As the most abundant marine microorganisms, SAR11 bacteria contribute significantly to global carbon and nutrient cycling. Pelagiphages, viruses that infect SAR11, are potential drivers in structuring the communities, shaping the evolution, and reprogramming the metabolism of SAR11. However, interactions between SAR11 and pelagiphages remain poorly understood. In this study, we investigated and compared the transcriptional dynamics of the SAR11 strain, Candidatus Pelagibacter communis HTCC1062, under independent infection with two phylogenetically distinct pelagiphages: the temperate HTVC019P-type pelagiphage HTVC022P and the lytic HTVC023P-type pelagiphage HTVC027P. These two pelagiphages exhibited distinct infection kinetics, with HTVC022P showing a shorter latent period and a faster host takeover. Transcriptome profiling revealed that infection with HTVC022P and HTVC027P led to the differential expression of 136 and 460 host genes, respectively. Compared to the uninfected control, both pelagiphage infections enhanced host transcription, upregulating the majority of differentially expressed genes. Both pelagiphages induced upregulation of host genes involved in DNA metabolism, transcription, translation, central carbon and nitrogen metabolism. Notably, HTVC027P infection led to the upregulation of 56 genes involved in phosphate, sulfur, and iron metabolism, as well as oxidative phosphorylation and one-carbon metabolism. In contrast, HTVC022P had minimal effects on these pathways. These results suggest that distinct pelagiphages exert unique effects on host metabolic processes, implying divergent ecological implications. Collectively, our study provides new insights into SAR11-pelagiphage interactions, enhancing our understanding of the metabolic states of phage-infected SAR11 bacteria and the ecological functions of phages in marine systems.
SAR11细菌是最丰富的海洋微生物,对全球碳和养分循环有重要贡献。表面噬菌体是感染SAR11的病毒,是构建群落、塑造进化和重编程SAR11代谢的潜在驱动因素。然而,SAR11和表皮细胞之间的相互作用仍然知之甚少。在本研究中,我们研究并比较了SAR11菌株Candidatus Pelagibacter communis HTCC1062在两种系统发育不同的噬菌体(温带型htvc019p型噬菌体HTVC022P和裂解型htvc023p型噬菌体HTVC027P)独立感染下的转录动力学。这两种噬菌体表现出不同的感染动力学,其中HTVC022P潜伏期较短,宿主接管速度较快。转录组分析显示,HTVC022P和HTVC027P感染分别导致136和460个宿主基因的差异表达。与未感染的对照组相比,两种噬菌体感染都增强了宿主转录,上调了大多数差异表达基因。这两种噬菌体均诱导宿主参与DNA代谢、转录、翻译、中心碳氮代谢的基因上调。值得注意的是,HTVC027P感染导致56个参与磷酸盐、硫和铁代谢以及氧化磷酸化和单碳代谢的基因上调。相比之下,HTVC022P对这些途径的影响微乎其微。这些结果表明,不同的外噬细胞对宿主的代谢过程有独特的影响,这意味着不同的生态意义。总的来说,我们的研究为SAR11-表面噬菌体相互作用提供了新的见解,增强了我们对噬菌体感染SAR11细菌代谢状态和海洋系统中噬菌体生态功能的理解。
{"title":"Comparative transcriptomes reveal differential effects on host metabolism reprogramming in two different pelagiphage-SAR11 infection systems.","authors":"Zefeng Zhang, Xinxin Liu, Yahui Zhang, Hang Xiao, Pei Liu, Mingyu Yang, Fang Qin, Ying Wu, Hanqi Ying, Zuqing Wu, Yanlin Zhao","doi":"10.1093/ismeco/ycaf233","DOIUrl":"10.1093/ismeco/ycaf233","url":null,"abstract":"<p><p>As the most abundant marine microorganisms, SAR11 bacteria contribute significantly to global carbon and nutrient cycling. Pelagiphages, viruses that infect SAR11, are potential drivers in structuring the communities, shaping the evolution, and reprogramming the metabolism of SAR11. However, interactions between SAR11 and pelagiphages remain poorly understood. In this study, we investigated and compared the transcriptional dynamics of the SAR11 strain, <i>Candidatus</i> Pelagibacter communis HTCC1062, under independent infection with two phylogenetically distinct pelagiphages: the temperate HTVC019P-type pelagiphage HTVC022P and the lytic HTVC023P-type pelagiphage HTVC027P. These two pelagiphages exhibited distinct infection kinetics, with HTVC022P showing a shorter latent period and a faster host takeover. Transcriptome profiling revealed that infection with HTVC022P and HTVC027P led to the differential expression of 136 and 460 host genes, respectively. Compared to the uninfected control, both pelagiphage infections enhanced host transcription, upregulating the majority of differentially expressed genes. Both pelagiphages induced upregulation of host genes involved in DNA metabolism, transcription, translation, central carbon and nitrogen metabolism. Notably, HTVC027P infection led to the upregulation of 56 genes involved in phosphate, sulfur, and iron metabolism, as well as oxidative phosphorylation and one-carbon metabolism. In contrast, HTVC022P had minimal effects on these pathways. These results suggest that distinct pelagiphages exert unique effects on host metabolic processes, implying divergent ecological implications. Collectively, our study provides new insights into SAR11-pelagiphage interactions, enhancing our understanding of the metabolic states of phage-infected SAR11 bacteria and the ecological functions of phages in marine systems.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf233"},"PeriodicalIF":6.1,"publicationDate":"2025-12-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753301/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890690","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The evolutionary adaptation of archaea to ecologically diverse habitats remains poorly understood. Ammonia-oxidizing archaea (AOA) exhibit significant diversification across various environmental conditions; however, their ecological dynamics, diversification, and associated evolutionary processes are still largely unexplored in coastal environments, which contain extensive ecosystem heterogeneity. Combining newly assembled metagenomic data from Chinese marginal seas (2059 km coverage) with global datasets (spanning over 16 000 km), these knowledge gaps were explored across a continental-scale latitudinal gradient. It revealed that coastal AOA genomic diversity is latitude-dependent, with predicted optimum growth temperatures and substrate metabolic pathways explaining the geographical distribution. The two dominant genus-level clades exhibited significantly distinct benthic-pelagic niches, associated with specific genes involved in nutrient uptake and stress resistance. Phylogenomic reconstructions suggest that AOA initially colonized the coastal ocean sediments around 718 million years ago (Mya), and subsequent purifying selection and low recombination facilitated the AOA niche expansion into marine coastal environments. By revealing the evolutionary trajectories of Nitrososphaeria and their differential colonization patterns, our findings offer a novel perspective on the mechanisms of AOA diversification in the coastal ocean. This work advances our understanding of microbial diversification and niche differentiation of AOA in coastal ecosystems as well as the evolutionary forces shaping their global biogeography.
{"title":"Purifying selection and low recombination facilitated sequential colonization of benthic and pelagic coastal ocean by ammonia-oxidizing archaea.","authors":"Gaoyang Ren, Cécile Gubry-Rangin, Wenhao Wang, Ronghua Liu, Jiao Liu, Jinmei Liu, Xiao-Hua Zhang, Jiwen Liu","doi":"10.1093/ismeco/ycaf234","DOIUrl":"10.1093/ismeco/ycaf234","url":null,"abstract":"<p><p>The evolutionary adaptation of archaea to ecologically diverse habitats remains poorly understood. Ammonia-oxidizing archaea (AOA) exhibit significant diversification across various environmental conditions; however, their ecological dynamics, diversification, and associated evolutionary processes are still largely unexplored in coastal environments, which contain extensive ecosystem heterogeneity. Combining newly assembled metagenomic data from Chinese marginal seas (2059 km coverage) with global datasets (spanning over 16 000 km), these knowledge gaps were explored across a continental-scale latitudinal gradient. It revealed that coastal AOA genomic diversity is latitude-dependent, with predicted optimum growth temperatures and substrate metabolic pathways explaining the geographical distribution. The two dominant genus-level clades exhibited significantly distinct benthic-pelagic niches, associated with specific genes involved in nutrient uptake and stress resistance. Phylogenomic reconstructions suggest that AOA initially colonized the coastal ocean sediments around 718 million years ago (Mya), and subsequent purifying selection and low recombination facilitated the AOA niche expansion into marine coastal environments. By revealing the evolutionary trajectories of <i>Nitrososphaeria</i> and their differential colonization patterns, our findings offer a novel perspective on the mechanisms of AOA diversification in the coastal ocean. This work advances our understanding of microbial diversification and niche differentiation of AOA in coastal ecosystems as well as the evolutionary forces shaping their global biogeography.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf234"},"PeriodicalIF":6.1,"publicationDate":"2025-12-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753310/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890659","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-06eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf228
Esteban Bustos-Caparros, Tomeu Viver, Juan F Gago, Stephanus N Venter, Rafael Bosch, Konstantinos T Konstantinidis, Luis M Rodriguez-R, Ramon Rossello-Mora
An unbiased and accurate estimation of intraspecies diversity, i.e. the extent of genetic diversity within species (or microdiversity), is crucial for clinical and environmental microbiome studies. Although it is well appreciated that sequencing depth (or coverage depth) below 10X can provide biased estimates of microdiversity, typically underestimating diversity due to the random sampling of alleles, there is a widely accepted convention that microdiversity estimates tend to be relatively stable at sequencing depth exceeding 10X. Therefore, discarding species with <10X or rarefying to 10-20X sequencing depth are generally used to compare microdiversity among taxa and samples. Our findings showed that these biases may persist even at depth levels above 50-200X for all popular sequencing platforms, including Illumina, PacBio, and Oxford Nanopore. The biases mostly, but not always, represent an underestimation of diversity and were attributable to the incomplete recovery of Single Nucleotide Variants (SNVs) at lower sequencing depth levels. To address this issue, we recommend using rarefaction-based approaches to standardize data at least 50X, and ideally at 200X sequencing depth, which reduces differences between observed and expected microdiversity values to <0.5%. Furthermore, the Average Nucleotide Identity of reads (ANIr) metric is significantly less sensitive to sequencing depth variability than nucleotide diversity (π), making it a robust alternative for estimating microdiversity at sequencing depth close or exceeding 10X, without a need to rarefying data. Therefore, the sequencing depth thresholds proposed herein provide a more standardized framework for direct comparisons of microdiversity across samples and studies.
{"title":"Uneven sequencing (coverage) depth can bias microbial intraspecies diversity estimates and how to account for it.","authors":"Esteban Bustos-Caparros, Tomeu Viver, Juan F Gago, Stephanus N Venter, Rafael Bosch, Konstantinos T Konstantinidis, Luis M Rodriguez-R, Ramon Rossello-Mora","doi":"10.1093/ismeco/ycaf228","DOIUrl":"10.1093/ismeco/ycaf228","url":null,"abstract":"<p><p>An unbiased and accurate estimation of intraspecies diversity, i.e. the extent of genetic diversity within species (or microdiversity), is crucial for clinical and environmental microbiome studies. Although it is well appreciated that sequencing depth (or coverage depth) below 10X can provide biased estimates of microdiversity, typically underestimating diversity due to the random sampling of alleles, there is a widely accepted convention that microdiversity estimates tend to be relatively stable at sequencing depth exceeding 10X. Therefore, discarding species with <10X or rarefying to 10-20X sequencing depth are generally used to compare microdiversity among taxa and samples. Our findings showed that these biases may persist even at depth levels above 50-200X for all popular sequencing platforms, including Illumina, PacBio, and Oxford Nanopore. The biases mostly, but not always, represent an underestimation of diversity and were attributable to the incomplete recovery of Single Nucleotide Variants (SNVs) at lower sequencing depth levels. To address this issue, we recommend using rarefaction-based approaches to standardize data at least 50X, and ideally at 200X sequencing depth, which reduces differences between observed and expected microdiversity values to <0.5%. Furthermore, the Average Nucleotide Identity of reads (ANIr) metric is significantly less sensitive to sequencing depth variability than nucleotide diversity (<i>π</i>), making it a robust alternative for estimating microdiversity at sequencing depth close or exceeding 10X, without a need to rarefying data. Therefore, the sequencing depth thresholds proposed herein provide a more standardized framework for direct comparisons of microdiversity across samples and studies.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf228"},"PeriodicalIF":6.1,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753299/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890627","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The bacterial-type Wood-Ljungdahl (WL) pathway and reductive tricarboxylic acid (rTCA) cycle are the dominant chemolithotrophic CO2 fixation pathways in bacteria inhabiting aphotic geothermal and deep-sea hydrothermal ecosystems. However, the activity of these bacterial metabolic systems in ecosystems with available organic carbons remains unclear. Here, we examined the impact of extracellular acetate on the CO2-fixation pathways of three thermophilic hydrogen-oxidizing and non-acetogenic bacteria using 13C tracer-based metabolomics. Under chemolithoautotrophic conditions, Thermodesulfatator indicus and Hydrogenobacter thermophilus fixed CO2 through the WL pathway and rTCA cycle, respectively, whereas Thermovibrio ammonificans, which has been suggested to operate both of these pathways, exhibited significant CO2 fixation through only the rTCA cycle. Under chemolithomixotrophic conditions with acetate, H. thermophilus and T. ammonificans assimilated both CO2 and acetate via the rTCA cycle. In contrast, acetate suppressed CO2 fixation through the WL pathway in T. indicus and was used as the primary carbon source under chemolithomixotrophic conditions. These results suggest that the contribution of the WL pathway for CO2 fixation might be overestimated in ecosystems where acetate is available. Moreover, the present findings indicate that simultaneous CO2 fixation through both the WL pathway and rTCA cycle in a cell, which has been proposed as a possible metabolic strategy for CO2-fixation in ancestral life, is not advantageous in extant microorganisms.
{"title":"Impact of acetate on CO<sub>2</sub> fixation pathways in thermophilic and hydrogenotrophic bacteria.","authors":"Yoko Chiba, Tomomi Sumida, Masafumi Kameya, Yuto Fukuyama, Tomoyuki Wakashima, Shigeru Shimamura, Ryoma Kamikawa, Yoshito Chikaraishi, Takuro Nunoura","doi":"10.1093/ismeco/ycaf227","DOIUrl":"10.1093/ismeco/ycaf227","url":null,"abstract":"<p><p>The bacterial-type Wood-Ljungdahl (WL) pathway and reductive tricarboxylic acid (rTCA) cycle are the dominant chemolithotrophic CO<sub>2</sub> fixation pathways in bacteria inhabiting aphotic geothermal and deep-sea hydrothermal ecosystems. However, the activity of these bacterial metabolic systems in ecosystems with available organic carbons remains unclear. Here, we examined the impact of extracellular acetate on the CO<sub>2</sub>-fixation pathways of three thermophilic hydrogen-oxidizing and non-acetogenic bacteria using <sup>13</sup>C tracer-based metabolomics. Under chemolithoautotrophic conditions, <i>Thermodesulfatator indicus</i> and <i>Hydrogenobacter thermophilus</i> fixed CO<sub>2</sub> through the WL pathway and rTCA cycle, respectively, whereas <i>Thermovibrio ammonificans</i>, which has been suggested to operate both of these pathways, exhibited significant CO<sub>2</sub> fixation through only the rTCA cycle. Under chemolithomixotrophic conditions with acetate, <i>H. thermophilus</i> and <i>T. ammonificans</i> assimilated both CO<sub>2</sub> and acetate via the rTCA cycle. In contrast, acetate suppressed CO<sub>2</sub> fixation through the WL pathway in <i>T. indicus</i> and was used as the primary carbon source under chemolithomixotrophic conditions. These results suggest that the contribution of the WL pathway for CO<sub>2</sub> fixation might be overestimated in ecosystems where acetate is available. Moreover, the present findings indicate that simultaneous CO<sub>2</sub> fixation through both the WL pathway and rTCA cycle in a cell, which has been proposed as a possible metabolic strategy for CO<sub>2</sub>-fixation in ancestral life, is not advantageous in extant microorganisms.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf227"},"PeriodicalIF":6.1,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12743299/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145851786","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-06eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf230
Tristan Cordier, François Keck, Anders Lanzén
Analyzing past ecosystems can improve our understanding of the mechanisms linking biodiversity with environmental changes. Sedimentary ancient DNA (sedaDNA) opens a window to past biodiversity, beyond the fossil record, that can be used to reconstruct ancient environments and ecosystems functions. To this end, modern biodiversity and environmental conditions are used to calibrate transfer functions, that are then applied to past biodiversity data to reconstruct environmental parameters. Doing this with sedaDNA can be challenging, because ancient DNA is often obtained in limited quantities and fragmented into smaller molecules. This leads to noisy datasets, with a low alpha diversity relative to modern DNA, patchy taxa detection patterns and/or skewed relative abundance profiles. How this affects beta-diversity measures, and the performance of transfer functions remain untested. Here we simulated ancient DNA reads counts matrices from synthetic and empirical datasets, and tested 464 combinations of counts transformations (n = 13), beta-diversity indices (n = 16), and ordinations methods (n = 4), and assessed their performance in (i) separating the ecological signal from the noise introduced by DNA degradation and in (ii) predicting ground-truth environmental conditions. Our results show that commonly used workflows in DNA-based community ecology studies are sensitive to the noise associated to ancient DNA signal. Instead, combinations of methods that include more recent ordination methods proved robust to ancient DNA noise and produced better transfer functions. Our study provides a framework for designing postprocessing workflows that are better suited for sedaDNA studies.
{"title":"Benchmarking beta-diversity measures and transfer functions for sedimentary ancient DNA.","authors":"Tristan Cordier, François Keck, Anders Lanzén","doi":"10.1093/ismeco/ycaf230","DOIUrl":"10.1093/ismeco/ycaf230","url":null,"abstract":"<p><p>Analyzing past ecosystems can improve our understanding of the mechanisms linking biodiversity with environmental changes. Sedimentary ancient DNA (<i>sed</i>aDNA) opens a window to past biodiversity, beyond the fossil record, that can be used to reconstruct ancient environments and ecosystems functions. To this end, modern biodiversity and environmental conditions are used to calibrate transfer functions, that are then applied to past biodiversity data to reconstruct environmental parameters. Doing this with <i>sed</i>aDNA can be challenging, because ancient DNA is often obtained in limited quantities and fragmented into smaller molecules. This leads to noisy datasets, with a low alpha diversity relative to modern DNA, patchy taxa detection patterns and/or skewed relative abundance profiles. How this affects beta-diversity measures, and the performance of transfer functions remain untested. Here we simulated ancient DNA reads counts matrices from synthetic and empirical datasets, and tested 464 combinations of counts transformations (n = 13), beta-diversity indices (n = 16), and ordinations methods (n = 4), and assessed their performance in (i) separating the ecological signal from the noise introduced by DNA degradation and in (ii) predicting ground-truth environmental conditions. Our results show that commonly used workflows in DNA-based community ecology studies are sensitive to the noise associated to ancient DNA signal. Instead, combinations of methods that include more recent ordination methods proved robust to ancient DNA noise and produced better transfer functions. Our study provides a framework for designing postprocessing workflows that are better suited for <i>sed</i>aDNA studies.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf230"},"PeriodicalIF":6.1,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753309/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890632","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-12-06eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf231
Yuxin Wang, Justine D M Lejoly, Alejandro Berlinches de Gea, Sven van den Elsen, G F Ciska Veen, Stefan Geisen
Microbial-mediated litter decomposition drives carbon and nutrient cycling. This process can be top-down regulated by microbiome predators, particularly the diverse protists. Size has been suggested to determine predation impacts, but how protists of different size categories affect microbial-mediated litter decomposition remains unknown. Using a litter decomposition experiment with three protist size categories, we investigated protist size-dependent effects on microbial-driven litter decomposition. We found that protists of the large-size category created more structurally similar bacterial communities compared to the no-protist control. These protists of the large size category also reduced litter mass loss by 40%, while increasing microbial respiration by 17% compared to the no-protist control after five weeks of decomposition. In contrast, protists of the small-size category and protists of the medium-size category had no measurable impact on bacterial communities, litter mass loss, or microbial respiration. Random forest analysis identified Streptomyces as a major contributor to litter mass loss (explained 8% of litter mass), while the potential protist symbionts Taonella and Reyranella explained 8% and 6% of microbial respiration, respectively. These likely predation-resistant bacterial taxa were primarily enriched by protists of the large-size category. Our results indicate that protists, especially large ones, can alter litter decomposition by shaping microbiome composition. Future studies on litter decomposition and carbon cycling should incorporate protists and their traits, particularly size, to enhance our understanding of global carbon and nutrient cycling.
{"title":"Protist size-dependent shifts of bacterial communities can reduce litter decomposition.","authors":"Yuxin Wang, Justine D M Lejoly, Alejandro Berlinches de Gea, Sven van den Elsen, G F Ciska Veen, Stefan Geisen","doi":"10.1093/ismeco/ycaf231","DOIUrl":"10.1093/ismeco/ycaf231","url":null,"abstract":"<p><p>Microbial-mediated litter decomposition drives carbon and nutrient cycling. This process can be top-down regulated by microbiome predators, particularly the diverse protists. Size has been suggested to determine predation impacts, but how protists of different size categories affect microbial-mediated litter decomposition remains unknown. Using a litter decomposition experiment with three protist size categories, we investigated protist size-dependent effects on microbial-driven litter decomposition. We found that protists of the large-size category created more structurally similar bacterial communities compared to the no-protist control. These protists of the large size category also reduced litter mass loss by 40%, while increasing microbial respiration by 17% compared to the no-protist control after five weeks of decomposition. In contrast, protists of the small-size category and protists of the medium-size category had no measurable impact on bacterial communities, litter mass loss, or microbial respiration. Random forest analysis identified <i>Streptomyces</i> as a major contributor to litter mass loss (explained 8% of litter mass), while the potential protist symbionts <i>Taonella</i> and <i>Reyranella</i> explained 8% and 6% of microbial respiration, respectively. These likely predation-resistant bacterial taxa were primarily enriched by protists of the large-size category. Our results indicate that protists, especially large ones, can alter litter decomposition by shaping microbiome composition. Future studies on litter decomposition and carbon cycling should incorporate protists and their traits, particularly size, to enhance our understanding of global carbon and nutrient cycling.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf231"},"PeriodicalIF":6.1,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753304/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890680","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Microorganisms associated with insects play crucial roles in mediating the host plant adaptation of their insect hosts. Although oral microbiota are the primary interface with ingested plant material, we still poorly understand their diversity, their function, and their ecological relationship with insect performance. Here, we investigated the diversity and function of the oral microbiota in two generalist lepidopteran pests (Spodoptera litura and Spodoptera frugiperda) feeding across three host plants (bok choy, peanut, and maize). Plant species significantly influenced the diversity and composition of oral microbiota in both S. litura and S. frugiperda. Oral microbial communities from insects feeding on bok choy exhibited significantly higher Sobs richness and Shannon diversity compared to those with peanut or maize plants. Community-level analysis revealed overlapping enriched oral taxa-including Brevibacterium, Staphylococcus, Microbacterium, Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium, Brachybacterium, and Rhodococcus-that were enriched in both insect species when consuming bok choy. In contrast, they accumulated distinct bacterial taxa emerged when feeding on peanut and maize. Microbial ligninolysis capacity within the oral microbiota showed positive associations with leaf lignin content and herbivore performance. This functional trait primarily associated with Brevibacterium and Rhodococcus taxa. Accordingly, two isolated strains, Brevibacterium sedimins OS20 and Rhodococcus sp. OS5 demonstrated effective lignin degradation capacity, achieving 41.01% and 17.62% lignin loss in litter, respectively, after 60 days in microcosm experiments. Overall, host plants shape the diversity and composition of insect oral microbiota. Crucially, microbial ligninolysis capacity and leaf lignin content positively correlated with herbivore performance. This study provides novel insights into the function of oral microbiota in plant-insect interactions, potentially informing the complex multitrophic relationships underlying coevolutionary dynamics.
{"title":"Oral microbiome is related to lepidopteran herbivore performance by lignin degradation.","authors":"Hao-Ran Li, Zhi-Quan Wang, Xiang-Yu Zhang, Yaseen Ullah, Rui Yuan, Jun-Yu Zhao, Xin Xu, Xue Luo, Wei Zhang","doi":"10.1093/ismeco/ycaf229","DOIUrl":"10.1093/ismeco/ycaf229","url":null,"abstract":"<p><p>Microorganisms associated with insects play crucial roles in mediating the host plant adaptation of their insect hosts. Although oral microbiota are the primary interface with ingested plant material, we still poorly understand their diversity, their function, and their ecological relationship with insect performance. Here, we investigated the diversity and function of the oral microbiota in two generalist lepidopteran pests (<i>Spodoptera litura</i> and <i>Spodoptera frugiperda</i>) feeding across three host plants (bok choy, peanut, and maize). Plant species significantly influenced the diversity and composition of oral microbiota in both <i>S. litura</i> and <i>S. frugiperda</i>. Oral microbial communities from insects feeding on bok choy exhibited significantly higher Sobs richness and Shannon diversity compared to those with peanut or maize plants. Community-level analysis revealed overlapping enriched oral taxa-including <i>Brevibacterium, Staphylococcus, Microbacterium, Allorhizobium-Neorhizobium-Pararhizobium-Rhizobium, Brachybacterium</i>, and <i>Rhodococcus</i>-that were enriched in both insect species when consuming bok choy. In contrast, they accumulated distinct bacterial taxa emerged when feeding on peanut and maize. Microbial ligninolysis capacity within the oral microbiota showed positive associations with leaf lignin content and herbivore performance. This functional trait primarily associated with <i>Brevibacterium</i> and <i>Rhodococcus</i> taxa. Accordingly, two isolated strains, <i>Brevibacterium sedimins</i> OS20 and <i>Rhodococcus</i> sp. OS5 demonstrated effective lignin degradation capacity, achieving 41.01% and 17.62% lignin loss in litter, respectively, after 60 days in microcosm experiments. Overall, host plants shape the diversity and composition of insect oral microbiota. Crucially, microbial ligninolysis capacity and leaf lignin content positively correlated with herbivore performance. This study provides novel insights into the function of oral microbiota in plant-insect interactions, potentially informing the complex multitrophic relationships underlying coevolutionary dynamics.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf229"},"PeriodicalIF":6.1,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12753300/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145890699","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Harmful algal blooms negatively impact the ecosystem and fisheries in affected areas. Eutrophication is a major factor contributing to bloom occurrence, and phosphorus is particularly important in limiting the growth of bloom-forming algae. Although algae efficiently utilize orthophosphate (Pi) as a phosphorous source over other molecular forms, Pi is often limited in the marine environment. While uptake and utilization of soluble inorganic and organic phosphorous by bloom-forming algae has been extensively studied, the details of geochemical and biological phosphorous cycling remain to be elucidated. Here, we report for the first time that the bloom-forming alga Heterosigma akashiwo can phagocytose bacteria and grow under phosphate-depleted conditions. The addition of Vibrio comitans to Pi-depleted H. akashiwo enabled the alga propagate to high cell densities, whereas other bacterial strains had only a minor effect. Importantly, V. comitans accumulates polyphosphate-a linear polymer of Pi-at high levels. The extent of algal proliferation induced by the addition of Vibrio species and polyphosphate-accumulating Escherichia coli correlated strongly with their polyphosphate content, indicating that bacterial polyphosphate served as an alternative PO43- source for H. akashiwo. The direct uptake of polyphosphate-accumulating bacteria through algal phagocytosis may represent a novel biological phosphorous-cycling pathway in marine ecosystems. The role of polyphosphate-accumulating marine bacteria as a hidden phosphorous source required for bloom formation warrants further investigation.
{"title":"Proliferation of a bloom-forming phytoplankton via uptake of polyphosphate-accumulating bacteria under phosphate-limiting conditions.","authors":"Seiya Fukuyama, Fumiko Usami, Ryuichi Hirota, Ayano Satoh, Shizuka Ohara, Ken Kondo, Yuki Gomibuchi, Takuo Yasunaga, Toshimitsu Onduka, Akio Kuroda, Kazuhiko Koike, Shoko Ueki","doi":"10.1093/ismeco/ycaf192","DOIUrl":"10.1093/ismeco/ycaf192","url":null,"abstract":"<p><p>Harmful algal blooms negatively impact the ecosystem and fisheries in affected areas. Eutrophication is a major factor contributing to bloom occurrence, and phosphorus is particularly important in limiting the growth of bloom-forming algae. Although algae efficiently utilize orthophosphate (Pi) as a phosphorous source over other molecular forms, Pi is often limited in the marine environment. While uptake and utilization of soluble inorganic and organic phosphorous by bloom-forming algae has been extensively studied, the details of geochemical and biological phosphorous cycling remain to be elucidated. Here, we report for the first time that the bloom-forming alga <i>Heterosigma akashiwo</i> can phagocytose bacteria and grow under phosphate-depleted conditions. The addition of <i>Vibrio comitans</i> to Pi-depleted <i>H. akashiwo</i> enabled the alga propagate to high cell densities, whereas other bacterial strains had only a minor effect. Importantly, <i>V. comitans</i> accumulates polyphosphate-a linear polymer of Pi-at high levels. The extent of algal proliferation induced by the addition of <i>Vibrio</i> species and polyphosphate-accumulating <i>Escherichia coli</i> correlated strongly with their polyphosphate content, indicating that bacterial polyphosphate served as an alternative PO<sub>4</sub> <sup>3-</sup> source for <i>H. akashiwo</i>. The direct uptake of polyphosphate-accumulating bacteria through algal phagocytosis may represent a novel biological phosphorous-cycling pathway in marine ecosystems. The role of polyphosphate-accumulating marine bacteria as a hidden phosphorous source required for bloom formation warrants further investigation.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf192"},"PeriodicalIF":6.1,"publicationDate":"2025-12-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12684721/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145716816","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-11-28eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf224
Alexandre Tronel, Morgane Roger-Margueritat, Caroline Plazy, Salomé Biennier, Anthony Craspay, Ipsita Mohanty, Stéphanie Cools Portier, Manolo Laiola, Guus Roeselers, Nicolas Mathieu, Marianne Hupe, Pieter C Dorrestein, Jean-Pierre Alcaraz, Donald Martin, Philippe Cinquin, Anne-Sophie Silvent, Joris Giai, Marion Proust, Thomas Soranzo, Elena Buelow, Audrey Le Gouellec
Because accessing the small intestine is technically challenging, studies of the small intestinal microbiome are predominantly conducted in patients rather than in healthy individuals. Invasive clinical procedures, such as endoscopy or surgery, usually performed for therapeutic purposes, are typically required for sample collection. Although stomas offer a less invasive means for repeated sampling, their use remains restricted to patient populations. As a result, the small intestinal microbiome of healthy individuals remains largely understudied. This study evaluated a novel ingestible medical device for collecting luminal samples from the small intestine. A monocentric interventional trial (NCT05477069) was conducted on 15 healthy subjects. Metagenomics, metabolomics, and culturomics were used to assess the effectiveness of the medical device in characterizing the healthy small intestinal microbiome and identifying potential biomarkers. The small intestinal microbiota differed significantly from the fecal microbiota, displaying high inter-individual variability, lower species richness and reduced alpha diversity. A combined untargeted and semi-targeted LC-MS/MS metabolomics approach identified a distinct small intestinal metabolic footprint, with bile acids and amino acids being the most abundant metabolite classes. Host- and host/microbe-derived bile acids were particularly abundant in small intestinal samples. Using a fast culturomics approach on two small intestinal samples, we achieved species-level characterization and identified 90 bacterial species, including five potentially novel ones. This study demonstrates the efficacy of our novel sampling device in enabling comprehensive small intestinal microbiome analysis through an integrative, multi-omics approach. This approach allows distinct microbiome signatures to be identified between small intestinal and fecal samples.
{"title":"Exploring the human small intestinal luminal microbiome via a newly developed ingestible sampling device.","authors":"Alexandre Tronel, Morgane Roger-Margueritat, Caroline Plazy, Salomé Biennier, Anthony Craspay, Ipsita Mohanty, Stéphanie Cools Portier, Manolo Laiola, Guus Roeselers, Nicolas Mathieu, Marianne Hupe, Pieter C Dorrestein, Jean-Pierre Alcaraz, Donald Martin, Philippe Cinquin, Anne-Sophie Silvent, Joris Giai, Marion Proust, Thomas Soranzo, Elena Buelow, Audrey Le Gouellec","doi":"10.1093/ismeco/ycaf224","DOIUrl":"10.1093/ismeco/ycaf224","url":null,"abstract":"<p><p>Because accessing the small intestine is technically challenging, studies of the small intestinal microbiome are predominantly conducted in patients rather than in healthy individuals. Invasive clinical procedures, such as endoscopy or surgery, usually performed for therapeutic purposes, are typically required for sample collection. Although stomas offer a less invasive means for repeated sampling, their use remains restricted to patient populations. As a result, the small intestinal microbiome of healthy individuals remains largely understudied. This study evaluated a novel ingestible medical device for collecting luminal samples from the small intestine. A monocentric interventional trial (NCT05477069) was conducted on 15 healthy subjects. Metagenomics, metabolomics, and culturomics were used to assess the effectiveness of the medical device in characterizing the healthy small intestinal microbiome and identifying potential biomarkers. The small intestinal microbiota differed significantly from the fecal microbiota, displaying high inter-individual variability, lower species richness and reduced alpha diversity. A combined untargeted and semi-targeted LC-MS/MS metabolomics approach identified a distinct small intestinal metabolic footprint, with bile acids and amino acids being the most abundant metabolite classes. Host- and host/microbe-derived bile acids were particularly abundant in small intestinal samples. Using a fast culturomics approach on two small intestinal samples, we achieved species-level characterization and identified 90 bacterial species, including five potentially novel ones. This study demonstrates the efficacy of our novel sampling device in enabling comprehensive small intestinal microbiome analysis through an integrative, multi-omics approach. This approach allows distinct microbiome signatures to be identified between small intestinal and fecal samples.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf224"},"PeriodicalIF":6.1,"publicationDate":"2025-11-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12721380/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145822286","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-11-27eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf226
Shrinivas Nandi, Timothy G Stephens, Kasey Walsh, Rebecca García-Camps, Maria F Villalpando, Rita I Sellares-Blasco, Ainhoa L Zubillaga, Aldo Croquer, Debashish Bhattacharya
Stony coral tissue loss disease (SCTLD) is a rapidly spreading lethal coral disease, the etiology of which remains poorly understood. In this study, using deep metagenomic sequencing, we investigated microbial and viral community dynamics associated with SCTLD progression in the Caribbean stony coral Diploria labyrinthiformis. We assembled 264 metagenome-assembled genomes and correlated their abundance with disease phenotypes, which revealed significant shifts in both the prokaryotic microbiome and virome. Our results provide clear evidence of microbial destabilization in diseased corals, suggesting that microbial dysbiosis is an outcome of SCTLD progression. We identified DNA viruses in our dataset that increase in abundance in SCTLD-affected corals and are present in existing coral data from other Caribbean regions. In addition, we identified the first putative instance of asymptomatic/resistant SCTLD-affected corals. These are apparently healthy colonies that share the viral profile of diseased individuals. However, these colonies contain a different prokaryotic microbiome than do diseased corals, suggesting microbe-induced resilience (i.e. beneficial microbiome) to SCTLD. Finally, utilizing differential abundance analysis and gene inventories, we propose a mechanistic model of SCTLD progression, in which viral dynamics may contribute to microbiome collapse. These findings provide novel insights into SCTLD pathogenesis and offer consistent molecular signals of disease across diverse geographic sites, presenting new opportunities for disease monitoring and mitigation.
{"title":"Shifts in the microbiome and virome are associated with stony coral tissue loss disease (SCTLD).","authors":"Shrinivas Nandi, Timothy G Stephens, Kasey Walsh, Rebecca García-Camps, Maria F Villalpando, Rita I Sellares-Blasco, Ainhoa L Zubillaga, Aldo Croquer, Debashish Bhattacharya","doi":"10.1093/ismeco/ycaf226","DOIUrl":"10.1093/ismeco/ycaf226","url":null,"abstract":"<p><p>Stony coral tissue loss disease (SCTLD) is a rapidly spreading lethal coral disease, the etiology of which remains poorly understood. In this study, using deep metagenomic sequencing, we investigated microbial and viral community dynamics associated with SCTLD progression in the Caribbean stony coral <i>Diploria labyrinthiformis</i>. We assembled 264 metagenome-assembled genomes and correlated their abundance with disease phenotypes, which revealed significant shifts in both the prokaryotic microbiome and virome. Our results provide clear evidence of microbial destabilization in diseased corals, suggesting that microbial dysbiosis is an outcome of SCTLD progression. We identified DNA viruses in our dataset that increase in abundance in SCTLD-affected corals and are present in existing coral data from other Caribbean regions. In addition, we identified the first putative instance of asymptomatic/resistant SCTLD-affected corals. These are apparently healthy colonies that share the viral profile of diseased individuals. However, these colonies contain a different prokaryotic microbiome than do diseased corals, suggesting microbe-induced resilience (i.e. beneficial microbiome) to SCTLD. Finally, utilizing differential abundance analysis and gene inventories, we propose a mechanistic model of SCTLD progression, in which viral dynamics may contribute to microbiome collapse. These findings provide novel insights into SCTLD pathogenesis and offer consistent molecular signals of disease across diverse geographic sites, presenting new opportunities for disease monitoring and mitigation.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf226"},"PeriodicalIF":6.1,"publicationDate":"2025-11-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12743298/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145851770","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}