Pub Date : 2024-11-04eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae137
Futing Zhang, Siyuan Wang, Anna-Neva Visser, Coco Koedooder, Meri Eichner, O Roger Anderson, Sonya T Dyhrman, Yeala Shaked
Colonies of the N2-fixing cyanobacterium Trichodesmium spp. constitute a consortium with multiple microorganisms that collectively exert ecosystem-level influence on marine carbon and nitrogen cycling, shunting newly fixed nitrogen to low nitrogen systems, and exporting both carbon and nitrogen to the deep sea. Here we identify a seasonally recurrent association between puff colonies and amoebae through a two-year survey involving over 10 000 Trichodesmium colonies in the Red Sea. This association was most commonly found in near-shore populations during spring. Microscopic observations revealed consistent amoebae morphology throughout the study, and both morphological characteristics and 18S rRNA gene sequencing suggested that these amoebae are likely to belong to the species Trichosphaerium micrum, an amoeba that forms a CaCO3 shell. Co-cultures of Trichosphaerium micrum and Trichodesmium grown in the laboratory suggest that the amoebae feed on heterotrophic bacteria and not Trichodesmium, which adds a consumer dynamic to the complex microbial interactions within these colonies. Sinking experiments with fresh colonies indicated that the presence of the CaCO3-shelled amoebae decreased colony buoyancy. As such, this novel association may accelerate Trichodesmium sinking rates and facilitate carbon and nitrogen export to the deep ocean. Amoebae have previously been identified in Trichodesmium colonies in the western North Atlantic (Bermuda and Barbados), suggesting that this type of association may be widespread. This association may add a new critical facet to the microbial interactions underpinning carbon and nitrogen fixation and fate in the present and future ocean.
{"title":"Recurrent association between <i>Trichodesmium</i> colonies and calcifying amoebae.","authors":"Futing Zhang, Siyuan Wang, Anna-Neva Visser, Coco Koedooder, Meri Eichner, O Roger Anderson, Sonya T Dyhrman, Yeala Shaked","doi":"10.1093/ismeco/ycae137","DOIUrl":"10.1093/ismeco/ycae137","url":null,"abstract":"<p><p>Colonies of the N<sub>2</sub>-fixing cyanobacterium <i>Trichodesmium</i> spp. constitute a consortium with multiple microorganisms that collectively exert ecosystem-level influence on marine carbon and nitrogen cycling, shunting newly fixed nitrogen to low nitrogen systems, and exporting both carbon and nitrogen to the deep sea. Here we identify a seasonally recurrent association between puff colonies and amoebae through a two-year survey involving over 10 000 <i>Trichodesmium</i> colonies in the Red Sea. This association was most commonly found in near-shore populations during spring. Microscopic observations revealed consistent amoebae morphology throughout the study, and both morphological characteristics and 18S rRNA gene sequencing suggested that these amoebae are likely to belong to the species <i>Trichosphaerium micrum</i>, an amoeba that forms a CaCO<sub>3</sub> shell. Co-cultures of <i>Trichosphaerium micrum</i> and <i>Trichodesmium</i> grown in the laboratory suggest that the amoebae feed on heterotrophic bacteria and not <i>Trichodesmium</i>, which adds a consumer dynamic to the complex microbial interactions within these colonies. Sinking experiments with fresh colonies indicated that the presence of the CaCO<sub>3</sub>-shelled amoebae decreased colony buoyancy. As such, this novel association may accelerate <i>Trichodesmium</i> sinking rates and facilitate carbon and nitrogen export to the deep ocean. Amoebae have previously been identified in <i>Trichodesmium</i> colonies in the western North Atlantic (Bermuda and Barbados), suggesting that this type of association may be widespread. This association may add a new critical facet to the microbial interactions underpinning carbon and nitrogen fixation and fate in the present and future ocean.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae137"},"PeriodicalIF":5.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11575492/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142677967","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}
Microeukaryotes are critical components of sinking particles contributing to carbon export from the surface to deep oceans. However, the knowledge of the sinking microeukaryotic communities and their dynamics is currently limited. In this study, we applied 18S rRNA gene metabarcoding to investigate the microeukaryotic communities in sinking and suspended particles distinguished by marine snow catchers during spring in the Oyashio region. Sinking particles displayed distinct communities and lower diversity than suspended particles. The community compositions of the sinking particles varied with depth, suggesting that microeukaryotes were selectively disaggregated or decomposed during settling. Prymnesiophyceae and diatoms were effectively removed, as indicated by their decreased abundance in sinking particles at increasing depths. Conversely, Dinophyceae maintained a higher abundance in sinking particles across depths, indicating resistance to disaggregation and decomposition. Spirotrichea and heterotrophic Dinophyceae were enriched in sinking particles, while marine stramenopiles groups were enriched in suspended particles. The heterotrophs in the deeper layers were mainly transported from the surface layers by increasing their relative abundance towards deep layers, indicating that they contributed to the transformation processes of sinking particles. Overall, our results demonstrate the functional differences among microeukaryotes in the biological carbon pump.
{"title":"Taxon-specific contributions of microeukaryotes to biological carbon pump in the Oyashio region.","authors":"Qingwei Yang, Yanhui Yang, Jun Xia, Hideki Fukuda, Yusuke Okazaki, Toshi Nagata, Hiroyuki Ogata, Hisashi Endo","doi":"10.1093/ismeco/ycae136","DOIUrl":"10.1093/ismeco/ycae136","url":null,"abstract":"<p><p>Microeukaryotes are critical components of sinking particles contributing to carbon export from the surface to deep oceans. However, the knowledge of the sinking microeukaryotic communities and their dynamics is currently limited. In this study, we applied 18S rRNA gene metabarcoding to investigate the microeukaryotic communities in sinking and suspended particles distinguished by marine snow catchers during spring in the Oyashio region. Sinking particles displayed distinct communities and lower diversity than suspended particles. The community compositions of the sinking particles varied with depth, suggesting that microeukaryotes were selectively disaggregated or decomposed during settling. Prymnesiophyceae and diatoms were effectively removed, as indicated by their decreased abundance in sinking particles at increasing depths. Conversely, Dinophyceae maintained a higher abundance in sinking particles across depths, indicating resistance to disaggregation and decomposition. Spirotrichea and heterotrophic Dinophyceae were enriched in sinking particles, while marine stramenopiles groups were enriched in suspended particles. The heterotrophs in the deeper layers were mainly transported from the surface layers by increasing their relative abundance towards deep layers, indicating that they contributed to the transformation processes of sinking particles. Overall, our results demonstrate the functional differences among microeukaryotes in the biological carbon pump.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae136"},"PeriodicalIF":5.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11575449/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142677968","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 : 2024-10-30eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae127
Qi Liu, Tiancong Sun, Penglong Wang, Lifang Wang, Helena Frantova, David Hartmann, Jan Perner, Weiwei Sun, Baoliang Pan
Endosymbiotic bacteria significantly impact the fitness of their arthropod hosts. Dermanyssus gallinae, the poultry red mite, is a blood-feeding ectoparasite that exclusively feeds on avian blood. While there is a relatively comprehensive understanding of its microbial community structures across developmental stages based on 16S rRNA sequencing, the functional integration of these microbes within the host's physiology remains elusive. This study aims to elucidate the role of symbiotic bacteria in D. gallinae biology. 16S rRNA amplicon sequencing and fluorescence in situ hybridization revealed a prominent midgut-confinement bacterial microbiota with considerable diversity, out of which Kocuria and Bartonella A acted as the predominant bacterial genera inhabiting D. gallinae. The relative abundance of Bartonella A increased rapidly after blood-sucking, suggesting its adaptation to a blood-based diet and its pivotal role in post-engorgement activities. Some of the isolated bacterial strains from D. gallinae display hemolytic activity on blood agar, potentially aiding blood digestion. To corroborate this in vivo, antibiotic-mediated clearance was exploited to generate dysbiosed cohorts of D. gallinae mites, lacking some of the key bacterial species. Phenotypic assessments revealed that dysbiosed mites experienced delayed blood digestion and diminished reproductive capacity. Whole-genome sequencing identified Bartonella A as a new species within the genus Bartonella, exhibiting characteristics of an obligate symbiont. These findings underscore the significance of microbiota in poultry red mites and suggest microbiota-targeted strategies for controlling mite populations in poultry farms.
内共生细菌对节肢动物宿主的健康状况有重大影响。家禽红螨 Dermanyssus gallinae 是一种专门以禽类血液为食的外寄生虫。虽然基于 16S rRNA 测序对其各发育阶段的微生物群落结构有了相对全面的了解,但这些微生物在宿主生理机能中的功能整合仍然难以捉摸。本研究旨在阐明共生细菌在五倍子生物学中的作用。16S rRNA扩增片段测序和荧光原位杂交显示,中肠融合细菌微生物群具有显著的多样性,其中Kocuria和Bartonella A是栖息在五倍子中的主要细菌属。巴顿氏菌 A 的相对丰度在吸血后迅速增加,表明其适应了以血液为基础的食物,并在窒息后的活动中发挥了关键作用。从五倍子中分离出的一些细菌菌株在血液琼脂上显示出溶血活性,可能有助于血液消化。为了在体内证实这一点,研究人员利用抗生素介导的清除作用,产生了一批菌群失调的五倍子螨,其中缺乏一些关键的细菌种类。表型评估显示,菌群失调的螨虫消化血液的时间会推迟,繁殖能力也会减弱。全基因组测序发现巴顿氏菌 A 是巴顿氏菌属中的一个新物种,表现出必须共生的特征。这些发现强调了微生物群在家禽红螨中的重要性,并提出了以微生物群为目标的家禽养殖场螨虫种群控制策略。
{"title":"Significant role of symbiotic bacteria in the blood digestion and reproduction of <i>Dermanyssus gallinae</i> mites.","authors":"Qi Liu, Tiancong Sun, Penglong Wang, Lifang Wang, Helena Frantova, David Hartmann, Jan Perner, Weiwei Sun, Baoliang Pan","doi":"10.1093/ismeco/ycae127","DOIUrl":"https://doi.org/10.1093/ismeco/ycae127","url":null,"abstract":"<p><p>Endosymbiotic bacteria significantly impact the fitness of their arthropod hosts. <i>Dermanyssus gallinae</i>, the poultry red mite, is a blood-feeding ectoparasite that exclusively feeds on avian blood. While there is a relatively comprehensive understanding of its microbial community structures across developmental stages based on 16S rRNA sequencing, the functional integration of these microbes within the host's physiology remains elusive. This study aims to elucidate the role of symbiotic bacteria in <i>D. gallinae</i> biology. 16S rRNA amplicon sequencing and fluorescence <i>in situ</i> hybridization revealed a prominent midgut-confinement bacterial microbiota with considerable diversity, out of which <i>Kocuria</i> and <i>Bartonella</i> A acted as the predominant bacterial genera inhabiting <i>D. gallinae</i>. The relative abundance of <i>Bartonella</i> A increased rapidly after blood-sucking, suggesting its adaptation to a blood-based diet and its pivotal role in post-engorgement activities. Some of the isolated bacterial strains from <i>D. gallinae</i> display hemolytic activity on blood agar, potentially aiding blood digestion. To corroborate this <i>in vivo</i>, antibiotic-mediated clearance was exploited to generate dysbiosed cohorts of <i>D. gallinae</i> mites, lacking some of the key bacterial species. Phenotypic assessments revealed that dysbiosed mites experienced delayed blood digestion and diminished reproductive capacity. Whole-genome sequencing identified <i>Bartonella</i> A as a new species within the genus <i>Bartonella</i>, exhibiting characteristics of an obligate symbiont. These findings underscore the significance of microbiota in poultry red mites and suggest microbiota-targeted strategies for controlling mite populations in poultry farms.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae127"},"PeriodicalIF":5.1,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11550332/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633807","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 : 2024-10-29eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae132
Debjyoti Ghosh, Yijie Shi, Iris M Zimmermann, Tobias Stürzebecher, Katja Holzhauser, Martin von Bergen, Anne-Kristin Kaster, Sandra Spielvogel, Michaela A Dippold, Jochen A Müller, Nico Jehmlich
Cover cropping is an effective method to protect agricultural soils from erosion, promote nutrient and moisture retention, encourage beneficial microbial activity, and maintain soil structure. Re-utilization of winter cover crop root channels by maize roots during summer allows the cash crop to extract resources from distal regions in the soil horizon. In this study, we investigated how cover cropping during winter followed by maize (Zea mays L.) during summer affects the spatiotemporal composition and function of the bacterial communities in the maize rhizosphere and surrounding soil samples using quantitative polymerase chain reaction (PCR), 16S ribosomal ribonucleic acid (rRNA) gene amplicon sequencing, and metaproteomics. We found that the bacterial community differed significantly among cover crop species, soil depths, and maize growth stages. Bacterial abundance increased in reused root channels, and it continued to increase as cover crop diversity changed from monocultures to mixtures. Mixing Fabaceae with Brassicaceae or Poaceae enhanced the overall contributions of several steps of the bacterial carbon and nitrogen cycles, especially glycolysis and the pentose phosphate pathway. The deeper root channels of Fabaceae and Brassicaceae as compared to Poaceae corresponded to higher bacterial 16S rRNA gene copy numbers and improved community presence in the subsoil regimes, likely due to the increased availability of root exudates secreted by maize roots. In conclusion, root channel reuse improved the expression of metabolic pathways of the carbon and nitrogen cycles and the bacterial communities, which is beneficial to the soil and to the growing crops.
{"title":"Cover crop monocultures and mixtures enhance bacterial abundance and functionality in the maize root zone.","authors":"Debjyoti Ghosh, Yijie Shi, Iris M Zimmermann, Tobias Stürzebecher, Katja Holzhauser, Martin von Bergen, Anne-Kristin Kaster, Sandra Spielvogel, Michaela A Dippold, Jochen A Müller, Nico Jehmlich","doi":"10.1093/ismeco/ycae132","DOIUrl":"https://doi.org/10.1093/ismeco/ycae132","url":null,"abstract":"<p><p>Cover cropping is an effective method to protect agricultural soils from erosion, promote nutrient and moisture retention, encourage beneficial microbial activity, and maintain soil structure. Re-utilization of winter cover crop root channels by maize roots during summer allows the cash crop to extract resources from distal regions in the soil horizon. In this study, we investigated how cover cropping during winter followed by maize (<i>Zea mays</i> L.) during summer affects the spatiotemporal composition and function of the bacterial communities in the maize rhizosphere and surrounding soil samples using quantitative polymerase chain reaction (PCR), 16S ribosomal ribonucleic acid (rRNA) gene amplicon sequencing, and metaproteomics. We found that the bacterial community differed significantly among cover crop species, soil depths, and maize growth stages. Bacterial abundance increased in reused root channels, and it continued to increase as cover crop diversity changed from monocultures to mixtures. Mixing <i>Fabaceae</i> with <i>Brassicaceae</i> or <i>Poaceae</i> enhanced the overall contributions of several steps of the bacterial carbon and nitrogen cycles, especially glycolysis and the pentose phosphate pathway. The deeper root channels of <i>Fabaceae</i> and <i>Brassicaceae</i> as compared to <i>Poaceae</i> corresponded to higher bacterial 16S rRNA gene copy numbers and improved community presence in the subsoil regimes, likely due to the increased availability of root exudates secreted by maize roots. In conclusion, root channel reuse improved the expression of metabolic pathways of the carbon and nitrogen cycles and the bacterial communities, which is beneficial to the soil and to the growing crops.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae132"},"PeriodicalIF":5.1,"publicationDate":"2024-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11546721/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633715","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 : 2024-10-25eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae126
Ulrike Binsker, Carlus Deneke, Hafiz Muhammad Hamid, Ashish K Gadicherla, André Göhler, Annemarie Käsbohrer, Jens A Hammerl
Anthropogenic activities enhance the interconnection of human, animal, and environmental habitats and drive the evolution and inter-niche transmission of bacteria. Clear identification of emerging bacteria and pathogen control is therefore a public health priority. In 2015, the novel Escherichia species Escherichia marmotae was assigned, but due to the lack of appropriate detection and typing technologies, the One Health impact of this species is still being unraveled. E. marmotae represents a missing link in the impact of Escherichia spp. Here, we report 25 E. marmotae identified by next-generation sequencing that were previously phenotypically characterized as Escherichia coli during national zoonosis monitoring of food-producing animals. Applying fastANI to 153 738 published Escherichia spp. genome assemblies, we identified further 124 E. marmotae, originally classified as E. coli. Phylogenomics of all 149 isolates reveals an undefined population structure that is independent of the ecological niche. We highlight the phenotypic, genomic, and plasmid diversity of E. marmotae and provide evidence for gene flow across the species. The latter is illustrated by the acquisition of antibiotic resistance plasmids and pathogenicity islands, such as the type III secretion system. Thus, our comprehensive genomic overview of an emerging potential opportunistic pathogen underlines the importance of improved detection and characterization.
{"title":"Genomic dissection of <i>Escherichia marmotae</i> provides insights into diversity and pathogenic potential.","authors":"Ulrike Binsker, Carlus Deneke, Hafiz Muhammad Hamid, Ashish K Gadicherla, André Göhler, Annemarie Käsbohrer, Jens A Hammerl","doi":"10.1093/ismeco/ycae126","DOIUrl":"https://doi.org/10.1093/ismeco/ycae126","url":null,"abstract":"<p><p>Anthropogenic activities enhance the interconnection of human, animal, and environmental habitats and drive the evolution and inter-niche transmission of bacteria. Clear identification of emerging bacteria and pathogen control is therefore a public health priority. In 2015, the novel <i>Escherichia</i> species <i>Escherichia marmotae</i> was assigned, but due to the lack of appropriate detection and typing technologies, the One Health impact of this species is still being unraveled. <i>E. marmotae</i> represents a missing link in the impact of <i>Escherichia</i> spp. Here, we report 25 <i>E. marmotae</i> identified by next-generation sequencing that were previously phenotypically characterized as <i>Escherichia coli</i> during national zoonosis monitoring of food-producing animals. Applying fastANI to 153 738 published <i>Escherichia</i> spp. genome assemblies, we identified further 124 <i>E. marmotae</i>, originally classified as <i>E. coli</i>. Phylogenomics of all 149 isolates reveals an undefined population structure that is independent of the ecological niche. We highlight the phenotypic, genomic, and plasmid diversity of <i>E. marmotae</i> and provide evidence for gene flow across the species. The latter is illustrated by the acquisition of antibiotic resistance plasmids and pathogenicity islands, such as the type III secretion system. Thus, our comprehensive genomic overview of an emerging potential opportunistic pathogen underlines the importance of improved detection and characterization.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae126"},"PeriodicalIF":5.1,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11546641/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633720","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 : 2024-10-24eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae129
Christiana Abiola, Joo-Han Gwak, Ui-Ju Lee, Samuel Imisi Awala, Man-Young Jung, Woojun Park, Sung-Keun Rhee
Soil microorganisms often thrive as microcolonies or biofilms within pores of soil aggregates exposed to the soil atmosphere. However, previous studies on the physiology of soil ammonia-oxidizing microorganisms (AOMs), which play a critical role in the nitrogen cycle, were primarily conducted using freely suspended AOM cells (planktonic cells) in liquid media. In this study, we examined the growth of two representative soil ammonia-oxidizing archaea (AOA), Nitrososphaera viennensis EN76 and "Nitrosotenuis chungbukensis" MY2, and a soil ammonia-oxidizing bacterium, Nitrosomonas europaea ATCC 19718 on polycarbonate membrane filters floated on liquid media to observe their adaptation to air-exposed solid surfaces. Interestingly, ammonia oxidation activities of N. viennensis EN76 and "N. chungbukensis" MY2 were significantly repressed on floating filters compared to the freely suspended cells in liquid media. Conversely, the ammonia oxidation activity of N. europaea ATCC 19718 was comparable on floating filters and liquid media. N. viennensis EN76 and N. europaea ATCC 19718 developed microcolonies on floating filters. Transcriptome analysis of N. viennensis EN76 floating filter-grown cells revealed upregulation of unique sets of genes for cell wall and extracellular polymeric substance biosynthesis, ammonia oxidation (including ammonia monooxygenase subunit C (amoC3) and multicopper oxidases), and defense against H2O2-induced oxidative stress. These genes may play a pivotal role in adapting AOA to air-exposed solid surfaces. Furthermore, the floating filter technique resulted in the enrichment of distinct soil AOA communities dominated by the "Ca. Nitrosocosmicus" clade. Overall, this study sheds light on distinct adaptive mechanisms governing AOA growth on air-exposed solid surfaces.
{"title":"Growth of soil ammonia-oxidizing archaea on air-exposed solid surface.","authors":"Christiana Abiola, Joo-Han Gwak, Ui-Ju Lee, Samuel Imisi Awala, Man-Young Jung, Woojun Park, Sung-Keun Rhee","doi":"10.1093/ismeco/ycae129","DOIUrl":"10.1093/ismeco/ycae129","url":null,"abstract":"<p><p>Soil microorganisms often thrive as microcolonies or biofilms within pores of soil aggregates exposed to the soil atmosphere. However, previous studies on the physiology of soil ammonia-oxidizing microorganisms (AOMs), which play a critical role in the nitrogen cycle, were primarily conducted using freely suspended AOM cells (planktonic cells) in liquid media. In this study, we examined the growth of two representative soil ammonia-oxidizing archaea (AOA), <i>Nitrososphaera viennensis</i> EN76 and \"<i>Nitrosotenuis chungbukensis</i>\" MY2, and a soil ammonia-oxidizing bacterium, <i>Nitrosomonas europaea</i> ATCC 19718 on polycarbonate membrane filters floated on liquid media to observe their adaptation to air-exposed solid surfaces. Interestingly, ammonia oxidation activities of <i>N. viennensis</i> EN76 and \"<i>N. chungbukensis</i>\" MY2 were significantly repressed on floating filters compared to the freely suspended cells in liquid media. Conversely, the ammonia oxidation activity of <i>N. europaea</i> ATCC 19718 was comparable on floating filters and liquid media. <i>N. viennensis</i> EN76 and <i>N. europaea</i> ATCC 19718 developed microcolonies on floating filters. Transcriptome analysis of <i>N. viennensis</i> EN76 floating filter-grown cells revealed upregulation of unique sets of genes for cell wall and extracellular polymeric substance biosynthesis, ammonia oxidation (including ammonia monooxygenase subunit C (<i>amoC3</i>) and multicopper oxidases), and defense against H<sub>2</sub>O<sub>2</sub>-induced oxidative stress. These genes may play a pivotal role in adapting AOA to air-exposed solid surfaces. Furthermore, the floating filter technique resulted in the enrichment of distinct soil AOA communities dominated by the \"Ca. Nitrosocosmicus\" clade. Overall, this study sheds light on distinct adaptive mechanisms governing AOA growth on air-exposed solid surfaces.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae129"},"PeriodicalIF":5.1,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11561398/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633659","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 : 2024-10-23eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae128
Haocai Wang, Hang Wang, Thomas W Crowther, Kazuo Isobe, Peter B Reich, Ryunosuke Tateno, Weiyu Shi
There is growing awareness of the need for regenerative practices in the fight against biodiversity loss and climate change. Yet, we lack a mechanistic understanding of how microbial community composition and functioning are likely to change alongside transition from high-density tillage to large-scale vegetation restoration. Here, we investigated the functional dynamics of microbial communities following a complete vegetation successional chronosequence in a subtropical zone, Southwestern China, using shotgun metagenomics approaches. The contents of total soil phosphorus (P), available P, litter P, and microbial biomass P decreased significantly during vegetation succession, indicating that P is the most critical limiting nutrient. The abundance of genes related to P-uptake and transport, inorganic P-solubilization, organic P-mineralization, and P-starvation response regulation significantly increased with successional time, indicating an increased microbial "mining" for P under P limitation. Multi-analysis demonstrated microbial P limitation strongly inhibits carbon (C) catabolism potential, resulting in a significant decrease in carbohydrate-active enzyme family gene abundances. Nevertheless, over successional time, microorganisms increased investment in genes involved in degradation-resistant compounds (lignin and its aromatic compounds) to acquire P resources in the litter. Our study provides functional gene-level insights into how P limitation during vegetation succession in subtropical regions inhibits soil microbial C metabolic processes, thereby advancing our understanding of belowground C cycling and microbial metabolic feedback during forest restoration.
人们越来越意识到,在应对生物多样性丧失和气候变化的过程中,需要采用再生方法。然而,我们对微生物群落的组成和功能如何可能随着从高密度耕作到大规模植被恢复的过渡而发生变化缺乏机制上的了解。在此,我们采用霰弹枪元基因组学方法研究了中国西南亚热带地区完整植被演替时序后微生物群落的功能动态。在植被演替过程中,土壤总磷、可利用磷、枯落物磷和微生物生物量磷的含量显著下降,表明磷是最关键的限制性养分。与磷吸收和转运、无机磷溶解、有机磷矿化和磷饥饿反应调节相关的基因丰度随着演替时间的延长而显著增加,表明在磷限制条件下微生物对磷的 "挖掘 "增加。多重分析表明,微生物的 P 限制强烈抑制了碳(C)分解潜力,导致碳水化合物活性酶家族基因丰度显著下降。然而,随着演替时间的推移,微生物增加了对涉及抗降解化合物(木质素及其芳香族化合物)基因的投资,以获取枯落物中的钾资源。我们的研究从功能基因水平上揭示了亚热带地区植被演替过程中P限制是如何抑制土壤微生物C代谢过程的,从而加深了我们对森林恢复过程中地下C循环和微生物代谢反馈的理解。
{"title":"Metagenomic insights into inhibition of soil microbial carbon metabolism by phosphorus limitation during vegetation succession.","authors":"Haocai Wang, Hang Wang, Thomas W Crowther, Kazuo Isobe, Peter B Reich, Ryunosuke Tateno, Weiyu Shi","doi":"10.1093/ismeco/ycae128","DOIUrl":"10.1093/ismeco/ycae128","url":null,"abstract":"<p><p>There is growing awareness of the need for regenerative practices in the fight against biodiversity loss and climate change. Yet, we lack a mechanistic understanding of how microbial community composition and functioning are likely to change alongside transition from high-density tillage to large-scale vegetation restoration. Here, we investigated the functional dynamics of microbial communities following a complete vegetation successional chronosequence in a subtropical zone, Southwestern China, using shotgun metagenomics approaches. The contents of total soil phosphorus (P), available P, litter P, and microbial biomass P decreased significantly during vegetation succession, indicating that P is the most critical limiting nutrient. The abundance of genes related to P-uptake and transport, inorganic P-solubilization, organic P-mineralization, and P-starvation response regulation significantly increased with successional time, indicating an increased microbial \"mining\" for P under P limitation. Multi-analysis demonstrated microbial P limitation strongly inhibits carbon (C) catabolism potential, resulting in a significant decrease in carbohydrate-active enzyme family gene abundances. Nevertheless, over successional time, microorganisms increased investment in genes involved in degradation-resistant compounds (lignin and its aromatic compounds) to acquire P resources in the litter. Our study provides functional gene-level insights into how P limitation during vegetation succession in subtropical regions inhibits soil microbial C metabolic processes, thereby advancing our understanding of belowground C cycling and microbial metabolic feedback during forest restoration.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae128"},"PeriodicalIF":5.1,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11538728/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142592455","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 : 2024-10-23eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae125
Stephanie N Vaughn, Garrett W Hopper, Irene Sánchez González, Jamie R Bucholz, Ryan C Garrick, Jeffrey D Lozier, Paul D Johnson, Carla L Atkinson, Colin R Jackson
The gut microbiome is influenced by host species and the environment, but how the environment influences the microbiome of animals introduced into a new ecosystem has rarely been investigated. Freshwater mussels are aquatic fauna, with some threatened or endangered species propagated in hatcheries and introduced into natural systems as part of conservation efforts. The effects of the environment on the freshwater mussel gut microbiome were assessed for two hatchery-propagated species (Lampsilis ovata, Lampsilis ornata) introduced into rivers within their natural range. Mussels were placed in rivers for 8 weeks, after which one subset was collected, another subset remained in that river, and a third subset was reciprocally transplanted to another river in the same river basin for a further 8 weeks. Gut microbiome composition and diversity were characterized for all mussels. After the initial 8 weeks, mussels showed increased gut bacterial species richness and distinct community composition compared to hatchery mussels, but gut microbiome diversity then decreased for mussels that remained in the same river for all 16 weeks. The gut bacterial community of mussels transplanted between rivers shifted to resemble that of mussels placed initially into the recipient river and that remained there for the whole study. All mussels showed high proportions of Firmicutes in their gut microbiome after 8 weeks, suggesting an essential role of this phylum in the gut of Lampsilis species. These findings show that the mussel gut microbiome shifts in response to new environments and provide insights into conservation strategies that involve species reintroductions.
{"title":"Introduction into natural environments shifts the gut microbiome of captivity-raised filter-feeding bivalves.","authors":"Stephanie N Vaughn, Garrett W Hopper, Irene Sánchez González, Jamie R Bucholz, Ryan C Garrick, Jeffrey D Lozier, Paul D Johnson, Carla L Atkinson, Colin R Jackson","doi":"10.1093/ismeco/ycae125","DOIUrl":"10.1093/ismeco/ycae125","url":null,"abstract":"<p><p>The gut microbiome is influenced by host species and the environment, but how the environment influences the microbiome of animals introduced into a new ecosystem has rarely been investigated. Freshwater mussels are aquatic fauna, with some threatened or endangered species propagated in hatcheries and introduced into natural systems as part of conservation efforts. The effects of the environment on the freshwater mussel gut microbiome were assessed for two hatchery-propagated species (<i>Lampsilis ovata</i>, <i>Lampsilis ornata</i>) introduced into rivers within their natural range. Mussels were placed in rivers for 8 weeks, after which one subset was collected, another subset remained in that river, and a third subset was reciprocally transplanted to another river in the same river basin for a further 8 weeks. Gut microbiome composition and diversity were characterized for all mussels. After the initial 8 weeks, mussels showed increased gut bacterial species richness and distinct community composition compared to hatchery mussels, but gut microbiome diversity then decreased for mussels that remained in the same river for all 16 weeks. The gut bacterial community of mussels transplanted between rivers shifted to resemble that of mussels placed initially into the recipient river and that remained there for the whole study. All mussels showed high proportions of <i>Firmicutes</i> in their gut microbiome after 8 weeks, suggesting an essential role of this phylum in the gut of <i>Lampsilis</i> species. These findings show that the mussel gut microbiome shifts in response to new environments and provide insights into conservation strategies that involve species reintroductions.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae125"},"PeriodicalIF":5.1,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11538807/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142592474","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 : 2024-10-22eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae124
Hon Lun Wong, Paul-Adrian Bulzu, Rohit Ghai, Maria-Cecilia Chiriac, Michaela M Salcher
Acidobacteriota are abundant in soil, peatlands, and sediments, but their ecology in freshwater environments remains understudied. UBA12189, an Acidobacteriota genus, is an uncultivated, genome-streamlined lineage with a small genome size found in aquatic environments where detailed genomic analyses are lacking. Here, we analyzed 66 MAGs of UBA12189 (including one complete genome) from freshwater lakes and rivers in Europe, North America, and Asia. UBA12189 has small genome sizes (<1.4 Mbp), low GC content, and a highly diverse pangenome. In freshwater lakes, this bacterial lineage is abundant from the surface waters (epilimnion) down to a 300-m depth (hypolimnion). UBA12189 appears to be free-living from CARD-FISH analysis. When compared to other genome-streamlined bacteria such as Nanopelagicales and Methylopumilus, genome reduction has caused UBA12189 to have a more limited metabolic repertoire in carbon, sulfur, and nitrogen metabolisms, limited numbers of membrane transporters, as well as a higher degree of auxotrophy for various amino acids, vitamins, and reduced sulfur. Despite having reduced genomes, UBA12189 encodes proteorhodopsin, complete biosynthesis pathways for heme and vitamin K2, cbb3-type cytochrome c oxidases, and heme-requiring enzymes. These genes may give a selective advantage during the genome streamlining process. We propose the new genus Acidiparvus, with two new species named "A. lacustris" and "A. fluvialis". Acidiparvus is the first described genome-streamlined lineage under the phylum Acidobacteriota, which is a free-living, slow-growing scavenger in freshwater environments.
{"title":"Ubiquitous genome streamlined <i>Acidobacteriota</i> in freshwater environments.","authors":"Hon Lun Wong, Paul-Adrian Bulzu, Rohit Ghai, Maria-Cecilia Chiriac, Michaela M Salcher","doi":"10.1093/ismeco/ycae124","DOIUrl":"10.1093/ismeco/ycae124","url":null,"abstract":"<p><p><i>Acidobacteriota</i> are abundant in soil, peatlands, and sediments, but their ecology in freshwater environments remains understudied. UBA12189, an <i>Acidobacteriota</i> genus, is an uncultivated, genome-streamlined lineage with a small genome size found in aquatic environments where detailed genomic analyses are lacking. Here, we analyzed 66 MAGs of UBA12189 (including one complete genome) from freshwater lakes and rivers in Europe, North America, and Asia. UBA12189 has small genome sizes (<1.4 Mbp), low GC content, and a highly diverse pangenome. In freshwater lakes, this bacterial lineage is abundant from the surface waters (epilimnion) down to a 300-m depth (hypolimnion). UBA12189 appears to be free-living from CARD-FISH analysis. When compared to other genome-streamlined bacteria such as <i>Nanopelagicales</i> and <i>Methylopumilus</i>, genome reduction has caused UBA12189 to have a more limited metabolic repertoire in carbon, sulfur, and nitrogen metabolisms, limited numbers of membrane transporters, as well as a higher degree of auxotrophy for various amino acids, vitamins, and reduced sulfur. Despite having reduced genomes, UBA12189 encodes proteorhodopsin, complete biosynthesis pathways for heme and vitamin K<sub>2</sub>, cbb<sub>3</sub>-type cytochrome <i>c</i> oxidases, and heme-requiring enzymes. These genes may give a selective advantage during the genome streamlining process. We propose the new genus <i>Acidiparvus</i>, with two new species named \"<i>A. lacustris</i>\" and \"<i>A. fluvialis</i>\". <i>Acidiparvus</i> is the first described genome-streamlined lineage under the phylum <i>Acidobacteriota</i>, which is a free-living, slow-growing scavenger in freshwater environments.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae124"},"PeriodicalIF":5.1,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11561045/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633790","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 influence of chronically administered host-targeted drugs on the gut microbiome remains less understood compared to antibiotics. We investigated repetitive exposure effects of three common antiseizure medications [carbamazepine (CBZ), valproic acid, and levetiracetam] on the gut microbial composition, resistome, and metabolome using microcosms constructed from feces of young children. Microcosms were established by cultivating feces for 24 h (C0). These microcosms were daily transferred into fresh media for seven cycles (C1-C7) with antiseizure medications or carrier molecules, followed by four cycles without any drugs (C8-C11). The microbial dynamics and resistome of microcosms at C0, C1, C7, and C11 were assessed with 16S ribosomal ribonucleic acid gene sequencing or shotgun metagenome sequencing and real-time quantitative polymerase chain reaction analysis of the antimicrobial resistance genes, respectively. Metabolites of CBZ-treated and control microcosms at C0, C1, and C7 were evaluated using non-targeted metabolomics. Our findings revealed that the serial transfer approach longitudinally altered the microcosm composition. Among the medications, CBZ had the most substantial impact on the structure and metabolism of the feces-derived microcosms. The microbiome composition partially recovered during the drug-free period. Specifically, Bacteroides and Flavonifractor were depleted and Escherichia and Clostridium were enriched. Additionally, repetitive CBZ exposure increased the abundance and expression of genes related to various antibiotic resistance mechanisms, more specifically, efflux pumps and antibiotic target alteration. CBZ-induced changes in the microbiome were mirrored in the metabolome, with reductions in the citric acid cycle metabolites, glutamine, and spermidine, alongside increased levels of vitamin B6. Our study suggests that repetitive CBZ exposure may negatively impact gut microbial homeostasis and metabolism.
{"title":"Longitudinal exposure to antiseizure medications shape gut-derived microbiome, resistome, and metabolome landscape.","authors":"Camille Dop, Stéphane Auvin, Stanislas Mondot, Patricia Lepage, Zehra Esra Ilhan","doi":"10.1093/ismeco/ycae123","DOIUrl":"https://doi.org/10.1093/ismeco/ycae123","url":null,"abstract":"<p><p>The influence of chronically administered host-targeted drugs on the gut microbiome remains less understood compared to antibiotics. We investigated repetitive exposure effects of three common antiseizure medications [carbamazepine (CBZ), valproic acid, and levetiracetam] on the gut microbial composition, resistome, and metabolome using microcosms constructed from feces of young children. Microcosms were established by cultivating feces for 24 h (C0). These microcosms were daily transferred into fresh media for seven cycles (C1-C7) with antiseizure medications or carrier molecules, followed by four cycles without any drugs (C8-C11). The microbial dynamics and resistome of microcosms at C0, C1, C7, and C11 were assessed with 16S ribosomal ribonucleic acid gene sequencing or shotgun metagenome sequencing and real-time quantitative polymerase chain reaction analysis of the antimicrobial resistance genes, respectively. Metabolites of CBZ-treated and control microcosms at C0, C1, and C7 were evaluated using non-targeted metabolomics. Our findings revealed that the serial transfer approach longitudinally altered the microcosm composition. Among the medications, CBZ had the most substantial impact on the structure and metabolism of the feces-derived microcosms. The microbiome composition partially recovered during the drug-free period. Specifically, <i>Bacteroides</i> and <i>Flavonifractor</i> were depleted and <i>Escherichia</i> and <i>Clostridium</i> were enriched. Additionally, repetitive CBZ exposure increased the abundance and expression of genes related to various antibiotic resistance mechanisms, more specifically, efflux pumps and antibiotic target alteration. CBZ-induced changes in the microbiome were mirrored in the metabolome, with reductions in the citric acid cycle metabolites, glutamine, and spermidine, alongside increased levels of vitamin B6. Our study suggests that repetitive CBZ exposure may negatively impact gut microbial homeostasis and metabolism.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae123"},"PeriodicalIF":5.1,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11544314/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142633661","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}