergillus westerdijkiae on cheese-rind development, revealing how specialized metabolites like penicillic acid and ochratoxin B influence rind bacterial communities. By integrating biosynthetic gene cluster analyses with mass spectrometry, we demonstrate how chemical communication shapes microbial interactions, with possible implications for food safety and cheese quality. Understanding these interactions is essential for assessing the risks of fungal-driven spoilage and mycotoxin production in cheese-rind maturation. Beyond cheese, these findings contribute to broader microbiome ecology, emphasizing how secondary metabolites mediate microbial competition in natural and fermented food environments.
{"title":"Spatial metabolomics reveals the role of penicillic acid in cheese-rind microbiome disruption by a spoilage fungus.","authors":"Carlismari O Grundmann, Christopher J Tomo, Julia L Hershelman, Benjamin E Wolfe, Laura M Sanchez","doi":"10.1128/msystems.01305-25","DOIUrl":"10.1128/msystems.01305-25","url":null,"abstract":"<p><p>Microbial interactions in cheese rinds influence community structure, food safety, and product quality. But the chemical mechanisms that mediate microbial interactions in cheeses and other fermented foods are generally not known. Here, we investigate how the spoilage mold <i>Aspergillus westerdijkiae</i> chemically inhibits beneficial cheese-rind bacteria using a combination of omics technologies. In cheese-rind community and co-culture experiments, <i>A. westerdijkiae</i> strongly inhibited most cheese-rind community members. In co-culture with <i>Staphylococcus equorum</i>, <i>A. westerdijkiae</i> strongly affected bacterial gene expression, including upregulation of a putative <i>bceAB</i> gene cluster that is associated with resistance to antimicrobial compounds in other bacteria. Mass spectrometry imaging revealed spatially localized production of secondary metabolites, including penicillic acid and ochratoxin B at the fungal-bacterial interface with <i>Brachybacterium alimentarium</i>. Integration of liquid chromatography-tandem mass spectrometry and genome annotations confirmed the presence of additional bioactive metabolites, such as notoamides and circumdatins. Fungal metabolic responses varied by bacterial partner, suggesting species-specific chemical strategies. Notably, penicillic acid levels increased 2.5-fold during interaction with <i>B. alimentarium</i>, and experiments with purified penicillic acid showed inhibition in a dose-dependent manner against this rind bacterium. These findings show that <i>A. westerdijkiae</i> deploys a context-dependent suite of mycotoxins and other metabolites, disrupting microbial community assembly in cheese rinds.IMPORTANCEThis study identifies the chemical mechanisms underlying the negative impacts of <i>Aspergillus westerdijkiae</i> on cheese-rind development, revealing how specialized metabolites like penicillic acid and ochratoxin B influence rind bacterial communities. By integrating biosynthetic gene cluster analyses with mass spectrometry, we demonstrate how chemical communication shapes microbial interactions, with possible implications for food safety and cheese quality. Understanding these interactions is essential for assessing the risks of fungal-driven spoilage and mycotoxin production in cheese-rind maturation. Beyond cheese, these findings contribute to broader microbiome ecology, emphasizing how secondary metabolites mediate microbial competition in natural and fermented food environments.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0130525"},"PeriodicalIF":4.6,"publicationDate":"2026-01-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145952545","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
<p><p>Neonatal jaundice (NJ) might increase the risk of autism spectrum disorder (ASD) in children. This study examined whether alterations in the gut microbiota could explain the link between NJ and ASD. We analyzed three cohorts: NJ cohort 1 comprised 68 neonates with NJ and 68 healthy controls (HCs); NJ cohort 2 included 56 infants with NJ and 14 HCs; and the ASD cohort consisted of 43 children with ASD and 31 typically developing children. Fecal samples were collected aseptically. We performed 16S rRNA sequencing (NJ cohort 1), liquid chromatography with tandem mass spectrometry metabolomics (NJ cohort 1 and ASD cohort), and shotgun metagenomics (NJ cohort 2 and ASD cohort). We characterized the gut DNA virome, quantified bile acid metabolism genes, and integrated multi-omics data using causal mediation and machine learning causal inference. Both NJ and ASD were associated with increased diversity of bile acid metabolism genes, suggesting biomarker potential. The gut DNA virome was also identified as a potential biomarker. Causal mediation analysis showed that the gut DNA virome influences bile acid metabolism genes in both conditions. Using machine learning-based causal modeling, we further found that gut <i>human betaherpesviruses</i> and <i>human mastadenoviruses</i> contribute to NJ and ASD, respectively, mediated by gut bile acid-metabolizing bacteria. These findings suggest that perturbations in the virome and bile acid-metabolizing bacteria may explain the link between NJ and ASD. Our results indicate that NJ and ASD are associated with bile acid metabolism alterations, which are also influenced by the gut DNA virome. Dysbiosis of the gut DNA virome and bile acid-metabolizing bacteria may mechanistically link NJ and ASD.</p><p><strong>Importance: </strong>Human epidemiological studies have established an association between perinatal pathogenic infections and autism spectrum disorder (ASD), and the gut microbiota plays an extremely important role in this relationship. Neonatal jaundice (NJ) may increase the risk of ASD in children. However, it remains unclear whether alterations in the gut microbiota affect the association between NJ and ASD. Both NJ and ASD are linked to altered gut bile acid metabolism and significantly elevated gene diversity among bile acid metabolism enzymes, and these relationships are influenced by the gut virome. Gut human betaherpesviruses and human mastadenoviruses influence the development of NJ and ASD, respectively, by influencing the abundance of gut bile acid-metabolizing microbes. Alterations of the gut virome and bile acid-metabolizing bacteria appear to explain the link between NJ and ASD. There is a lack of effective treatment options for ASD. We found that both NJ and ASD are linked to altered bile acid metabolism. Gaining a comprehensive understanding of the role of the bile acid-gut microbiota axis in the pathogenesis of NJ and ASD, as well as regulating this axis, may be crucial for developing no
{"title":"Machine learning and causal inference applied to the gut metagenome-metabolome axis reveals a link between neonatal jaundice and autism spectrum disorder.","authors":"Xianhong Chen, Cheng Chen, Xiucai Lan, Xueli Zhang, Tingting Li, Peng Zhang, Guoqiang Cheng, Wei Zhou, Zhangxing Wang, Yingmei Xie, Shujuan Zeng, Wenhao Zhou, Mingbang Wang","doi":"10.1128/msystems.01405-25","DOIUrl":"https://doi.org/10.1128/msystems.01405-25","url":null,"abstract":"<p><p>Neonatal jaundice (NJ) might increase the risk of autism spectrum disorder (ASD) in children. This study examined whether alterations in the gut microbiota could explain the link between NJ and ASD. We analyzed three cohorts: NJ cohort 1 comprised 68 neonates with NJ and 68 healthy controls (HCs); NJ cohort 2 included 56 infants with NJ and 14 HCs; and the ASD cohort consisted of 43 children with ASD and 31 typically developing children. Fecal samples were collected aseptically. We performed 16S rRNA sequencing (NJ cohort 1), liquid chromatography with tandem mass spectrometry metabolomics (NJ cohort 1 and ASD cohort), and shotgun metagenomics (NJ cohort 2 and ASD cohort). We characterized the gut DNA virome, quantified bile acid metabolism genes, and integrated multi-omics data using causal mediation and machine learning causal inference. Both NJ and ASD were associated with increased diversity of bile acid metabolism genes, suggesting biomarker potential. The gut DNA virome was also identified as a potential biomarker. Causal mediation analysis showed that the gut DNA virome influences bile acid metabolism genes in both conditions. Using machine learning-based causal modeling, we further found that gut <i>human betaherpesviruses</i> and <i>human mastadenoviruses</i> contribute to NJ and ASD, respectively, mediated by gut bile acid-metabolizing bacteria. These findings suggest that perturbations in the virome and bile acid-metabolizing bacteria may explain the link between NJ and ASD. Our results indicate that NJ and ASD are associated with bile acid metabolism alterations, which are also influenced by the gut DNA virome. Dysbiosis of the gut DNA virome and bile acid-metabolizing bacteria may mechanistically link NJ and ASD.</p><p><strong>Importance: </strong>Human epidemiological studies have established an association between perinatal pathogenic infections and autism spectrum disorder (ASD), and the gut microbiota plays an extremely important role in this relationship. Neonatal jaundice (NJ) may increase the risk of ASD in children. However, it remains unclear whether alterations in the gut microbiota affect the association between NJ and ASD. Both NJ and ASD are linked to altered gut bile acid metabolism and significantly elevated gene diversity among bile acid metabolism enzymes, and these relationships are influenced by the gut virome. Gut human betaherpesviruses and human mastadenoviruses influence the development of NJ and ASD, respectively, by influencing the abundance of gut bile acid-metabolizing microbes. Alterations of the gut virome and bile acid-metabolizing bacteria appear to explain the link between NJ and ASD. There is a lack of effective treatment options for ASD. We found that both NJ and ASD are linked to altered bile acid metabolism. Gaining a comprehensive understanding of the role of the bile acid-gut microbiota axis in the pathogenesis of NJ and ASD, as well as regulating this axis, may be crucial for developing no","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0140525"},"PeriodicalIF":4.6,"publicationDate":"2026-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145934356","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2026-01-08DOI: 10.1128/msystems.01298-25
Izumo Kanesaka, Anurag Kumar Bari, Saïd Abdellati, Thibaut Vanbaelen, Irith De Baetselier, Tessa de Block, Reinout Naesens, Basil Britto Xavier, John Rossen, Chris Kenyon, Sheeba Santhini Manoharan-Basil
This study aims to characterize the phenotypic behavior and in vivo persistence of a ceftriaxone-tolerant Neisseria gonorrhoeae clinical isolate from a single patient and evaluate the potential role of tolerance in treatment failure. A previously identified ceftriaxone-tolerant vaginal isolate was compared with isogenic and clinical non-tolerant strains. Bacterial growth was assessed in vitro, and tolerance was quantified using the minimum duration required to kill 99% of the population (MDK99), and persistence was evaluated in an in vivo Galleria mellonella infection model. Whole-genome sequencing (WGS) and transcriptomic (RNA-sequencing [RNA-seq]) profiling were performed to identify tolerance-associated genetic and transcriptional signatures. The tolerant strain exhibited prolonged MDK99 values across ceftriaxone concentrations, persisting for up to 24 hours under drug exposure. It also showed delayed early-phase growth, suggesting a fitness cost. In vivo, the tolerant strain remained viable up to 8 hours after treatment, whereas non-tolerant strains were cleared. WGS revealed identical gene content across all isolates, but non-synonymous mutations in pilE_3, a type IV pilin gene, were exclusively present in tolerant strains. RNA-seq analysis showed upregulation of pilin-associated genes and downregulation of zinc-independent ribosomal paralogs (rpmE2 and ykgO), suggesting a combined mechanism of surface remodeling and translational suppression associated with the tolerant phenotype. Ceftriaxone tolerance enables prolonged survival of N. gonorrhoeae despite apparent susceptibility by standard MIC-based testing. This phenotype may contribute to treatment failure, recurrent infection, and ongoing transmission, indicating the need for revised diagnostic and therapeutic strategies.IMPORTANCECeftriaxone remains the last reliable option for gonorrhea therapy, yet recurrent infections can occur despite isolates being classified as susceptible by MIC testing. One possible explanation is antibiotic tolerance, a phenotype that allows survival during drug exposure without changes in MIC. Although tolerance has been described in other pathogens, its role in gonococcal infection has remained poorly defined. In this study, we provide the first detailed characterization of a ceftriaxone-tolerant Neisseria gonorrhoeae clinical isolate associated with repeated treatment failure. By combining in vitro killing assays, an in vivo Galleria mellonella infection model, whole-genome sequencing, and transcriptomic profiling, we demonstrate that tolerance enables prolonged survival under ceftriaxone and is linked to pilin gene variation and ribosomal remodeling. These findings illustrate how a clinically observed phenomenon can be mechanistically dissected and emphasize tolerance as a hidden factor contributing to gonococcal persistence and potential treatment failure.
{"title":"Characterizing ceftriaxone tolerance in <i>Neisseria gonorrhoeae</i> across <i>in vitro</i> and <i>in vivo</i> models.","authors":"Izumo Kanesaka, Anurag Kumar Bari, Saïd Abdellati, Thibaut Vanbaelen, Irith De Baetselier, Tessa de Block, Reinout Naesens, Basil Britto Xavier, John Rossen, Chris Kenyon, Sheeba Santhini Manoharan-Basil","doi":"10.1128/msystems.01298-25","DOIUrl":"https://doi.org/10.1128/msystems.01298-25","url":null,"abstract":"<p><p>This study aims to characterize the phenotypic behavior and <i>in vivo</i> persistence of a ceftriaxone-tolerant <i>Neisseria gonorrhoeae</i> clinical isolate from a single patient and evaluate the potential role of tolerance in treatment failure. A previously identified ceftriaxone-tolerant vaginal isolate was compared with isogenic and clinical non-tolerant strains. Bacterial growth was assessed <i>in vitro</i>, and tolerance was quantified using the minimum duration required to kill 99% of the population (MDK99), and persistence was evaluated in an <i>in vivo Galleria mellonella</i> infection model. Whole-genome sequencing (WGS) and transcriptomic (RNA-sequencing [RNA-seq]) profiling were performed to identify tolerance-associated genetic and transcriptional signatures. The tolerant strain exhibited prolonged MDK99 values across ceftriaxone concentrations, persisting for up to 24 hours under drug exposure. It also showed delayed early-phase growth, suggesting a fitness cost. <i>In vivo</i>, the tolerant strain remained viable up to 8 hours after treatment, whereas non-tolerant strains were cleared. WGS revealed identical gene content across all isolates, but non-synonymous mutations in pilE_3, a type IV pilin gene, were exclusively present in tolerant strains. RNA-seq analysis showed upregulation of pilin-associated genes and downregulation of zinc-independent ribosomal paralogs (<i>rpmE2</i> and <i>ykgO</i>), suggesting a combined mechanism of surface remodeling and translational suppression associated with the tolerant phenotype. Ceftriaxone tolerance enables prolonged survival of <i>N. gonorrhoeae</i> despite apparent susceptibility by standard MIC-based testing. This phenotype may contribute to treatment failure, recurrent infection, and ongoing transmission, indicating the need for revised diagnostic and therapeutic strategies.IMPORTANCECeftriaxone remains the last reliable option for gonorrhea therapy, yet recurrent infections can occur despite isolates being classified as susceptible by MIC testing. One possible explanation is antibiotic tolerance, a phenotype that allows survival during drug exposure without changes in MIC. Although tolerance has been described in other pathogens, its role in gonococcal infection has remained poorly defined. In this study, we provide the first detailed characterization of a ceftriaxone-tolerant <i>Neisseria gonorrhoeae</i> clinical isolate associated with repeated treatment failure. By combining <i>in vitro</i> killing assays, an <i>in vivo Galleria mellonella</i> infection model, whole-genome sequencing, and transcriptomic profiling, we demonstrate that tolerance enables prolonged survival under ceftriaxone and is linked to pilin gene variation and ribosomal remodeling. These findings illustrate how a clinically observed phenomenon can be mechanistically dissected and emphasize tolerance as a hidden factor contributing to gonococcal persistence and potential treatment failure.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0129825"},"PeriodicalIF":4.6,"publicationDate":"2026-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145934264","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-31DOI: 10.1128/msystems.01440-25
Hilary J Ranson, Yan-Song Ye, Valentina Z Petukhova, Abigail Green-Saxena, Ruolin He, Jiadong Sun, Bhaskar Godugu, Laura M Sanchez, Qihao Wu, David C Rowley
Bacteria produce a diverse range of specialized metabolites that influence the health and behavior of neighboring cells and, therefore, have potential applications in treating diseases. Deciphering the intended ecological functions of specialized metabolites is challenging due to the small scales at which these interactions occur and the complexity of unraveling simultaneous responses to multiple signals. In this study, we investigated the chemical interactions between two marine bacterial colonies, Vibrio parahaemolyticus PSU5429 and Bacillus pumilus YP001. When the two bacteria were grown in proximity on agar, V. parahaemolyticus exhibited swarming motility toward B. pumilus, but close approach to the B. pumilus colony was impeded by a zone of inhibition. Matrix-assisted laser desorption/ionization time-of-flight imaging mass spectrometry (MALDI-TOF IMS) suggested that lipopeptides produced by Bacillus induced swarming motility, a finding corroborated by genomic and chemical analyses of YP001. Based on activity and metabolomics guidance, the antibiotic amicoumacin B was found to be responsible for the observed antibiosis, while swarming motility by V. parahaemolyticus was induced by lipopeptides and two lipoamides. In this scenario, lipopeptide production by the Bacillus colony induces the Vibrio colony to swarm toward a lysis zone, resulting in a possible "catch and kill" effect. These results demonstrate the complexity of behaviors and outcomes exhibited by microbes under the simultaneous influence of different allelochemicals, suggesting possible interplays between antibiotics and compounds that induce motility.
Importance: Microbes communicate and compete using small molecules, yet linking specific metabolites to visible behaviors is difficult. We combine imaging mass spectrometry, genomics, analytical chemistry, and bioassays to decode an interaction between a marine Bacillus and the pathogen Vibrio parahaemolyticus. Surfactin-like lipopeptides act at a distance to stimulate Vibrio swarming and draw cells toward the colony. Amicoumacin B accumulates at the interface and halts growth, yielding a simple "catch and kill" outcome. This study shows that the spatial localization of natural products shapes microbial behavior on surfaces and provides a general, scalable workflow that maps chemistry to phenotype. Beyond this case, the approach can be applied broadly to understand and, ultimately, tune microbial interactions relevant to marine ecosystems, aquaculture health, and microbiome engineering.
{"title":"Lipopeptides and antibiotics from a marine <i>Bacillus pumilus</i> mediate a potential \"catch and kill\" effect on pathogenetic <i>Vibrio parahaemolyticus</i>.","authors":"Hilary J Ranson, Yan-Song Ye, Valentina Z Petukhova, Abigail Green-Saxena, Ruolin He, Jiadong Sun, Bhaskar Godugu, Laura M Sanchez, Qihao Wu, David C Rowley","doi":"10.1128/msystems.01440-25","DOIUrl":"https://doi.org/10.1128/msystems.01440-25","url":null,"abstract":"<p><p>Bacteria produce a diverse range of specialized metabolites that influence the health and behavior of neighboring cells and, therefore, have potential applications in treating diseases. Deciphering the intended ecological functions of specialized metabolites is challenging due to the small scales at which these interactions occur and the complexity of unraveling simultaneous responses to multiple signals. In this study, we investigated the chemical interactions between two marine bacterial colonies, <i>Vibrio parahaemolyticus</i> PSU5429 and <i>Bacillus pumilus</i> YP001. When the two bacteria were grown in proximity on agar, <i>V. parahaemolyticus</i> exhibited swarming motility toward <i>B. pumilus</i>, but close approach to the <i>B. pumilus</i> colony was impeded by a zone of inhibition. Matrix-assisted laser desorption/ionization time-of-flight imaging mass spectrometry (MALDI-TOF IMS) suggested that lipopeptides produced by <i>Bacillus</i> induced swarming motility, a finding corroborated by genomic and chemical analyses of YP001. Based on activity and metabolomics guidance, the antibiotic amicoumacin B was found to be responsible for the observed antibiosis, while swarming motility by <i>V. parahaemolyticus</i> was induced by lipopeptides and two lipoamides. In this scenario, lipopeptide production by the <i>Bacillus</i> colony induces the <i>Vibrio</i> colony to swarm toward a lysis zone, resulting in a possible \"catch and kill\" effect. These results demonstrate the complexity of behaviors and outcomes exhibited by microbes under the simultaneous influence of different allelochemicals, suggesting possible interplays between antibiotics and compounds that induce motility.</p><p><strong>Importance: </strong>Microbes communicate and compete using small molecules, yet linking specific metabolites to visible behaviors is difficult. We combine imaging mass spectrometry, genomics, analytical chemistry, and bioassays to decode an interaction between a marine <i>Bacillus</i> and the pathogen <i>Vibrio parahaemolyticus</i>. Surfactin-like lipopeptides act at a distance to stimulate <i>Vibrio</i> swarming and draw cells toward the colony. Amicoumacin B accumulates at the interface and halts growth, yielding a simple \"catch and kill\" outcome. This study shows that the spatial localization of natural products shapes microbial behavior on surfaces and provides a general, scalable workflow that maps chemistry to phenotype. Beyond this case, the approach can be applied broadly to understand and, ultimately, tune microbial interactions relevant to marine ecosystems, aquaculture health, and microbiome engineering.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0144025"},"PeriodicalIF":4.6,"publicationDate":"2025-12-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145878686","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-31DOI: 10.1128/msystems.01270-25
Ginger Tsueng, Emily Bullen, Candice Czech, Dylan Welzel, Leandro Collares, Jason Lin, Everaldo Rodolpho, Zubair Qazi, Nichollette Acosta, Lisa M Mayer, Sudha Venkatachari, Zorana Mitrović Vučičević, Poromendro N Burman, Deepti Jain, Jack DiGiovanna, Maria Giovanni, Asiyah Lin, Wilbert Van Panhuis, Laura D Hughes, Andrew I Su, Chunlei Wu
The National Institute of Allergy and Infectious Diseases (NIAID) Data Ecosystem Discovery Portal (https://data.niaid.nih.gov) provides a unified search interface for over 4 million data sets relevant to infectious and immune-mediated disease (IID) research. Integrating metadata from domain-specific and generalist repositories, the Portal enables researchers to identify and access data sets using user-friendly filters or advanced queries, without requiring technical expertise. The Portal supports discovery of a wide range of resources, including epidemiological, clinical, and multi-omic data sets and is designed to accommodate exploratory browsing and precise searches. The Portal provides filters, prebuilt queries, and data set collections to simplify the discovery process for users. The Portal additionally provides documentation and an API for programmatic access to harmonized metadata. By easing access barriers to important biomedical data sets, the NIAID Data Ecosystem Discovery Portal serves as an entry point for researchers working to understand, diagnose, or treat IID.IMPORTANCEValuable data sets are often overlooked because they are difficult to locate. The NIAID Data Ecosystem Discovery Portal fills this gap by providing a centralized, searchable interface that empowers users with varying levels of technical expertise to find and reuse data. By standardizing key metadata fields and harmonizing heterogeneous formats, the Portal improves data findability, accessibility, and reusability. This resource supports hypothesis generation, comparative analysis, and secondary use of public data by the IID research community, including those funded by NIAID. The Portal supports data sharing by standardizing metadata and linking to source repositories and maximizes the impact of public investment in research data by supporting scientific advancement via secondary use.
{"title":"The NIAID Discovery Portal: a unified search engine for infectious and immune-mediated disease datasets.","authors":"Ginger Tsueng, Emily Bullen, Candice Czech, Dylan Welzel, Leandro Collares, Jason Lin, Everaldo Rodolpho, Zubair Qazi, Nichollette Acosta, Lisa M Mayer, Sudha Venkatachari, Zorana Mitrović Vučičević, Poromendro N Burman, Deepti Jain, Jack DiGiovanna, Maria Giovanni, Asiyah Lin, Wilbert Van Panhuis, Laura D Hughes, Andrew I Su, Chunlei Wu","doi":"10.1128/msystems.01270-25","DOIUrl":"https://doi.org/10.1128/msystems.01270-25","url":null,"abstract":"<p><p>The National Institute of Allergy and Infectious Diseases (NIAID) Data Ecosystem Discovery Portal (https://data.niaid.nih.gov) provides a unified search interface for over 4 million data sets relevant to infectious and immune-mediated disease (IID) research. Integrating metadata from domain-specific and generalist repositories, the Portal enables researchers to identify and access data sets using user-friendly filters or advanced queries, without requiring technical expertise. The Portal supports discovery of a wide range of resources, including epidemiological, clinical, and multi-omic data sets and is designed to accommodate exploratory browsing and precise searches. The Portal provides filters, prebuilt queries, and data set collections to simplify the discovery process for users. The Portal additionally provides documentation and an API for programmatic access to harmonized metadata. By easing access barriers to important biomedical data sets, the NIAID Data Ecosystem Discovery Portal serves as an entry point for researchers working to understand, diagnose, or treat IID.IMPORTANCEValuable data sets are often overlooked because they are difficult to locate. The NIAID Data Ecosystem Discovery Portal fills this gap by providing a centralized, searchable interface that empowers users with varying levels of technical expertise to find and reuse data. By standardizing key metadata fields and harmonizing heterogeneous formats, the Portal improves data findability, accessibility, and reusability. This resource supports hypothesis generation, comparative analysis, and secondary use of public data by the IID research community, including those funded by NIAID. The Portal supports data sharing by standardizing metadata and linking to source repositories and maximizes the impact of public investment in research data by supporting scientific advancement via secondary use.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0127025"},"PeriodicalIF":4.6,"publicationDate":"2025-12-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145878763","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-31DOI: 10.1128/msystems.01492-25
Shuo Jiang, Peng Gao, Ping Shen, Suying Hou, Chenlu Xiao, Richard Yi Tsun Kao, Pak-Leung Ho, Yonghong Xiao, Huiluo Cao
Staphylococcus aureus clonal complex 59 (CC59) has emerged as a significant public health threat in Asia, yet the mechanisms driving its host adaptation and global evolutionary success remain poorly understood. Here, we performed a comprehensive genomic analysis of 3,994 global CC59 isolates, which included 549 isolates associated with bloodstream infections from China. Our analysis revealed three phylogenetically distinct lineages exhibiting region-specific distribution patterns, tracing their origins to the USA, Australia, and China. Notably, high-risk CC59 clones circulating in Taiwan likely diverged from mainland Chinese strains during the 1940s-1960s, coinciding with historical population migration following the Chinese civil war around 1949. Among China-associated CC59 strains, respiratory tract colonization was related to high cross-source linkage across multiple ecological niches, suggesting its role as a dissemination hub, particularly for bloodstream infection (BSI). Additionally, we observed significant enrichment of Clf-Sdr family proteins in human isolates, especially in BSI cases. Functional characterization using ΔclfB and ΔsdrD knockout strains demonstrated impaired biofilm formation, recapitulating findings in USA300. These findings establish an evolutionary framework for CC59 surveillance and highlight promising potential targets for anti-virulence therapeutics.
Importance: The prevalence and propagation of Staphylococcus aureus clonal complex 59 (CC59) in Asia are serious public health concerns. To understand its adaptation to hosts and worldwide evolutionary success, we analyzed the genomic population structure of all CC59 isolates and traced their evolutionary history. Our research indicates that CC59 lineages developed through unique evolutionary routes that vary across time and space, highlighting their adaptation to diverse ecological environments. This study presents a comprehensive genomic epidemiology framework that integrates extensive metadata analysis with evolutionary assessment. It serves as a model for future S. aureus monitoring and provides insights into potential targets for interventions focused on reducing virulence.
{"title":"Global emergence and evolution of <i>Staphylococcus aureus</i> clonal complex 59.","authors":"Shuo Jiang, Peng Gao, Ping Shen, Suying Hou, Chenlu Xiao, Richard Yi Tsun Kao, Pak-Leung Ho, Yonghong Xiao, Huiluo Cao","doi":"10.1128/msystems.01492-25","DOIUrl":"https://doi.org/10.1128/msystems.01492-25","url":null,"abstract":"<p><p><i>Staphylococcus aureus</i> clonal complex 59 (CC59) has emerged as a significant public health threat in Asia, yet the mechanisms driving its host adaptation and global evolutionary success remain poorly understood. Here, we performed a comprehensive genomic analysis of 3,994 global CC59 isolates, which included 549 isolates associated with bloodstream infections from China. Our analysis revealed three phylogenetically distinct lineages exhibiting region-specific distribution patterns, tracing their origins to the USA, Australia, and China. Notably, high-risk CC59 clones circulating in Taiwan likely diverged from mainland Chinese strains during the 1940s-1960s, coinciding with historical population migration following the Chinese civil war around 1949. Among China-associated CC59 strains, respiratory tract colonization was related to high cross-source linkage across multiple ecological niches, suggesting its role as a dissemination hub, particularly for bloodstream infection (BSI). Additionally, we observed significant enrichment of Clf-Sdr family proteins in human isolates, especially in BSI cases. Functional characterization using Δ<i>clfB</i> and Δ<i>sdrD</i> knockout strains demonstrated impaired biofilm formation, recapitulating findings in USA300. These findings establish an evolutionary framework for CC59 surveillance and highlight promising potential targets for anti-virulence therapeutics.</p><p><strong>Importance: </strong>The prevalence and propagation of <i>Staphylococcus aureus</i> clonal complex 59 (CC59) in Asia are serious public health concerns. To understand its adaptation to hosts and worldwide evolutionary success, we analyzed the genomic population structure of all CC59 isolates and traced their evolutionary history. Our research indicates that CC59 lineages developed through unique evolutionary routes that vary across time and space, highlighting their adaptation to diverse ecological environments. This study presents a comprehensive genomic epidemiology framework that integrates extensive metadata analysis with evolutionary assessment. It serves as a model for future <i>S. aureus</i> monitoring and provides insights into potential targets for interventions focused on reducing virulence.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0149225"},"PeriodicalIF":4.6,"publicationDate":"2025-12-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145878676","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}