The gut microbiome plays a crucial role in human health, and certain bacterial species, such as Faecalibacterium prausnitzii, are particularly beneficial. This study conducted a comprehensive investigation of prebiotic compounds that showed potential for specifically promoting beneficial gut bacteria. Using in vitro fecal cultures and a human intervention study, we identified maltobionic acid and lactobionic acid as compounds that specifically promoted Faecalibacterium growth both in vitro and in vivo without significantly affecting Bifidobacterium, which is typically increased by traditional prebiotics. In a human intervention study (n = 27), a significant increase was observed in Faecalibacterium abundance following maltobionic acid supplementation, with effectiveness correlating with the initial Parabacteroides abundance. Mechanistic investigations revealed a cross-feeding pathway between gut bacteria. In this pathway, Parabacteroides species converted the gluconic acid moiety of maltobionic and lactobionic acids to glucuronic acid, which was then preferentially utilized by Faecalibacterium. These findings suggest that gluconic acid-containing oligosaccharides are promising prebiotics for the targeted enhancement of beneficial Faecalibacterium and underscore the importance of microbial interactions in prebiotic research, offering new avenues for personalized microbiome modulation strategies.
{"title":"Targeted prebiotic application of gluconic acid-containing oligosaccharides promotes Faecalibacterium growth through microbial cross-feeding networks.","authors":"Hiroki Negishi, Ayumi Ichikawa, Saori Takahashi, Hiroshi Kano, Seiya Makino","doi":"10.1093/ismejo/wraf027","DOIUrl":"https://doi.org/10.1093/ismejo/wraf027","url":null,"abstract":"<p><p>The gut microbiome plays a crucial role in human health, and certain bacterial species, such as Faecalibacterium prausnitzii, are particularly beneficial. This study conducted a comprehensive investigation of prebiotic compounds that showed potential for specifically promoting beneficial gut bacteria. Using in vitro fecal cultures and a human intervention study, we identified maltobionic acid and lactobionic acid as compounds that specifically promoted Faecalibacterium growth both in vitro and in vivo without significantly affecting Bifidobacterium, which is typically increased by traditional prebiotics. In a human intervention study (n = 27), a significant increase was observed in Faecalibacterium abundance following maltobionic acid supplementation, with effectiveness correlating with the initial Parabacteroides abundance. Mechanistic investigations revealed a cross-feeding pathway between gut bacteria. In this pathway, Parabacteroides species converted the gluconic acid moiety of maltobionic and lactobionic acids to glucuronic acid, which was then preferentially utilized by Faecalibacterium. These findings suggest that gluconic acid-containing oligosaccharides are promising prebiotics for the targeted enhancement of beneficial Faecalibacterium and underscore the importance of microbial interactions in prebiotic research, offering new avenues for personalized microbiome modulation strategies.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-02-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143400615","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Shengjie Li, Xiaoli Dong, Pauline Humez, Joanna Borecki, Jean Birks, Cynthia McClain, Bernhard Mayer, Marc Strous, Muhe Diao
Members of Methylotenera are signature denitrifiers and methylotrophs commonly found together with methanotrophic bacteria in lakes and freshwater sediments. Here we show that three distinct Methylotenera ecotypes were abundant in methane-rich groundwaters recharged during the Pleistocene. Just like in surface water biomes, groundwater Methylotenera often co-occurred with methane-oxidizing bacteria, even though they were generally unable to denitrify. One abundant Methylotenera ecotype expressed a pathway for aerobic methane production from methylphosphonate. This phosphate-acquisition strategy was recently found to contribute to methane production in the oligotrophic, oxic upper ocean. Gene organization, phylogeny, and 3D protein structure of the key enzyme, C-P lyase subunit PhnJ, were consistent with a role in phosphate uptake. We conclude that phosphate may be a limiting nutrient in productive, methane-rich aquifers, and that methylphosphonate degradation might contribute to groundwater methane production.
{"title":"Proteomic evidence for aerobic methane production in groundwater by methylotrophic Methylotenera.","authors":"Shengjie Li, Xiaoli Dong, Pauline Humez, Joanna Borecki, Jean Birks, Cynthia McClain, Bernhard Mayer, Marc Strous, Muhe Diao","doi":"10.1093/ismejo/wraf024","DOIUrl":"https://doi.org/10.1093/ismejo/wraf024","url":null,"abstract":"<p><p>Members of Methylotenera are signature denitrifiers and methylotrophs commonly found together with methanotrophic bacteria in lakes and freshwater sediments. Here we show that three distinct Methylotenera ecotypes were abundant in methane-rich groundwaters recharged during the Pleistocene. Just like in surface water biomes, groundwater Methylotenera often co-occurred with methane-oxidizing bacteria, even though they were generally unable to denitrify. One abundant Methylotenera ecotype expressed a pathway for aerobic methane production from methylphosphonate. This phosphate-acquisition strategy was recently found to contribute to methane production in the oligotrophic, oxic upper ocean. Gene organization, phylogeny, and 3D protein structure of the key enzyme, C-P lyase subunit PhnJ, were consistent with a role in phosphate uptake. We conclude that phosphate may be a limiting nutrient in productive, methane-rich aquifers, and that methylphosphonate degradation might contribute to groundwater methane production.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-02-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143384060","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gi Yoon Shin, Jo Ann Asselin, Amy Smith, Brenna Aegerter, Teresa Coutinho, Mei Zhao, Bhabesh Dutta, Jennie Mazzone, Ram Neupane, Beth Gugino, Christy Hoepting, Manzeal Khanal, Subas Malla, Claudia Nischwitz, Jaspreet Sidhu, Antoinette Machado Burke, Jane Davey, Mark Uchanski, Michael L Derie, Lindsey J du Toit, Stephen Stresow-Cortez, Jean M Bonasera, Paul Stodghill, Brian Kvitko
Pantoea agglomerans is one of four Pantoea species reported in the USA to cause bacterial rot of onion bulbs. However, not all P. agglomerans strains are pathogenic to onion. We characterized onion-associated strains of P. agglomerans to elucidate the genetic and genomic signatures of onion-pathogenic P. agglomerans. We collected >300 P. agglomerans strains associated with symptomatic onion plants and bulbs from public culture collections, research laboratories, and a multi-year survey in 11 states in the USA. Combining the 87 genome assemblies with 100 high-quality, public P. agglomerans genome assemblies we identified two well-supported P. agglomerans phylogroups. Strains causing severe symptoms on onion were only identified in Phylogroup II and encoded the HiVir pantaphos biosynthetic cluster, supporting the role of HiVir as a pathogenicity factor. The P. agglomerans HiVir cluster was encoded in two distinct plasmid contexts: 1) as an accessory gene cluster on a conserved P. agglomerans plasmid (pAggl), or 2) on a mosaic cluster of plasmids common among onion strains (pOnion). Analysis of closed genomes revealed that the pOnion plasmids harbored alt genes conferring tolerance to Allium thiosulfinate defensive chemistry and many harbored cop genes conferring resistance to copper. We demonstrated that the pOnion plasmid pCB1C can act as a natively mobilizable pathogenicity plasmid that transforms P. agglomerans Phylogroup I strains, including environmental strains, into virulent pathogens of onion. This work indicates a central role for plasmids and plasmid ecology in mediating P. agglomerans interactions with onion plants, with potential implications for onion bacterial disease management.
{"title":"Plasmids encode and can mobilize onion pathogenicity in Pantoea agglomerans.","authors":"Gi Yoon Shin, Jo Ann Asselin, Amy Smith, Brenna Aegerter, Teresa Coutinho, Mei Zhao, Bhabesh Dutta, Jennie Mazzone, Ram Neupane, Beth Gugino, Christy Hoepting, Manzeal Khanal, Subas Malla, Claudia Nischwitz, Jaspreet Sidhu, Antoinette Machado Burke, Jane Davey, Mark Uchanski, Michael L Derie, Lindsey J du Toit, Stephen Stresow-Cortez, Jean M Bonasera, Paul Stodghill, Brian Kvitko","doi":"10.1093/ismejo/wraf019","DOIUrl":"https://doi.org/10.1093/ismejo/wraf019","url":null,"abstract":"<p><p>Pantoea agglomerans is one of four Pantoea species reported in the USA to cause bacterial rot of onion bulbs. However, not all P. agglomerans strains are pathogenic to onion. We characterized onion-associated strains of P. agglomerans to elucidate the genetic and genomic signatures of onion-pathogenic P. agglomerans. We collected >300 P. agglomerans strains associated with symptomatic onion plants and bulbs from public culture collections, research laboratories, and a multi-year survey in 11 states in the USA. Combining the 87 genome assemblies with 100 high-quality, public P. agglomerans genome assemblies we identified two well-supported P. agglomerans phylogroups. Strains causing severe symptoms on onion were only identified in Phylogroup II and encoded the HiVir pantaphos biosynthetic cluster, supporting the role of HiVir as a pathogenicity factor. The P. agglomerans HiVir cluster was encoded in two distinct plasmid contexts: 1) as an accessory gene cluster on a conserved P. agglomerans plasmid (pAggl), or 2) on a mosaic cluster of plasmids common among onion strains (pOnion). Analysis of closed genomes revealed that the pOnion plasmids harbored alt genes conferring tolerance to Allium thiosulfinate defensive chemistry and many harbored cop genes conferring resistance to copper. We demonstrated that the pOnion plasmid pCB1C can act as a natively mobilizable pathogenicity plasmid that transforms P. agglomerans Phylogroup I strains, including environmental strains, into virulent pathogens of onion. This work indicates a central role for plasmids and plasmid ecology in mediating P. agglomerans interactions with onion plants, with potential implications for onion bacterial disease management.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143069444","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carlos N Lozano-Andrade, Caja Dinesen, Mario Wibowo, Nil Arenos Bach, Viktor Hesselberg-Thomsen, Scott A Jarmusch, Mikael Lenz Strube, Ákos T Kovács
Soil bacteria are prolific producers of a myriad of biologically active secondary metabolites. These natural products play key roles in modern society, finding use as anti-cancer agents, as food additives, and as alternatives to chemical pesticides. As for their original role in interbacterial communication, secondary metabolites have been extensively studied under in vitro conditions, revealing many roles including antagonism, effects on motility, niche colonization, signaling, and cellular differentiation. Despite the growing body of knowledge on their mode of action, biosynthesis, and regulation, we still do not fully understand the role of secondary metabolites on the ecology of the producers and resident communities in situ. Here, we specifically examine the influence of Bacillus subtilis-produced cyclic lipopeptides during the assembly of a bacterial synthetic community, and simultaneously, explore the impact of cyclic lipopeptides on B. subtilis establishment success in a synthetic community propagated in an artificial soil microcosm. We found that surfactin production facilitates B. subtilis establishment success within multiple synthetic communities. Although neither a wild type nor a cyclic lipopeptide non-producer mutant had a major impact on the synthetic community composition over time, both the B. subtilis and the synthetic community metabolomes were altered during co-cultivation. Overall, our work demonstrates the importance of surfactin production in microbial communities, suggesting a broad spectrum of action of this natural product.
{"title":"Surfactin facilitates establishment of Bacillus subtilis in synthetic communities.","authors":"Carlos N Lozano-Andrade, Caja Dinesen, Mario Wibowo, Nil Arenos Bach, Viktor Hesselberg-Thomsen, Scott A Jarmusch, Mikael Lenz Strube, Ákos T Kovács","doi":"10.1093/ismejo/wraf013","DOIUrl":"10.1093/ismejo/wraf013","url":null,"abstract":"<p><p>Soil bacteria are prolific producers of a myriad of biologically active secondary metabolites. These natural products play key roles in modern society, finding use as anti-cancer agents, as food additives, and as alternatives to chemical pesticides. As for their original role in interbacterial communication, secondary metabolites have been extensively studied under in vitro conditions, revealing many roles including antagonism, effects on motility, niche colonization, signaling, and cellular differentiation. Despite the growing body of knowledge on their mode of action, biosynthesis, and regulation, we still do not fully understand the role of secondary metabolites on the ecology of the producers and resident communities in situ. Here, we specifically examine the influence of Bacillus subtilis-produced cyclic lipopeptides during the assembly of a bacterial synthetic community, and simultaneously, explore the impact of cyclic lipopeptides on B. subtilis establishment success in a synthetic community propagated in an artificial soil microcosm. We found that surfactin production facilitates B. subtilis establishment success within multiple synthetic communities. Although neither a wild type nor a cyclic lipopeptide non-producer mutant had a major impact on the synthetic community composition over time, both the B. subtilis and the synthetic community metabolomes were altered during co-cultivation. Overall, our work demonstrates the importance of surfactin production in microbial communities, suggesting a broad spectrum of action of this natural product.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143025722","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Escherichia coli is an increasingly antibiotic-resistant opportunistic pathogen. Few data are available on its ecological and evolutionary dynamics in its primary commensal niche, the vertebrate gut. Using Illumina and/or Nanopore technologies, we sequenced whole genomes of 210 E. coli isolates from 22 stools sampled during a 20-year period from a healthy man (ED) living in Paris, France. All phylogroups, except C, were represented, with a predominance of B2 (34.3%), followed by A and F (19% each) phylogroups. Thirty-five clones were identified based on their haplogroup and pairwise genomic single nucleotide polymorphism distance and classified in three phenotypes according to their abundance and residence time: 25 sub-dominant/transient (52 isolates), five dominant/transient (48 isolates) and five dominant/resident (110 isolates). Four over five dominant/resident clones belonged to B2 and closely related F phylogroups, whereas sub-dominant/transient clones belonged mainly to B1, A and D phylogroups. The long residence times of B2 clones seemed to be counterbalanced by lower colonization abilities. Clones with larger within-host frequency persisted for longer. By comparing ED strain genomes to a collection of commensal E. coli genomes from 359 French individuals, we identified ED-specific genomic properties including an enrichment in genes involved in a metabolic pathway (mhp cluster) and the presence of a very rare antiviral defense island. The E. coli colonization within the gut microbiota was shaped by both the intrinsic properties of the strain lineages, in particular longer residence of phylogroup B2, and the environmental constraints such as diet or phages.
大肠埃希菌是一种抗生素耐药性日益增强的机会性病原体。有关其在脊椎动物肠道这一主要共生生态位中的生态和进化动态的数据很少。利用 Illumina 和/或 Nanopore 技术,我们对生活在法国巴黎的一名健康男性(ED)20 年间从 22 份粪便样本中分离出的 210 个大肠杆菌进行了全基因组测序。除 C 型大肠杆菌外,所有系统群均有大肠杆菌,其中以 B2 型大肠杆菌居多(占 34.3%),其次是 A 型大肠杆菌和 F 型大肠杆菌(各占 19%)。根据单倍群和配对基因组单核苷酸多态性距离确定了 35 个克隆,并根据其丰度和驻留时间将其分为三种表型:25 个亚优势/瞬时型(52 个分离株)、5 个优势/瞬时型(48 个分离株)和 5 个优势/驻留型(110 个分离株)。五个优势/常驻克隆中有四个属于 B2 和密切相关的 F 系统群,而亚优势/瞬时克隆主要属于 B1、A 和 D 系统群。B2 克隆的驻留时间较长,但其定殖能力较低。宿主内频率较高的克隆持续时间较长。通过将 ED 菌株基因组与来自 359 个法国人的共生大肠杆菌基因组进行比较,我们发现了 ED 的特异性基因组特性,包括富含参与代谢途径(mhp 簇)的基因,以及存在一个非常罕见的抗病毒防御岛。大肠杆菌在肠道微生物群中的定植既受菌株品系固有特性的影响,尤其是噬菌体群 B2 的长期存在,也受饮食或噬菌体等环境因素的制约。
{"title":"Strain phylogroup and environmental constraints shape Escherichia coli dynamics and diversity over a 20-year human gut time series.","authors":"Bénédicte Condamine, Thibaut Morel-Journel, Florian Tesson, Guilhem Royer, Mélanie Magnan, Aude Bernheim, Erick Denamur, François Blanquart, Olivier Clermont","doi":"10.1093/ismejo/wrae245","DOIUrl":"10.1093/ismejo/wrae245","url":null,"abstract":"<p><p>Escherichia coli is an increasingly antibiotic-resistant opportunistic pathogen. Few data are available on its ecological and evolutionary dynamics in its primary commensal niche, the vertebrate gut. Using Illumina and/or Nanopore technologies, we sequenced whole genomes of 210 E. coli isolates from 22 stools sampled during a 20-year period from a healthy man (ED) living in Paris, France. All phylogroups, except C, were represented, with a predominance of B2 (34.3%), followed by A and F (19% each) phylogroups. Thirty-five clones were identified based on their haplogroup and pairwise genomic single nucleotide polymorphism distance and classified in three phenotypes according to their abundance and residence time: 25 sub-dominant/transient (52 isolates), five dominant/transient (48 isolates) and five dominant/resident (110 isolates). Four over five dominant/resident clones belonged to B2 and closely related F phylogroups, whereas sub-dominant/transient clones belonged mainly to B1, A and D phylogroups. The long residence times of B2 clones seemed to be counterbalanced by lower colonization abilities. Clones with larger within-host frequency persisted for longer. By comparing ED strain genomes to a collection of commensal E. coli genomes from 359 French individuals, we identified ED-specific genomic properties including an enrichment in genes involved in a metabolic pathway (mhp cluster) and the presence of a very rare antiviral defense island. The E. coli colonization within the gut microbiota was shaped by both the intrinsic properties of the strain lineages, in particular longer residence of phylogroup B2, and the environmental constraints such as diet or phages.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11728103/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142814841","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}
Amanda M Zdimal, Giacomo Di Dio, Wanxiang Liu, Tanya Aftab, Taryn Collins, Remy Colin, Abhishek Shrivastava
The collective surface motility and swarming behavior of microbes play a crucial role in the formation of polymicrobial communities, shaping ecosystems as diverse as animal and human microbiota, plant rhizospheres, and various aquatic environments. In the human oral microbiota, T9SS-driven gliding bacteria transport non-motile microbes and bacteriophages as cargo, thereby influencing the spatial organization and structural complexity of these polymicrobial communities. However, the physical rules governing the dispersal of T9SS-driven bacterial swarms are barely understood. Here, we collected time-lapse images, under anaerobic conditions, of developing swarms of a T9SS-driven microbe common to the human oral microbiota. Tracking of swarms revealed that small peripheral flares emerging from a colony develop structures that resemble fireworks displaying a chrysanthemum effect and flower-like patterns that convert to wave-like patterns and which further evolve into scattered microcolonies. Particle-image velocimetry showed density-dependent phase transitions and initial vorticity within these emerging patterns. Numerical simulations demonstrate that these patterns arise due to changes in swarm speed and alignment strength. Our data reveal a strategy used by an anaerobic swarming bacterium to control swarm behavior, resulting in scattered microcolonies distant from the mother colony, thus reducing competition for resources among colony members. This might ensure species survival even if conditions change drastically in one location of the human oral cavity.
{"title":"Swarming bacteria exhibit developmental phase transitions to establish scattered colonies in new regions.","authors":"Amanda M Zdimal, Giacomo Di Dio, Wanxiang Liu, Tanya Aftab, Taryn Collins, Remy Colin, Abhishek Shrivastava","doi":"10.1093/ismejo/wrae263","DOIUrl":"10.1093/ismejo/wrae263","url":null,"abstract":"<p><p>The collective surface motility and swarming behavior of microbes play a crucial role in the formation of polymicrobial communities, shaping ecosystems as diverse as animal and human microbiota, plant rhizospheres, and various aquatic environments. In the human oral microbiota, T9SS-driven gliding bacteria transport non-motile microbes and bacteriophages as cargo, thereby influencing the spatial organization and structural complexity of these polymicrobial communities. However, the physical rules governing the dispersal of T9SS-driven bacterial swarms are barely understood. Here, we collected time-lapse images, under anaerobic conditions, of developing swarms of a T9SS-driven microbe common to the human oral microbiota. Tracking of swarms revealed that small peripheral flares emerging from a colony develop structures that resemble fireworks displaying a chrysanthemum effect and flower-like patterns that convert to wave-like patterns and which further evolve into scattered microcolonies. Particle-image velocimetry showed density-dependent phase transitions and initial vorticity within these emerging patterns. Numerical simulations demonstrate that these patterns arise due to changes in swarm speed and alignment strength. Our data reveal a strategy used by an anaerobic swarming bacterium to control swarm behavior, resulting in scattered microcolonies distant from the mother colony, thus reducing competition for resources among colony members. This might ensure species survival even if conditions change drastically in one location of the human oral cavity.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11773418/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142923881","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}
Sarah Bolius, Alexandra Schmidt, Jérôme Kaiser, Helge W Arz, Olaf Dellwig, Ulf Karsten, Laura S Epp, Anke Kremp
Dormancy is a widespread key life history trait observed across the tree of life. Many plankton species form dormant cell stages that accumulate in aquatic sediments and, under anoxic conditions, form chronological records of past species and population dynamics under changing environmental conditions. Here we report on the germination of a microscopic alga, the abundant marine diatom Skeletonema marinoi Sarno et Zigone, that had remained dormant for up to 6871 ± 140 years in anoxic sediments of the Baltic Sea and resumed growth when exposed to oxygen and light. Resurrected diatom strains, representing cohorts from six different time points of the past 6871 ± 140 years, are genetically differentiated, and fundamental physiological functions such as growth and photosynthesis have remained stable through time despite distinct environmental dynamics. Showing that resurrection and full functional recovery, in comparison to 3 ± 2 years of dormancy, is possible after millennial resting, we emphasize the relevance of dormancy and living sediment archives. For the future, sediment archives, together with the resurrection approach, would offer a powerful tool to trace adaptive traits over millennia under distinct climatic conditions and elucidate the underlying mechanisms.
{"title":"Resurrection of a diatom after 7000 years from anoxic Baltic Sea sediment.","authors":"Sarah Bolius, Alexandra Schmidt, Jérôme Kaiser, Helge W Arz, Olaf Dellwig, Ulf Karsten, Laura S Epp, Anke Kremp","doi":"10.1093/ismejo/wrae252","DOIUrl":"10.1093/ismejo/wrae252","url":null,"abstract":"<p><p>Dormancy is a widespread key life history trait observed across the tree of life. Many plankton species form dormant cell stages that accumulate in aquatic sediments and, under anoxic conditions, form chronological records of past species and population dynamics under changing environmental conditions. Here we report on the germination of a microscopic alga, the abundant marine diatom Skeletonema marinoi Sarno et Zigone, that had remained dormant for up to 6871 ± 140 years in anoxic sediments of the Baltic Sea and resumed growth when exposed to oxygen and light. Resurrected diatom strains, representing cohorts from six different time points of the past 6871 ± 140 years, are genetically differentiated, and fundamental physiological functions such as growth and photosynthesis have remained stable through time despite distinct environmental dynamics. Showing that resurrection and full functional recovery, in comparison to 3 ± 2 years of dormancy, is possible after millennial resting, we emphasize the relevance of dormancy and living sediment archives. For the future, sediment archives, together with the resurrection approach, would offer a powerful tool to trace adaptive traits over millennia under distinct climatic conditions and elucidate the underlying mechanisms.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11742256/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142923862","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}
Sébastien Santini, Audrey Lartigue, Jean-Marie Alempic, Yohann Couté, Lucid Belmudes, William J Brazelton, Susan Q Lang, Jean-Michel Claverie, Matthieu Legendre, Chantal Abergel
The microbial sampling of submarine hydrothermal vents remains challenging, with even fewer studies focused on viruses. Here we report what is to our knowledge the first isolation of a eukaryotic virus from the Lost City hydrothermal field, by co-culture with the laboratory host Acanthamoeba castellanii. This virus, named pacmanvirus lostcity, is closely related to previously isolated pacmanviruses (strains A23 and S19), clustering in a divergent clade within the long-established family Asfarviridae. The icosahedral particles of this virus are 200 nm in diameter, with an electron-dense core surrounded by an inner membrane. The viral genome of 395 708 bp (33% G + C) has been predicted to encode 473 proteins. However, besides these standard properties, pacmanvirus lostcity was found to be associated with a new type of selfish genetic element, 7 kb in length, whose architecture and gene content are reminiscent of those of transpovirons, hitherto specific to the family Mimiviridae. As in previously described transpovirons, this selfishg genetic element propagates as an episome within its host virus particles and exhibits partial recombination with its genome. In addition, an unrelated episome with a length of 2 kb was also found to be associated with pacmanvirus lostcity. Together, the transpoviron and the 2-kb episome might participate in exchanges between pacmanviruses and other DNA virus families. It remains to be elucidated if the presence of these mobile genetic elements is restricted to pacmanviruses or was simply overlooked in other members of the Asfarviridae.
海底热液喷口的微生物取样仍然具有挑战性,关注病毒的研究甚至更少。在这里,我们报告了第一次从失落之城热液区分离出真核病毒,通过与实验室宿主棘阿米巴castellanii共同培养。这种病毒被命名为pacmanvirus lostcity,与以前分离的pacmanvirus(毒株A23和S19)密切相关,在建立已久的Asfarviridae家族中聚集在一个不同的分支中。它的二十面体粒子直径为200纳米,有一个被内膜包围的电子密集的核。其基因组全长395 708 bp (33% G + C),预计编码473种蛋白质。然而,除了这些标准特性外,还发现pacmanvirus的失活与一种新的自私遗传元件有关,其长度为7kb,其结构和基因含量与转座子的结构和基因含量相似,迄今为止仅为Mimiviridae家族所特有。与先前描述的转座子一样,该元件在其宿主病毒颗粒内作为片段繁殖,并表现出与其基因组的部分重组。此外,一个不相关的2 kb长的片段也与pacmanvirus的丧失有关。转座子和2kb片段可能共同参与了吃豆病毒和其他大型DNA病毒家族之间的交换。这些可移动遗传因子的存在是否仅限于吃豆病毒,还是在其他阿斯法病毒科成员中被简单地忽略了,还有待阐明。
{"title":"Pacmanvirus isolated from the Lost City hydrothermal field extends the concept of transpoviron beyond the family Mimiviridae.","authors":"Sébastien Santini, Audrey Lartigue, Jean-Marie Alempic, Yohann Couté, Lucid Belmudes, William J Brazelton, Susan Q Lang, Jean-Michel Claverie, Matthieu Legendre, Chantal Abergel","doi":"10.1093/ismejo/wraf002","DOIUrl":"10.1093/ismejo/wraf002","url":null,"abstract":"<p><p>The microbial sampling of submarine hydrothermal vents remains challenging, with even fewer studies focused on viruses. Here we report what is to our knowledge the first isolation of a eukaryotic virus from the Lost City hydrothermal field, by co-culture with the laboratory host Acanthamoeba castellanii. This virus, named pacmanvirus lostcity, is closely related to previously isolated pacmanviruses (strains A23 and S19), clustering in a divergent clade within the long-established family Asfarviridae. The icosahedral particles of this virus are 200 nm in diameter, with an electron-dense core surrounded by an inner membrane. The viral genome of 395 708 bp (33% G + C) has been predicted to encode 473 proteins. However, besides these standard properties, pacmanvirus lostcity was found to be associated with a new type of selfish genetic element, 7 kb in length, whose architecture and gene content are reminiscent of those of transpovirons, hitherto specific to the family Mimiviridae. As in previously described transpovirons, this selfishg genetic element propagates as an episome within its host virus particles and exhibits partial recombination with its genome. In addition, an unrelated episome with a length of 2 kb was also found to be associated with pacmanvirus lostcity. Together, the transpoviron and the 2-kb episome might participate in exchanges between pacmanviruses and other DNA virus families. It remains to be elucidated if the presence of these mobile genetic elements is restricted to pacmanviruses or was simply overlooked in other members of the Asfarviridae.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11788076/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142958163","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}
Caitlin M Broderick, Gian Maria Niccolò Benucci, Luciana Ruggiero Bachega, Gabriel D Miller, Sarah E Evans, Christine V Hawkes
Long-term climate history can influence rates of soil carbon cycling but the microbial traits underlying these legacy effects are not well understood. Legacies may result if historical climate differences alter the traits of soil microbial communities, particularly those associated with carbon cycling and stress tolerance. However, it is also possible that contemporary conditions can overcome the influence of historical climate, particularly under extreme conditions. Using shotgun metagenomics, we assessed the composition of soil microbial functional genes across a mean annual precipitation gradient that previously showed evidence of strong climate legacies in soil carbon flux and extracellular enzyme activity. Sampling coincided with recovery from a regional, multi-year severe drought, allowing us to document how the strength of climate legacies varied with contemporary conditions. We found increased investment in genes associated with resource cycling with historically higher precipitation across the gradient, particularly in traits related to resource transport and complex carbon degradation. This legacy effect was strongest in seasons with the lowest soil moisture, suggesting that contemporary conditions-particularly, resource stress under water limitation-influences the strength of legacy effects. In contrast, investment in stress tolerance did not vary with historical precipitation, likely due to frequent periodic drought throughout the gradient. Differences in the relative abundance of functional genes explained over half of variation in microbial functional capacity-potential enzyme activity-more so than historical precipitation or current moisture conditions. Together, these results suggest that long-term climate can alter the functional potential of soil microbial communities, leading to legacies in carbon cycling.
{"title":"Long-term climate establishes functional legacies by altering microbial traits.","authors":"Caitlin M Broderick, Gian Maria Niccolò Benucci, Luciana Ruggiero Bachega, Gabriel D Miller, Sarah E Evans, Christine V Hawkes","doi":"10.1093/ismejo/wraf005","DOIUrl":"10.1093/ismejo/wraf005","url":null,"abstract":"<p><p>Long-term climate history can influence rates of soil carbon cycling but the microbial traits underlying these legacy effects are not well understood. Legacies may result if historical climate differences alter the traits of soil microbial communities, particularly those associated with carbon cycling and stress tolerance. However, it is also possible that contemporary conditions can overcome the influence of historical climate, particularly under extreme conditions. Using shotgun metagenomics, we assessed the composition of soil microbial functional genes across a mean annual precipitation gradient that previously showed evidence of strong climate legacies in soil carbon flux and extracellular enzyme activity. Sampling coincided with recovery from a regional, multi-year severe drought, allowing us to document how the strength of climate legacies varied with contemporary conditions. We found increased investment in genes associated with resource cycling with historically higher precipitation across the gradient, particularly in traits related to resource transport and complex carbon degradation. This legacy effect was strongest in seasons with the lowest soil moisture, suggesting that contemporary conditions-particularly, resource stress under water limitation-influences the strength of legacy effects. In contrast, investment in stress tolerance did not vary with historical precipitation, likely due to frequent periodic drought throughout the gradient. Differences in the relative abundance of functional genes explained over half of variation in microbial functional capacity-potential enzyme activity-more so than historical precipitation or current moisture conditions. Together, these results suggest that long-term climate can alter the functional potential of soil microbial communities, leading to legacies in carbon cycling.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11805608/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142973118","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}
One of the central questions in microbial ecology is how to explain the high biodiversity of communities. A large number of rare taxa in the community have not been excluded by abundant taxa with competitive advantages, a contradiction known as the biodiversity paradox. Recently, increasing evidence has revealed the central importance of antimicrobial toxins as crucial weapons of antagonism in microbial survival. The powerful effects of antimicrobial toxins result in simple combinations of microorganisms failing to coexist under laboratory conditions, but it is unclear whether they also have a negative impact on the biodiversity of natural communities. Here, we revealed that microbial communities worldwide universally possess functional potential for antimicrobial toxin production. Counterintuitively, the biodiversity of global microbial communities increases, rather than decreases, as the abundance of antimicrobial toxins in rare taxa rises. Rare taxa may encode more antimicrobial toxins than abundant taxa, which is associated with the maintenance of the high biodiversity of microbial communities amid complex interactions. Our findings suggest that the antagonistic interaction caused by antimicrobial toxins may play a positive role in microbial community biodiversity at the global scale.
{"title":"Global microbial community biodiversity increases with antimicrobial toxin abundance of rare taxa.","authors":"Ya Liu, Yu Geng, Yiru Jiang, Peng Li, Yue-Zhong Li, Zheng Zhang","doi":"10.1093/ismejo/wraf012","DOIUrl":"10.1093/ismejo/wraf012","url":null,"abstract":"<p><p>One of the central questions in microbial ecology is how to explain the high biodiversity of communities. A large number of rare taxa in the community have not been excluded by abundant taxa with competitive advantages, a contradiction known as the biodiversity paradox. Recently, increasing evidence has revealed the central importance of antimicrobial toxins as crucial weapons of antagonism in microbial survival. The powerful effects of antimicrobial toxins result in simple combinations of microorganisms failing to coexist under laboratory conditions, but it is unclear whether they also have a negative impact on the biodiversity of natural communities. Here, we revealed that microbial communities worldwide universally possess functional potential for antimicrobial toxin production. Counterintuitively, the biodiversity of global microbial communities increases, rather than decreases, as the abundance of antimicrobial toxins in rare taxa rises. Rare taxa may encode more antimicrobial toxins than abundant taxa, which is associated with the maintenance of the high biodiversity of microbial communities amid complex interactions. Our findings suggest that the antagonistic interaction caused by antimicrobial toxins may play a positive role in microbial community biodiversity at the global scale.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11822679/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143030278","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}