Plants and microbes use many strategies to acquire soil amino acids. Recent findings suggest that genes related to amino acid metabolism and transport are influenced by plant miRNAs. Here, we first show that Arabidopsis modifies its root miRNA content when fertilized with a mixture of 17 amino acids. The miRNAs that responded to amino acid fertilization and other rhizosphere-abundant miRNAs were applied to a simplified soil community, grown with diverse amino acid sources, to test if they interfered with microbial community growth, community composition, and amino acid consumption. Plant miRNAs affected the community's growth in over 70% of the amino acid sources. The impact of plant miRNAs also depended on the N source supplied to the microbial community, with the strongest effect observed with L-lysine. Specifically, ath-miR159a reduced the microbial consumption of L-lysine, further supporting that plant miRNAs can influence microbial amino acid uptake. Plant miRNAs also strongly affected the relative abundance of specific bacterial taxa, which we subsequently isolated. These community shifts were explained by the subtle but robust impact of plant miRNAs on isolates' growth and, for two out of three isolates, on amino acid consumption. Surprisingly, while plant miRNAs inhibited amino acid consumption at both the community and isolate levels, the effects of plant miRNAs were mostly positive. Our results suggest that rhizospheric plant miRNAs might have a role in modulating the amino acid consumption of soil bacteria which reshapes the community, but not necessarily in a competitive framework.
{"title":"Plant miRNAs influence soil bacterial growth and amino acid uptake, restructuring community composition.","authors":"Jessica A Dozois, Marc-Antoine Duchesne, Katel Hallaf, Julien Tremblay, Étienne Yergeau","doi":"10.1093/ismeco/ycaf206","DOIUrl":"https://doi.org/10.1093/ismeco/ycaf206","url":null,"abstract":"<p><p>Plants and microbes use many strategies to acquire soil amino acids. Recent findings suggest that genes related to amino acid metabolism and transport are influenced by plant miRNAs. Here, we first show that <i>Arabidopsis</i> modifies its root miRNA content when fertilized with a mixture of 17 amino acids. The miRNAs that responded to amino acid fertilization and other rhizosphere-abundant miRNAs were applied to a simplified soil community, grown with diverse amino acid sources, to test if they interfered with microbial community growth, community composition, and amino acid consumption. Plant miRNAs affected the community's growth in over 70% of the amino acid sources. The impact of plant miRNAs also depended on the N source supplied to the microbial community, with the strongest effect observed with L-lysine. Specifically, ath-miR159a reduced the microbial consumption of L-lysine, further supporting that plant miRNAs can influence microbial amino acid uptake. Plant miRNAs also strongly affected the relative abundance of specific bacterial taxa, which we subsequently isolated. These community shifts were explained by the subtle but robust impact of plant miRNAs on isolates' growth and, for two out of three isolates, on amino acid consumption. Surprisingly, while plant miRNAs inhibited amino acid consumption at both the community and isolate levels, the effects of plant miRNAs were mostly positive. Our results suggest that rhizospheric plant miRNAs might have a role in modulating the amino acid consumption of soil bacteria which reshapes the community, but not necessarily in a competitive framework.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf206"},"PeriodicalIF":6.1,"publicationDate":"2025-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12648395/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145643486","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 : 2025-11-07eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf186
Selina Lepori, Nadja Rohner, Xingqi Li, Xiaojuan Feng, Rota Wagai, Viviana Loaiza, David Sebag, Eric Verrecchia, Daniel B Nelson, Ansgar Kahmen, Claire Chenu, Pascal A Niklaus, Anna-Liisa Laine, Luiz A Domeignoz-Horta
Multiple global change drivers have caused a large carbon (C) debt in our soils. To remedy this debt, understanding the role of microorganisms in soil C cycling is crucial to tackle the C soil loss. Microbial carbon use efficiency (CUE) is a parameter that captures the formation of microbially-derived soil organic matter (SOM). While it is known that biotic and abiotic drivers influence CUE, it remains unclear whether bacteria, fungi and their interactions influence the formation of microbially-derived SOC and its persistence in soils. Here, we combined the inoculation of distinct communities (a biotic factor) grown at different moisture levels (an abiotic factor) to manipulate the formation of microbial necromass in a model soil. In a follow-up experiment, we then evaluated the persistence of this previously formed microbially-derived C to decomposition. While we show that necromass formation reflects the microbial community composition, the SOC formed within the most complex community of bacteria and fungi seems to be more resistant to decomposition compared to the SOC formed within the simpler communities (bacteria and fungi simple community, bacteria only and fungi only communities). Moreover, fungal necromass proved to be more thermally-stable than bacterial necromass, if this necromass is formed with both bacteria and fungi present. Our findings reveal that although abiotic factors can influence microbial physiology, the biological origin of microbially-derived C and the co-occurrence of fungal and bacterial growth were the stronger drivers explaining SOM persistence in these soils, suggesting the importance of microbial succession in SOC stabilization.
{"title":"Who is who in necromass formation and stabilization in soil? The role of fungi and bacteria as complementary players of biogeochemical functioning.","authors":"Selina Lepori, Nadja Rohner, Xingqi Li, Xiaojuan Feng, Rota Wagai, Viviana Loaiza, David Sebag, Eric Verrecchia, Daniel B Nelson, Ansgar Kahmen, Claire Chenu, Pascal A Niklaus, Anna-Liisa Laine, Luiz A Domeignoz-Horta","doi":"10.1093/ismeco/ycaf186","DOIUrl":"10.1093/ismeco/ycaf186","url":null,"abstract":"<p><p>Multiple global change drivers have caused a large carbon (C) debt in our soils. To remedy this debt, understanding the role of microorganisms in soil C cycling is crucial to tackle the C soil loss. Microbial carbon use efficiency (CUE) is a parameter that captures the formation of microbially-derived soil organic matter (SOM). While it is known that biotic and abiotic drivers influence CUE, it remains unclear whether bacteria, fungi and their interactions influence the formation of microbially-derived SOC and its persistence in soils. Here, we combined the inoculation of distinct communities (a biotic factor) grown at different moisture levels (an abiotic factor) to manipulate the formation of microbial necromass in a model soil. In a follow-up experiment, we then evaluated the persistence of this previously formed microbially-derived C to decomposition. While we show that necromass formation reflects the microbial community composition, the SOC formed within the most complex community of bacteria and fungi seems to be more resistant to decomposition compared to the SOC formed within the simpler communities (bacteria and fungi simple community, bacteria only and fungi only communities). Moreover, fungal necromass proved to be more thermally-stable than bacterial necromass, if this necromass is formed with both bacteria and fungi present. Our findings reveal that although abiotic factors can influence microbial physiology, the biological origin of microbially-derived C and the co-occurrence of fungal and bacterial growth were the stronger drivers explaining SOM persistence in these soils, suggesting the importance of microbial succession in SOC stabilization.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf186"},"PeriodicalIF":6.1,"publicationDate":"2025-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12642871/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145607931","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 : 2025-11-06eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf203
Yujun Zhong, Yingyue Zhang, José Luis López Arcondo, Ruoyi Xu, Mark Radosevich, Jeffery L Dangl, Bas E Dutilh, Xiaolong Liang
Bacteriophages, lytic or lysogenic, play critical roles in structuring different soil bacteriomes and driving their functionality. Lysogeny is favored in the plant rhizosphere and may play a major role in plant-rhizobacteria assembly and function. However, the ecological footprint and consequence of prophage activity in the rhizosphere are poorly understood. Here, we conducted a 35-day pot experiment to examine how prophage induction influences soybean rhizosphere viromes and bacterial communities, along with associated changes in nutrient cycling and plant development. The results showed that mitomycin C-induced prophage induction triggered immense viral production, altering virome structure-with more observed species richness in the rhizosphere. We observed a greater impact on the rhizosphere virome than on the bulk soil virome. The resulting lysis decreased the soil organic matter content but significantly increased dissolved organic carbon and nitrate contents in the soil, which improved soil nutrient conditions and stimulated soybean root development. Prophage induction markedly influenced the rhizobacterial community structure, resulting in reduced community diversity. The enrichment of fast-growing bacterial populations was stimulated, suggesting that viral lysis increased microbial activities and accelerated nutrient turnover. The bacterial interaction network was drastically shifted, with complexity being decreased in the bulk soil and increased in the rhizosphere, potentially stimulating the differentiation of the bacterial communities. Together, our results demonstrated that induction of prophages can cause extensive nutrient turnover and variations in plant-rhizobacteria interactions, driving the rhizobacterial community assembly process. This study provides novel insights into the mechanisms of phages controlling microbial function in primary production and soil carbon storage by modulating microbial traits (e.g., carbon use efficiency, growth rate, death, and community assembly) and via processes like the viral shunt.
{"title":"Prophage induction drives soybean rhizobacterial community differentiation and nutrient cycling benefiting root development.","authors":"Yujun Zhong, Yingyue Zhang, José Luis López Arcondo, Ruoyi Xu, Mark Radosevich, Jeffery L Dangl, Bas E Dutilh, Xiaolong Liang","doi":"10.1093/ismeco/ycaf203","DOIUrl":"https://doi.org/10.1093/ismeco/ycaf203","url":null,"abstract":"<p><p>Bacteriophages, lytic or lysogenic, play critical roles in structuring different soil bacteriomes and driving their functionality. Lysogeny is favored in the plant rhizosphere and may play a major role in plant-rhizobacteria assembly and function. However, the ecological footprint and consequence of prophage activity in the rhizosphere are poorly understood. Here, we conducted a 35-day pot experiment to examine how prophage induction influences soybean rhizosphere viromes and bacterial communities, along with associated changes in nutrient cycling and plant development. The results showed that mitomycin C-induced prophage induction triggered immense viral production, altering virome structure-with more observed species richness in the rhizosphere. We observed a greater impact on the rhizosphere virome than on the bulk soil virome. The resulting lysis decreased the soil organic matter content but significantly increased dissolved organic carbon and nitrate contents in the soil, which improved soil nutrient conditions and stimulated soybean root development. Prophage induction markedly influenced the rhizobacterial community structure, resulting in reduced community diversity. The enrichment of fast-growing bacterial populations was stimulated, suggesting that viral lysis increased microbial activities and accelerated nutrient turnover. The bacterial interaction network was drastically shifted, with complexity being decreased in the bulk soil and increased in the rhizosphere, potentially stimulating the differentiation of the bacterial communities. Together, our results demonstrated that induction of prophages can cause extensive nutrient turnover and variations in plant-rhizobacteria interactions, driving the rhizobacterial community assembly process. This study provides novel insights into the mechanisms of phages controlling microbial function in primary production and soil carbon storage by modulating microbial traits (e.g., carbon use efficiency, growth rate, death, and community assembly) and via processes like the viral shunt.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf203"},"PeriodicalIF":6.1,"publicationDate":"2025-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12645843/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145643479","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 : 2025-11-04eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf199
Lucas Horstmann, Daniel Lipus, Alexander Bartholomäus, Romulo Oses, Axel Kitte, Thomas Friedl, Dirk Wagner
Subsurface microorganisms face extreme challenges such as anoxic, xeric, and oligotrophic conditions. In igneous systems, nutrient limitation is critical, as biomass input relies on surface-derived fluids via tectonic fractures. Despite growing interest in subsurface habitats, little is known about ecosystems beneath arid landscapes, where surface water input is limited by the low annual precipitation. This study compares granitic subsurface environments beneath arid and humid surface ecosystems, highlighting the link between surface climate and subsurface biodiversity. DNA was extracted from granitic subsurface rocks recovered from two endmember sites along a north-south climate gradient in Chile's Coastal Cordillera. Microbial communities inhabiting down to 55 m deep subsurface rocks were characterized using 16S rRNA amplicon and shotgun metagenomic sequencing. We identified an abundant and potentially active subsurface community below both climates dominated by heterotrophic bacteria, including Pseudarthrobacter, Janthinobacterium, and Pseudomonas. However, rare taxa affiliated with common chemolithoautrophs, e.g. Thiobacillus, Sulfuriferula, and Sulfuricurvum, were only observed in the arid subsurface, indicating increased oligotrophic conditions and reliance on inorganic electron donors in the deeper subsurface of the desert. Functional analysis revealed sulphur, hydrogen, and carbon monoxide as potential inorganic electron donors. These findings expand the current understanding of microbial life in the subsurface of granite rocks showing the influence of surface climate on nutrient conditions in the deeper subsurface, providing new insights into the extent and functional capacity of terrestrial subsurface habitats and their role in global biogeochemical processes.
{"title":"Microbial ecology of subsurface granitic bedrock: a humid-arid site comparison in Chile.","authors":"Lucas Horstmann, Daniel Lipus, Alexander Bartholomäus, Romulo Oses, Axel Kitte, Thomas Friedl, Dirk Wagner","doi":"10.1093/ismeco/ycaf199","DOIUrl":"10.1093/ismeco/ycaf199","url":null,"abstract":"<p><p>Subsurface microorganisms face extreme challenges such as anoxic, xeric, and oligotrophic conditions. In igneous systems, nutrient limitation is critical, as biomass input relies on surface-derived fluids via tectonic fractures. Despite growing interest in subsurface habitats, little is known about ecosystems beneath arid landscapes, where surface water input is limited by the low annual precipitation. This study compares granitic subsurface environments beneath arid and humid surface ecosystems, highlighting the link between surface climate and subsurface biodiversity. DNA was extracted from granitic subsurface rocks recovered from two endmember sites along a north-south climate gradient in Chile's Coastal Cordillera. Microbial communities inhabiting down to 55 m deep subsurface rocks were characterized using 16S rRNA amplicon and shotgun metagenomic sequencing. We identified an abundant and potentially active subsurface community below both climates dominated by heterotrophic bacteria, including <i>Pseudarthrobacter</i>, <i>Janthinobacterium</i>, and <i>Pseudomonas.</i> However, rare taxa affiliated with common chemolithoautrophs, e.g. <i>Thiobacillus</i>, <i>Sulfuriferula</i>, and <i>Sulfuricurvum</i>, were only observed in the arid subsurface, indicating increased oligotrophic conditions and reliance on inorganic electron donors in the deeper subsurface of the desert. Functional analysis revealed sulphur, hydrogen, and carbon monoxide as potential inorganic electron donors. These findings expand the current understanding of microbial life in the subsurface of granite rocks showing the influence of surface climate on nutrient conditions in the deeper subsurface, providing new insights into the extent and functional capacity of terrestrial subsurface habitats and their role in global biogeochemical processes.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf199"},"PeriodicalIF":6.1,"publicationDate":"2025-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12663961/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145650178","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 : 2025-11-04eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf191
Su Ding, Nicole J Bale, Anna Cutmore, F A Bastiaan von Meijenfeldt, Stefan Schouten, Jaap S Sinninghe Damsté
The sedimentary lipid pool is comprised of a myriad of individual components. Due to their importance for organic carbon sequestration and their application in paleoclimatic and geobiological reconstructions, its composition has been studied for many decades with targeted approaches but an overall view on its composition is still lacking. In part this uncertainty relates to the different sources of sedimentary lipids, they can be both delivered from the overlying water column by sedimentation, but also produced in situ by sediment dwelling organisms. Another uncertainty relates to the differing degree of preservation, both between lipid groups and relative to other organic matters. Here we conduct an untargeted analysis of the sedimentary lipidome in the Black Sea using ultra high-pressure liquid chromatography coupled with high-resolution tandem mass spectrometry (UHPLC-HRMS2). Besides commonly reported phytoplankton-derived fossil lipids, a diverse and abundant set of sphingolipids was discovered, accounting for ~20% of the sedimentary lipidome. We hypothesize that these sphingolipids are produced in situ by sedimentary anaerobic bacteria, which likely use sphingolipids instead of phospholipids, probably because phospholipids are preferentially utilized in the uppermost layers of the anoxic sediments. Our results suggest that while phytoplankton-derived lipids contribute 50%-60% of the sedimentary lipidome, the importance of bacterial lipids, particularly in situ produced sphingolipids, may have been overlooked.
{"title":"Substantial contribution of <i>in situ</i> produced bacterial lipids to the sedimentary lipidome.","authors":"Su Ding, Nicole J Bale, Anna Cutmore, F A Bastiaan von Meijenfeldt, Stefan Schouten, Jaap S Sinninghe Damsté","doi":"10.1093/ismeco/ycaf191","DOIUrl":"10.1093/ismeco/ycaf191","url":null,"abstract":"<p><p>The sedimentary lipid pool is comprised of a myriad of individual components. Due to their importance for organic carbon sequestration and their application in paleoclimatic and geobiological reconstructions, its composition has been studied for many decades with targeted approaches but an overall view on its composition is still lacking. In part this uncertainty relates to the different sources of sedimentary lipids, they can be both delivered from the overlying water column by sedimentation, but also produced <i>in situ</i> by sediment dwelling organisms. Another uncertainty relates to the differing degree of preservation, both between lipid groups and relative to other organic matters. Here we conduct an untargeted analysis of the sedimentary lipidome in the Black Sea using ultra high-pressure liquid chromatography coupled with high-resolution tandem mass spectrometry (UHPLC-HRMS<sup>2</sup>). Besides commonly reported phytoplankton-derived fossil lipids, a diverse and abundant set of sphingolipids was discovered, accounting for ~20% of the sedimentary lipidome. We hypothesize that these sphingolipids are produced <i>in situ</i> by sedimentary anaerobic bacteria, which likely use sphingolipids instead of phospholipids, probably because phospholipids are preferentially utilized in the uppermost layers of the anoxic sediments. Our results suggest that while phytoplankton-derived lipids contribute 50%-60% of the sedimentary lipidome, the importance of bacterial lipids, particularly <i>in situ</i> produced sphingolipids, may have been overlooked.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf191"},"PeriodicalIF":6.1,"publicationDate":"2025-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12619533/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145544148","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 : 2025-11-03eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf196
Dhiraj Paul, Inga Paasisalo, Anuliina Putkinen, Christopher M Jones, Lukas Kohl, Sara Hallin, Mari Pihlatie, Henri M P Siljanen
Current climate change assessments and greenhouse gas flux models often lack information on the microbiological processes that consume atmospheric nitrous oxide (N2O), a potent greenhouse gas. There is limited understanding of phyllospheric microorganisms controlling N2O exchange. In this study, we determined the microbial potential for N2O consumption in aboveground vegetation in boreal forests. For this, we collected shoot samples from upland spruce forests in Finland and used a novel targeted metagenomics approach with a hybridization capture of gene-specific probes. Most of the samples contained nosZ genes, encoding the N2O reductase. Phylogenetic placement showed a significantly higher relative abundance (P < .01) of nosZ Clade I than nosZ Clade II. Bacterial members such as Comamonadaceae, Hydrogenophaga, and Paracoccus, which all harbor nosZ Clade I, were found in high relative abundance in the spruce shoots across the sites, suggesting they play a role in N2O consumption capabilities in the spruce phyllosphere. Anoxic incubations, utilizing gas chromatography for N2O analyses, showed potential N2O consumption activity across the spruce samples. The presence of nirK and nirS suggests potential for denitrification, possibly resulting in N2O production. Our finding provides evidence of microbial communities in spruce canopies with potential for N2O exchange. Given the vast coverage of boreal forests globally, understanding the role of phyllospheric microorganisms in N₂O exchange is crucial for improving the accuracy of greenhouse gas models and enhancing climate prediction reliability.
{"title":"Microorganisms in the phyllosphere of Norway spruce controlling nitrous oxide dynamics.","authors":"Dhiraj Paul, Inga Paasisalo, Anuliina Putkinen, Christopher M Jones, Lukas Kohl, Sara Hallin, Mari Pihlatie, Henri M P Siljanen","doi":"10.1093/ismeco/ycaf196","DOIUrl":"10.1093/ismeco/ycaf196","url":null,"abstract":"<p><p>Current climate change assessments and greenhouse gas flux models often lack information on the microbiological processes that consume atmospheric nitrous oxide (N<sub>2</sub>O), a potent greenhouse gas. There is limited understanding of phyllospheric microorganisms controlling N<sub>2</sub>O exchange. In this study, we determined the microbial potential for N<sub>2</sub>O consumption in aboveground vegetation in boreal forests. For this, we collected shoot samples from upland spruce forests in Finland and used a novel targeted metagenomics approach with a hybridization capture of gene-specific probes. Most of the samples contained <i>nos</i>Z genes, encoding the N<sub>2</sub>O reductase. Phylogenetic placement showed a significantly higher relative abundance (<i>P</i> < .01) of <i>nos</i>Z Clade I than <i>nos</i>Z Clade II. Bacterial members such as Comamonadaceae, <i>Hydrogenophaga</i>, and <i>Paracoccus</i>, which all harbor <i>nos</i>Z Clade I, were found in high relative abundance in the spruce shoots across the sites, suggesting they play a role in N<sub>2</sub>O consumption capabilities in the spruce phyllosphere. Anoxic incubations, utilizing gas chromatography for N<sub>2</sub>O analyses, showed potential N<sub>2</sub>O consumption activity across the spruce samples. The presence of <i>nir</i>K and <i>nir</i>S suggests potential for denitrification, possibly resulting in N<sub>2</sub>O production. Our finding provides evidence of microbial communities in spruce canopies with potential for N<sub>2</sub>O exchange. Given the vast coverage of boreal forests globally, understanding the role of phyllospheric microorganisms in N₂O exchange is crucial for improving the accuracy of greenhouse gas models and enhancing climate prediction reliability.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf196"},"PeriodicalIF":6.1,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12642870/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145607917","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 : 2025-11-03eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf200
Domitille Jarrige, Jonathan M Vyskocil, Muriel Joly, Binta Dieme, Marie Lagrée, Emilie E L Muller, Pierre Amato, Françoise Bringel
Microorganisms maintain metabolic activity in clouds, with recognized impacts on the chemistry of small organic compounds, radicals, and their precursors. However, how microbial activity is modulated by cloud environmental variables remains unknown. Here we explored the metabolic response of an assemblage of representative microbial isolates from cloud water, composed of a basidiomycetous yeast (Dioszegia hungarica) and three bacterial strains (Rhodococcus enclensis, Pseudomonas syringae, and Pseudomonas graminis), in synthetic cloud water exposed to contrasted conditions of temperature (5°C vs 17°C), light (dark vs artificial solar light) and oxidants (0 μM vs 250 μM H2O2), to mimic typical cloud conditions during winter night and summer day. Metabolomics and metatranscriptomics allowed the identification of 25 differentially abundant metabolites and 218 differentially expressed genes (DEGs). Both summer day metabolomes and metatranscriptomes suggested active mitochondria-driven energy production, with fungal DEGs involved in fatty acids biosynthesis and succinate assimilation, and three differentially abundant acylcarnitines that support fatty acid transport into the mitochondrion for oxidative phosphorylation. In contrast, bacteria displayed DEGs for cell division arrest and components of reactive oxygen species scavenging systems. Under the winter night condition, both bacteria and yeast exhibited a similar prosperous state with DEGs encoding translation, protein repair and turnover, as well as cell cycle related functions. Thus, eukaryotes and prokaryotes may engage in distinct strategies to survive in clouds, depending on environmental conditions. This study consolidates our understanding of microbial roles and interactions in cloud water, paving the way for deeper insights into the chemistry of atmospheric systems.
微生物在云中维持代谢活动,对小有机化合物、自由基及其前体的化学影响是公认的。然而,微生物活动如何被云环境变量调节仍然未知。本文研究了由担子菌酵母(Dioszegia hungarica)和三种细菌菌株(荚膜红球菌、丁香假单胞菌和禾草假单胞菌)组成的代表性云水微生物分离物在不同温度(5°C vs 17°C)、光照(黑暗vs人工日光)和氧化剂(0 μM vs 250 μM H2O2)条件下的代谢反应。模拟冬季夜晚和夏季白天的典型云况。代谢组学和亚转录组学鉴定出25种差异丰富的代谢物和218种差异表达基因(DEGs)。夏季代谢组和亚转录组都表明,真菌的deg参与脂肪酸的生物合成和琥珀酸盐的同化,并且三种不同丰度的酰基肉碱支持脂肪酸转运到线粒体进行氧化磷酸化。相比之下,细菌显示了用于细胞分裂的DEGs和活性氧清除系统的成分。在冬夜条件下,细菌和酵母都表现出相似的繁荣状态,它们都有编码翻译、蛋白质修复和周转以及细胞周期相关功能的DEGs。因此,真核生物和原核生物可能采取不同的策略在云中生存,这取决于环境条件。这项研究巩固了我们对云水中微生物作用和相互作用的理解,为深入了解大气系统的化学成分铺平了道路。
{"title":"Multi-kingdom microbial assemblage modulates its metabolism under contrasted cloud conditions.","authors":"Domitille Jarrige, Jonathan M Vyskocil, Muriel Joly, Binta Dieme, Marie Lagrée, Emilie E L Muller, Pierre Amato, Françoise Bringel","doi":"10.1093/ismeco/ycaf200","DOIUrl":"10.1093/ismeco/ycaf200","url":null,"abstract":"<p><p>Microorganisms maintain metabolic activity in clouds, with recognized impacts on the chemistry of small organic compounds, radicals, and their precursors. However, how microbial activity is modulated by cloud environmental variables remains unknown. Here we explored the metabolic response of an assemblage of representative microbial isolates from cloud water, composed of a basidiomycetous yeast (<i>Dioszegia hungarica</i>) and three bacterial strains (<i>Rhodococcus enclensis</i>, <i>Pseudomonas syringae</i>, and <i>Pseudomonas graminis</i>), in synthetic cloud water exposed to contrasted conditions of temperature (5°C vs 17°C), light (dark vs artificial solar light) and oxidants (0 μM vs 250 μM H<sub>2</sub>O<sub>2</sub>), to mimic typical cloud conditions during winter night and summer day. Metabolomics and metatranscriptomics allowed the identification of 25 differentially abundant metabolites and 218 differentially expressed genes (DEGs). Both summer day metabolomes and metatranscriptomes suggested active mitochondria-driven energy production, with fungal DEGs involved in fatty acids biosynthesis and succinate assimilation, and three differentially abundant acylcarnitines that support fatty acid transport into the mitochondrion for oxidative phosphorylation. In contrast, bacteria displayed DEGs for cell division arrest and components of reactive oxygen species scavenging systems. Under the winter night condition, both bacteria and yeast exhibited a similar prosperous state with DEGs encoding translation, protein repair and turnover, as well as cell cycle related functions. Thus, eukaryotes and prokaryotes may engage in distinct strategies to survive in clouds, depending on environmental conditions. This study consolidates our understanding of microbial roles and interactions in cloud water, paving the way for deeper insights into the chemistry of atmospheric systems.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf200"},"PeriodicalIF":6.1,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12721874/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145822240","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 : 2025-11-01eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf183
Henri M P Siljanen, Lokeshwaran Manoharan, Angus S Hilts, Alexandre Bagnoud, Ricardo J E Alves, Christopher M Jones, Melina Kerou, Felipa L Sousa, Sara Hallin, Christina Biasi, Christa Schleper
Microorganisms are key players in the global cycling of nitrogen and carbon, controlling their availability and fluxes, including the emissions of the powerful greenhouse gases nitrous oxide and methane. Standard sequencing methods often reveal only a limited fraction of their diversity, because of their low relative abundance, the insufficient sequencing depth of traditional metagenomes of complex communities, and limitations in coverage of DNA amplification-based assays. Here, we developed and tested a targeted metagenomics approach based on probe capture and hybridization to simultaneously characterize the diversity of multiple key metabolic genes involved in inorganic nitrogen and methane cycling. We designed comprehensive probe libraries for each of the 14 target marker genes comprising 264 111 unique probes. In validation experiments with mock communities, targeted metagenomics yielded gene profiles similar to the original communities. Only GC content had a small effect on probe efficiency, as low GC targets were less efficiently detected than those with high GC, within the mock communities. Furthermore, the relative abundances of the marker genes obtained using targeted or traditional shotgun metagenomics were significantly correlated. In addition, using archaeal amoA genes as a case-study, targeted metagenomics identified a substantially higher taxonomic diversity and a larger number of sequence reads per sample, yielding diversity estimates 28 or 1.24 times higher than shotgun metagenomics or amplicon sequencing, respectively. Our results show that targeted metagenomics complements current approaches to characterize key microbial populations and functional guilds in biogeochemical cycles in different ecosystems, enabling more detailed, simultaneous characterization of multiple functional genes.
{"title":"Targeted metagenomics using probe capture detect a larger diversity of nitrogen and methane cycling genes in complex microbial communities than traditional metagenomics.","authors":"Henri M P Siljanen, Lokeshwaran Manoharan, Angus S Hilts, Alexandre Bagnoud, Ricardo J E Alves, Christopher M Jones, Melina Kerou, Felipa L Sousa, Sara Hallin, Christina Biasi, Christa Schleper","doi":"10.1093/ismeco/ycaf183","DOIUrl":"10.1093/ismeco/ycaf183","url":null,"abstract":"<p><p>Microorganisms are key players in the global cycling of nitrogen and carbon, controlling their availability and fluxes, including the emissions of the powerful greenhouse gases nitrous oxide and methane. Standard sequencing methods often reveal only a limited fraction of their diversity, because of their low relative abundance, the insufficient sequencing depth of traditional metagenomes of complex communities, and limitations in coverage of DNA amplification-based assays. Here, we developed and tested a targeted metagenomics approach based on probe capture and hybridization to simultaneously characterize the diversity of multiple key metabolic genes involved in inorganic nitrogen and methane cycling. We designed comprehensive probe libraries for each of the 14 target marker genes comprising 264 111 unique probes. In validation experiments with mock communities, targeted metagenomics yielded gene profiles similar to the original communities. Only GC content had a small effect on probe efficiency, as low GC targets were less efficiently detected than those with high GC, within the mock communities. Furthermore, the relative abundances of the marker genes obtained using targeted or traditional shotgun metagenomics were significantly correlated. In addition, using archaeal <i>amoA</i> genes as a case-study, targeted metagenomics identified a substantially higher taxonomic diversity and a larger number of sequence reads per sample, yielding diversity estimates 28 or 1.24 times higher than shotgun metagenomics or amplicon sequencing, respectively. Our results show that targeted metagenomics complements current approaches to characterize key microbial populations and functional guilds in biogeochemical cycles in different ecosystems, enabling more detailed, simultaneous characterization of multiple functional genes.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf183"},"PeriodicalIF":6.1,"publicationDate":"2025-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12598625/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145497703","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 : 2025-10-29eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf197
Chance J English, Meenakshi Manoj, Lillian C Henderson, Keri Opalk, Craig A Carlson
A large amount of a photoautotroph's fixed carbon is released as dissolved organic matter, from both exudation and solubilized detritus. This dissolved material contributes to a surface mucilage layer that shapes their immediate environment, including the composition of their microbiome. Here we evaluated the microbiome and mucilage carbohydrate composition of Macrocystis pyrifera (giant kelp), a globally distributed foundation species, in response to seasonal nutrient availability and developmental stage. We combine 16S rRNA amplicon analysis of the giant kelp microbiome with carbohydrate monomer analysis of kelp mucilage to examine microbe-mucilage relationships. We found significant differences in the microbiome and mucilage composition between seasons and developmental stages of giant kelp. Higher tissue-nitrogen content in the spring coincided with elevated amounts of glucosamine, a nitrogen-containing sugar, in giant kelp mucilage, while senescence led to the release of mannuronic acid, an alginate indicator. The release of glucosamine and fucose-rich mucilage was correlated with an increase in the relative abundance of bacteria within the Planctomycetota phylum, whereas mannuronic acid-rich mucilage coincided with an increase in the relative abundance of members of the Flavobacteriia and Gammaproteobacteria lineages. We investigated putative carbohydrate-microbe relationships by isolating a member of the Planctomycetota phylum from the surface of giant kelp. Using whole genome analysis and growth assays, we demonstrate that this isolate grows on fucoidan and N-acetyl glucosamine, but not alginate, consistent with the observed relative abundance of this clade in the kelp microbiome in response to variable mucilage carbohydrate content. This suggests a key role of kelp mucilage carbohydrate composition in structuring its microbiome as has been observed for other organisms such as corals and within the human gut.
{"title":"Seasonal and developmental stage changes in mucilage carbohydrate content shape the kelp microbiome.","authors":"Chance J English, Meenakshi Manoj, Lillian C Henderson, Keri Opalk, Craig A Carlson","doi":"10.1093/ismeco/ycaf197","DOIUrl":"10.1093/ismeco/ycaf197","url":null,"abstract":"<p><p>A large amount of a photoautotroph's fixed carbon is released as dissolved organic matter, from both exudation and solubilized detritus. This dissolved material contributes to a surface mucilage layer that shapes their immediate environment, including the composition of their microbiome. Here we evaluated the microbiome and mucilage carbohydrate composition of <i>Macrocystis pyrifera</i> (giant kelp), a globally distributed foundation species, in response to seasonal nutrient availability and developmental stage. We combine 16S rRNA amplicon analysis of the giant kelp microbiome with carbohydrate monomer analysis of kelp mucilage to examine microbe-mucilage relationships. We found significant differences in the microbiome and mucilage composition between seasons and developmental stages of giant kelp. Higher tissue-nitrogen content in the spring coincided with elevated amounts of glucosamine, a nitrogen-containing sugar, in giant kelp mucilage, while senescence led to the release of mannuronic acid, an alginate indicator. The release of glucosamine and fucose-rich mucilage was correlated with an increase in the relative abundance of bacteria within the Planctomycetota phylum, whereas mannuronic acid-rich mucilage coincided with an increase in the relative abundance of members of the Flavobacteriia and Gammaproteobacteria lineages. We investigated putative carbohydrate-microbe relationships by isolating a member of the Planctomycetota phylum from the surface of giant kelp. Using whole genome analysis and growth assays, we demonstrate that this isolate grows on fucoidan and <i>N-</i>acetyl glucosamine, but not alginate, consistent with the observed relative abundance of this clade in the kelp microbiome in response to variable mucilage carbohydrate content. This suggests a key role of kelp mucilage carbohydrate composition in structuring its microbiome as has been observed for other organisms such as corals and within the human gut.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf197"},"PeriodicalIF":6.1,"publicationDate":"2025-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12642873/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145607892","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 : 2025-10-28eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf194
Ruben Schulte-Hillen, Jakob K Giesler, Thomas Mock, Nigel Belshaw, Uwe John, Tilmann Harder, Nancy Kühne, Stefan Neuhaus, Sylke Wohlrab
Primary production in aquatic systems is governed by interactions between microalgae and their associated bacteria. Most of our knowledge about algal microbiomes stems from natural mixed communities or isolated algal monocultures, which therefore does neither address the role of genotypic diversity among the algal host cells nor do they reveal how this host diversity impacts the assembly process of associated bacteria. To overcome this knowledge gap, we developed a single-cell 16S sequencing approach in combination with CRISPR-Cas9 guided depletion of host 16S contaminations from the chloroplast. The validity of this novel method was tested by comparing bacterial communities of 144 single-cells across three genotypes of the Arctic marine diatom Thalassiosira gravida grown under different environmental conditions. From these, 62 single-cells were additionally sequenced after CRISPR-Cas9 treatment. Due to the improved sequencing depth, bacterial richness associated with individual diatom cells was increased by up to 56%. By applying this CRISPR-Cas9 treatment we not only revealed intraspecific host-genotype associations but also low-abundance bacterial taxa that were not detected by standard 16S rRNA gene metabarcoding. Thus, the CRISPR-Cas9 assisted single-cell approach developed in this study advances our understanding on how the intraspecific diversity among algal hosts impacts the assembly process of their associated bacteria. This knowledge is essential to understand the co-evolution and adaptation of species in algal microbiomes.
{"title":"Genotype and culture condition effects on single-cell diatom microbiomes: enhanced detection of low-abundance taxa with CRISPR-Cas9.","authors":"Ruben Schulte-Hillen, Jakob K Giesler, Thomas Mock, Nigel Belshaw, Uwe John, Tilmann Harder, Nancy Kühne, Stefan Neuhaus, Sylke Wohlrab","doi":"10.1093/ismeco/ycaf194","DOIUrl":"10.1093/ismeco/ycaf194","url":null,"abstract":"<p><p>Primary production in aquatic systems is governed by interactions between microalgae and their associated bacteria. Most of our knowledge about algal microbiomes stems from natural mixed communities or isolated algal monocultures, which therefore does neither address the role of genotypic diversity among the algal host cells nor do they reveal how this host diversity impacts the assembly process of associated bacteria. To overcome this knowledge gap, we developed a single-cell 16S sequencing approach in combination with CRISPR-Cas9 guided depletion of host 16S contaminations from the chloroplast. The validity of this novel method was tested by comparing bacterial communities of 144 single-cells across three genotypes of the Arctic marine diatom <i>Thalassiosira gravida</i> grown under different environmental conditions. From these, 62 single-cells were additionally sequenced after CRISPR-Cas9 treatment. Due to the improved sequencing depth, bacterial richness associated with individual diatom cells was increased by up to 56%. By applying this CRISPR-Cas9 treatment we not only revealed intraspecific host-genotype associations but also low-abundance bacterial taxa that were not detected by standard 16S rRNA gene metabarcoding. Thus, the CRISPR-Cas9 assisted single-cell approach developed in this study advances our understanding on how the intraspecific diversity among algal hosts impacts the assembly process of their associated bacteria. This knowledge is essential to understand the co-evolution and adaptation of species in algal microbiomes.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf194"},"PeriodicalIF":6.1,"publicationDate":"2025-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12676716/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145703049","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}