Pub Date : 2024-10-21DOI: 10.1186/s40168-024-01923-9
Merel van Gogh, Jonas M Louwers, Anna Celli, Sanne Gräve, Marco C Viveen, Sofie Bosch, Nanne K H de Boer, Rik J Verheijden, Karijn P M Suijkerbuijk, Eelco C Brand, Janetta Top, Bas Oldenburg, Marcel R de Zoete
Background: The intestinal microbiota plays a significant role in maintaining systemic and intestinal homeostasis, but can also influence diseases such as inflammatory bowel disease (IBD) and cancer. Certain bacterial species within the intestinal tract can chronically activate the immune system, leading to low-grade intestinal inflammation. As a result, plasma cells produce high levels of secretory antigen-specific immunoglobulin A (IgA), which coats the immunostimulatory bacteria. This IgA immune response against intestinal bacteria may be associated with the maintenance of homeostasis and health, as well as disease. Unraveling this dichotomy and identifying the immunostimulatory bacteria is crucial for understanding the relationship between the intestinal microbiota and the immune system, and their role in health and disease. IgA-SEQ technology has successfully identified immunostimulatory, IgA-coated bacteria from fecal material. However, the original technology is time-consuming and has limited downstream applications. In this study, we aimed to develop a next-generation, high-throughput, magnet-based sorting approach (ng-IgA-SEQ) to overcome the limitations of the original IgA-SEQ protocol.
Results: We show, in various settings of complexity ranging from simple bacterial mixtures to human fecal samples, that our magnetic 96-well plate-based ng-IgA-SEQ protocol is highly efficient at sorting and identifying IgA-coated bacteria in a high-throughput and time efficient manner. Furthermore, we performed a comparative analysis between different IgA-SEQ protocols, highlighting that the original FACS-based IgA-SEQ approach overlooks certain nuances of IgA-coated bacteria, due to the low yield of sorted bacteria. Additionally, magnetic-based ng-IgA-SEQ allows for novel downstream applications. Firstly, as a proof-of-concept, we performed metagenomic shotgun sequencing on 10 human fecal samples to identify IgA-coated bacterial strains and associated pathways and CAZymes. Secondly, we successfully isolated and cultured IgA-coated bacteria by performing the isolation protocol under anaerobic conditions.
Conclusions: Our magnetic 96-well plate-based high-throughput next-generation IgA-SEQ technology efficiently identifies a great number of IgA-coated bacteria from fecal samples. This paves the way for analyzing large cohorts as well as novel downstream applications, including shotgun metagenomic sequencing, culturomics, and various functional assays. These downstream applications are essential to unravel the role of immunostimulatory bacteria in health and disease. Video Abstract.
背景:肠道微生物群在维持全身和肠道平衡方面发挥着重要作用,但也会影响炎症性肠病(IBD)和癌症等疾病。肠道内的某些细菌可长期激活免疫系统,导致低度肠道炎症。因此,浆细胞会产生大量分泌性抗原特异性免疫球蛋白 A(IgA),包裹住免疫刺激细菌。这种针对肠道细菌的 IgA 免疫反应可能与维持平衡和健康以及疾病有关。要了解肠道微生物群与免疫系统之间的关系以及它们在健康和疾病中的作用,揭示这种二分法并确定免疫刺激细菌至关重要。IgA-SEQ 技术已成功地从粪便材料中鉴定出了具有免疫刺激作用的 IgA 包被细菌。然而,原始技术耗时长,下游应用有限。在本研究中,我们旨在开发一种下一代、高通量、基于磁铁的分选方法(ng-IgA-SEQ),以克服原始 IgA-SEQ 方案的局限性:结果:我们在从简单的细菌混合物到人类粪便样本的各种复杂环境中表明,我们基于磁性 96 孔板的 ng-IgA-SEQ 方案能以高通量和省时的方式高效分拣和鉴定 IgA 包被细菌。此外,我们还对不同的 IgA-SEQ 方案进行了比较分析,结果表明,最初基于 FACS 的 IgA-SEQ 方法由于分选细菌的产量较低而忽略了 IgA 包被细菌的某些细微差别。此外,基于磁性的 ng-IgA-SEQ 还可用于新型下游应用。首先,作为概念验证,我们对 10 份人类粪便样本进行了元基因组枪式测序,以确定 IgA 包被细菌菌株及相关途径和 CAZymes。其次,我们通过在厌氧条件下执行分离方案,成功分离并培养了IgA包被菌:结论:我们基于磁性 96 孔板的高通量新一代 IgA-SEQ 技术能从粪便样本中有效鉴定出大量 IgA 包被菌。这为分析大型群体以及新型下游应用(包括散弹枪元基因组测序、培养组学和各种功能测定)铺平了道路。这些下游应用对于揭示免疫刺激细菌在健康和疾病中的作用至关重要。视频摘要。
{"title":"Next-generation IgA-SEQ allows for high-throughput, anaerobic, and metagenomic assessment of IgA-coated bacteria.","authors":"Merel van Gogh, Jonas M Louwers, Anna Celli, Sanne Gräve, Marco C Viveen, Sofie Bosch, Nanne K H de Boer, Rik J Verheijden, Karijn P M Suijkerbuijk, Eelco C Brand, Janetta Top, Bas Oldenburg, Marcel R de Zoete","doi":"10.1186/s40168-024-01923-9","DOIUrl":"10.1186/s40168-024-01923-9","url":null,"abstract":"<p><strong>Background: </strong>The intestinal microbiota plays a significant role in maintaining systemic and intestinal homeostasis, but can also influence diseases such as inflammatory bowel disease (IBD) and cancer. Certain bacterial species within the intestinal tract can chronically activate the immune system, leading to low-grade intestinal inflammation. As a result, plasma cells produce high levels of secretory antigen-specific immunoglobulin A (IgA), which coats the immunostimulatory bacteria. This IgA immune response against intestinal bacteria may be associated with the maintenance of homeostasis and health, as well as disease. Unraveling this dichotomy and identifying the immunostimulatory bacteria is crucial for understanding the relationship between the intestinal microbiota and the immune system, and their role in health and disease. IgA-SEQ technology has successfully identified immunostimulatory, IgA-coated bacteria from fecal material. However, the original technology is time-consuming and has limited downstream applications. In this study, we aimed to develop a next-generation, high-throughput, magnet-based sorting approach (ng-IgA-SEQ) to overcome the limitations of the original IgA-SEQ protocol.</p><p><strong>Results: </strong>We show, in various settings of complexity ranging from simple bacterial mixtures to human fecal samples, that our magnetic 96-well plate-based ng-IgA-SEQ protocol is highly efficient at sorting and identifying IgA-coated bacteria in a high-throughput and time efficient manner. Furthermore, we performed a comparative analysis between different IgA-SEQ protocols, highlighting that the original FACS-based IgA-SEQ approach overlooks certain nuances of IgA-coated bacteria, due to the low yield of sorted bacteria. Additionally, magnetic-based ng-IgA-SEQ allows for novel downstream applications. Firstly, as a proof-of-concept, we performed metagenomic shotgun sequencing on 10 human fecal samples to identify IgA-coated bacterial strains and associated pathways and CAZymes. Secondly, we successfully isolated and cultured IgA-coated bacteria by performing the isolation protocol under anaerobic conditions.</p><p><strong>Conclusions: </strong>Our magnetic 96-well plate-based high-throughput next-generation IgA-SEQ technology efficiently identifies a great number of IgA-coated bacteria from fecal samples. This paves the way for analyzing large cohorts as well as novel downstream applications, including shotgun metagenomic sequencing, culturomics, and various functional assays. These downstream applications are essential to unravel the role of immunostimulatory bacteria in health and disease. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492651/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469617","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Background: The ecosystems of marine ranching have enhanced marine biodiversity and ecological balance and have promoted the natural recovery and enhancement of fishery resources. The microbial communities of these ecosystems, including bacteria, fungi, protists, and viruses, are the drivers of biogeochemical cycles. Although seasonal changes in microbial communities are critical for ecosystem functioning, the current understanding of microbial-driven metabolic properties and their viral communities in marine sediments remains limited. Here, we employed amplicon (16S and 18S) and metagenomic approaches aiming to reveal the seasonal patterns of microbial communities, bacterial-eukaryotic interactions, whole metabolic potential, and their coupling mechanisms with carbon (C), nitrogen (N), and sulfur (S) cycling in marine ranching sediments. Additionally, the characterization and diversity of viral communities in different seasons were explored in marine ranching sediments.
Results: The current study demonstrated that seasonal variations dramatically affected the diversity of microbial communities in marine ranching sediments and the bacterial-eukaryotic interkingdom co-occurrence networks. Metabolic reconstruction of the 113 medium to high-quality metagenome-assembled genomes (MAGs) was conducted, and a total of 8 MAGs involved in key metabolic genes and pathways (methane oxidation - denitrification - S oxidation), suggesting a possible coupling effect between the C, N, and S cycles. In total, 338 viral operational taxonomic units (vOTUs) were identified, all possessing specific ecological characteristics in different seasons and primarily belonging to Caudoviricetes, revealing their widespread distribution and variety in marine sediment ecosystems. In addition, predicted virus-host linkages showed that high host specificity was observed, with few viruses associated with specific hosts.
Conclusions: This finding deepens our knowledge of element cycling and viral diversity in fisheries enrichment ecosystems, providing insights into microbial-virus interactions in marine sediments and their effects on biogeochemical cycling. These findings have potential applications in marine ranching management and ecological conservation. Video Abstract.
{"title":"Seasonal variations of microbial communities and viral diversity in fishery-enhanced marine ranching sediments: insights into metabolic potentials and ecological interactions.","authors":"Cheng-Zhuang Chen, Ping Li, Ling Liu, Yong-Jun Sun, Wen-Ming Ju, Zhi-Hua Li","doi":"10.1186/s40168-024-01922-w","DOIUrl":"10.1186/s40168-024-01922-w","url":null,"abstract":"<p><strong>Background: </strong>The ecosystems of marine ranching have enhanced marine biodiversity and ecological balance and have promoted the natural recovery and enhancement of fishery resources. The microbial communities of these ecosystems, including bacteria, fungi, protists, and viruses, are the drivers of biogeochemical cycles. Although seasonal changes in microbial communities are critical for ecosystem functioning, the current understanding of microbial-driven metabolic properties and their viral communities in marine sediments remains limited. Here, we employed amplicon (16S and 18S) and metagenomic approaches aiming to reveal the seasonal patterns of microbial communities, bacterial-eukaryotic interactions, whole metabolic potential, and their coupling mechanisms with carbon (C), nitrogen (N), and sulfur (S) cycling in marine ranching sediments. Additionally, the characterization and diversity of viral communities in different seasons were explored in marine ranching sediments.</p><p><strong>Results: </strong>The current study demonstrated that seasonal variations dramatically affected the diversity of microbial communities in marine ranching sediments and the bacterial-eukaryotic interkingdom co-occurrence networks. Metabolic reconstruction of the 113 medium to high-quality metagenome-assembled genomes (MAGs) was conducted, and a total of 8 MAGs involved in key metabolic genes and pathways (methane oxidation - denitrification - S oxidation), suggesting a possible coupling effect between the C, N, and S cycles. In total, 338 viral operational taxonomic units (vOTUs) were identified, all possessing specific ecological characteristics in different seasons and primarily belonging to Caudoviricetes, revealing their widespread distribution and variety in marine sediment ecosystems. In addition, predicted virus-host linkages showed that high host specificity was observed, with few viruses associated with specific hosts.</p><p><strong>Conclusions: </strong>This finding deepens our knowledge of element cycling and viral diversity in fisheries enrichment ecosystems, providing insights into microbial-virus interactions in marine sediments and their effects on biogeochemical cycling. These findings have potential applications in marine ranching management and ecological conservation. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492486/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469618","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-18DOI: 10.1186/s40168-024-01940-8
Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie
Background: Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.
Results: We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.
Conclusions: In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.
{"title":"Upper respiratory microbial communities of healthy populations are shaped by niche and age.","authors":"Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie","doi":"10.1186/s40168-024-01940-8","DOIUrl":"10.1186/s40168-024-01940-8","url":null,"abstract":"<p><strong>Background: </strong>Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.</p><p><strong>Results: </strong>We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.</p><p><strong>Conclusions: </strong>In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11490146/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469620","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-17DOI: 10.1186/s40168-024-01899-6
Abeeha Khalil, Anna R Bramucci, Amaranta Focardi, Nine Le Reun, Nathan L R Willams, Unnikrishnan Kuzhiumparambil, Jean-Baptiste Raina, Justin R Seymour
Background: Reciprocal exchanges of metabolites between phytoplankton and bacteria influence the fitness of these microorganisms which ultimately shapes the productivity of marine ecosystems. Recent evidence suggests that plant growth-promoting hormones may be key metabolites within mutualistic phytoplankton-bacteria partnerships, but very little is known about the diversity of plant growth-promoting hormones produced by marine bacteria and their specific effects on phytoplankton growth. Here, we aimed to investigate the capacity of marine bacteria to produce 7 plant growth-promoting hormones and the effects of these hormones on Actinocyclus sp. growth.
Results: We examined the plant growth-promoting hormone synthesis capabilities of 14 bacterial strains that enhance the growth of the common diatom Actinocyclus. Plant growth-promoting hormone biosynthesis was ubiquitous among the bacteria tested. Indeed all 14 strains displayed the genomic potential to synthesise multiple hormones, and mass-spectrometry confirmed that each strain produced at least 6 out of the 7 tested plant growth-promoting hormones. Some of the plant growth-promoting hormones identified here, such as brassinolide and trans-zeatin, have never been reported in marine microorganisms. Importantly, all strains produced the hormone indole-3 acetic acid (IAA) in high concentrations and released it into their surroundings. Furthermore, indole-3 acetic acid extracellular concentrations were positively correlated with the ability of each strain to promote Actinocyclus growth. When inoculated with axenic Actinocyclus cultures, only indole-3 acetic acid and gibberellic acid enhanced the growth of the diatom, with cultures exposed to indole-3 acetic acid exhibiting a two-fold increase in cell numbers.
Conclusion: Our results reveal that marine bacteria produce a much broader range of plant growth-promoting hormones than previously suspected and that some of these compounds enhance the growth of a marine diatom. These findings suggest plant growth-promoting hormones play a large role in microbial communication and broaden our knowledge of their fuctions in the marine environment. Video Abstract.
{"title":"Widespread production of plant growth-promoting hormones among marine bacteria and their impacts on the growth of a marine diatom.","authors":"Abeeha Khalil, Anna R Bramucci, Amaranta Focardi, Nine Le Reun, Nathan L R Willams, Unnikrishnan Kuzhiumparambil, Jean-Baptiste Raina, Justin R Seymour","doi":"10.1186/s40168-024-01899-6","DOIUrl":"https://doi.org/10.1186/s40168-024-01899-6","url":null,"abstract":"<p><strong>Background: </strong>Reciprocal exchanges of metabolites between phytoplankton and bacteria influence the fitness of these microorganisms which ultimately shapes the productivity of marine ecosystems. Recent evidence suggests that plant growth-promoting hormones may be key metabolites within mutualistic phytoplankton-bacteria partnerships, but very little is known about the diversity of plant growth-promoting hormones produced by marine bacteria and their specific effects on phytoplankton growth. Here, we aimed to investigate the capacity of marine bacteria to produce 7 plant growth-promoting hormones and the effects of these hormones on Actinocyclus sp. growth.</p><p><strong>Results: </strong>We examined the plant growth-promoting hormone synthesis capabilities of 14 bacterial strains that enhance the growth of the common diatom Actinocyclus. Plant growth-promoting hormone biosynthesis was ubiquitous among the bacteria tested. Indeed all 14 strains displayed the genomic potential to synthesise multiple hormones, and mass-spectrometry confirmed that each strain produced at least 6 out of the 7 tested plant growth-promoting hormones. Some of the plant growth-promoting hormones identified here, such as brassinolide and trans-zeatin, have never been reported in marine microorganisms. Importantly, all strains produced the hormone indole-3 acetic acid (IAA) in high concentrations and released it into their surroundings. Furthermore, indole-3 acetic acid extracellular concentrations were positively correlated with the ability of each strain to promote Actinocyclus growth. When inoculated with axenic Actinocyclus cultures, only indole-3 acetic acid and gibberellic acid enhanced the growth of the diatom, with cultures exposed to indole-3 acetic acid exhibiting a two-fold increase in cell numbers.</p><p><strong>Conclusion: </strong>Our results reveal that marine bacteria produce a much broader range of plant growth-promoting hormones than previously suspected and that some of these compounds enhance the growth of a marine diatom. These findings suggest plant growth-promoting hormones play a large role in microbial communication and broaden our knowledge of their fuctions in the marine environment. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11487934/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469622","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-17DOI: 10.1186/s40168-024-01925-7
Celia Boukadida, Amy Peralta-Prado, Monserrat Chávez-Torres, Karla Romero-Mora, Alma Rincon-Rubio, Santiago Ávila-Ríos, Daniela Garrido-Rodríguez, Gustavo Reyes-Terán, Sandra Pinto-Cardoso
Background: HIV-1 infection is characterized by a massive depletion of mucosal CD4 T cells that triggers a cascade of events ultimately linking gut microbial dysbiosis to HIV-1 disease progression and pathogenesis. The association between HIV infection and the enteric virome composition is less characterized, although viruses are an essential component of the gut ecosystem. Here, we performed a cross-sectional analysis of the fecal viral (eukaryotic viruses and bacteriophages) and bacterial microbiome in people with HIV (PWH) and in HIV-negative individuals. To gain further insight into the association between the gut microbiome composition, HIV-associated immunodeficiency, and immune recovery, we carried out a longitudinal study including 14 PWH who initiated antiretroviral therapy (ART) and were followed for 24 months with samplings performed at baseline (before ART) and at 2, 6, 12, and 24 months post-ART initiation.
Results: Our data revealed a striking expansion in the abundance and prevalence of several human virus genomic sequences (Anelloviridae, Adenoviridae, and Papillomaviridae) in stool samples of PWH with severe immunodeficiency (CD4 < 200). We also noted a decreased abundance of sequences belonging to two plant viruses from the Tobamovirus genus, a reduction in bacterial alpha diversity, and a decrease in Inoviridae bacteriophage sequences. Short-term ART (24 months) was linked to a significant decrease in human Anelloviridae sequences. Remarkably, the detection of Anellovirus sequences at baseline independently predicted poor immune recovery, as did low CD4 T cell counts. The bacterial and bacteriophage populations were unique to each PWH with individualized trajectories; we found no discernable pattern of clustering after 24 months on ART.
Conclusion: Advanced HIV-1 infection was associated with marked alterations in the virome composition, in particular a remarkable expansion of human anelloviruses, with a gradual restoration after ART initiation. In addition to CD4 T cell counts, anellovirus sequence detection might be useful to predict and monitor immune recovery. This study confirms data on the bacteriome and expands our knowledge on the viral component of the gut microbiome in HIV-1 infection. Video Abstract.
背景:HIV-1 感染的特点是粘膜 CD4 T 细胞大量耗竭,从而引发一系列事件,最终将肠道微生物菌群失调与 HIV-1 疾病进展和发病机制联系起来。尽管病毒是肠道生态系统的重要组成部分,但 HIV 感染与肠道病毒组组成之间的关系却不太明确。在此,我们对 HIV 感染者(PWH)和 HIV 阴性个体的粪便病毒(真核病毒和噬菌体)和细菌微生物组进行了横断面分析。为了进一步了解肠道微生物组的组成、艾滋病相关免疫缺陷和免疫恢复之间的关系,我们开展了一项纵向研究,其中包括 14 名开始接受抗逆转录病毒疗法(ART)的艾滋病病毒感染者,并对他们进行了长达 24 个月的随访,在基线期(开始接受抗逆转录病毒疗法之前)和开始接受抗逆转录病毒疗法后的 2、6、12 和 24 个月进行采样:我们的数据显示,在患有严重免疫缺陷(CD4 结语)的 PWH 粪便样本中,几种人类病毒基因组序列(Anelloviridae、Adenoviridae 和 Papillomaviridae)的丰度和流行率显著增加:晚期 HIV-1 感染与病毒组组成的明显改变有关,尤其是人类无病毒科病毒的显著扩增,在开始接受抗逆转录病毒疗法后病毒组组成逐渐恢复。除了 CD4 T 细胞计数外,鼻疽病毒序列检测可能有助于预测和监测免疫恢复情况。这项研究证实了细菌组的数据,并扩展了我们对 HIV-1 感染者肠道微生物组病毒成分的认识。视频摘要。
{"title":"Alterations of the gut microbiome in HIV infection highlight human anelloviruses as potential predictors of immune recovery.","authors":"Celia Boukadida, Amy Peralta-Prado, Monserrat Chávez-Torres, Karla Romero-Mora, Alma Rincon-Rubio, Santiago Ávila-Ríos, Daniela Garrido-Rodríguez, Gustavo Reyes-Terán, Sandra Pinto-Cardoso","doi":"10.1186/s40168-024-01925-7","DOIUrl":"https://doi.org/10.1186/s40168-024-01925-7","url":null,"abstract":"<p><strong>Background: </strong>HIV-1 infection is characterized by a massive depletion of mucosal CD4 T cells that triggers a cascade of events ultimately linking gut microbial dysbiosis to HIV-1 disease progression and pathogenesis. The association between HIV infection and the enteric virome composition is less characterized, although viruses are an essential component of the gut ecosystem. Here, we performed a cross-sectional analysis of the fecal viral (eukaryotic viruses and bacteriophages) and bacterial microbiome in people with HIV (PWH) and in HIV-negative individuals. To gain further insight into the association between the gut microbiome composition, HIV-associated immunodeficiency, and immune recovery, we carried out a longitudinal study including 14 PWH who initiated antiretroviral therapy (ART) and were followed for 24 months with samplings performed at baseline (before ART) and at 2, 6, 12, and 24 months post-ART initiation.</p><p><strong>Results: </strong>Our data revealed a striking expansion in the abundance and prevalence of several human virus genomic sequences (Anelloviridae, Adenoviridae, and Papillomaviridae) in stool samples of PWH with severe immunodeficiency (CD4 < 200). We also noted a decreased abundance of sequences belonging to two plant viruses from the Tobamovirus genus, a reduction in bacterial alpha diversity, and a decrease in Inoviridae bacteriophage sequences. Short-term ART (24 months) was linked to a significant decrease in human Anelloviridae sequences. Remarkably, the detection of Anellovirus sequences at baseline independently predicted poor immune recovery, as did low CD4 T cell counts. The bacterial and bacteriophage populations were unique to each PWH with individualized trajectories; we found no discernable pattern of clustering after 24 months on ART.</p><p><strong>Conclusion: </strong>Advanced HIV-1 infection was associated with marked alterations in the virome composition, in particular a remarkable expansion of human anelloviruses, with a gradual restoration after ART initiation. In addition to CD4 T cell counts, anellovirus sequence detection might be useful to predict and monitor immune recovery. This study confirms data on the bacteriome and expands our knowledge on the viral component of the gut microbiome in HIV-1 infection. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11483978/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469528","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-17DOI: 10.1186/s40168-024-01926-6
Xinzhao Tong, Danli Luo, Marcus H Y Leung, Justin Y Y Lee, Zhiyong Shen, Wengyao Jiang, Christopher E Mason, Patrick K H Lee
Background: Built environments (BEs) are typically considered to be oligotrophic and harsh environments for microbial communities under normal, non-damp conditions. However, the metabolic functions of microbial inhabitants in BEs remain poorly understood. This study aimed to shed light on the functional capabilities of microbes in BEs by analyzing 860 representative metagenome-assembled genomes (rMAGs) reconstructed from 738 samples collected from BEs across the city of Hong Kong and from the skin surfaces of human occupants. The study specifically focused on the metabolic functions of rMAGs that are either phylogenetically novel or prevalent in BEs.
Results: The diversity and composition of BE microbiomes were primarily shaped by the sample type, with Micrococcus luteus and Cutibacterium acnes being prevalent. The metabolic functions of rMAGs varied significantly based on taxonomy, even at the strain level. A novel strain affiliated with the Candidatus class Xenobia in the Candidatus phylum Eremiobacterota and two novel strains affiliated with the superphylum Patescibacteria exhibited unique functions compared with their close relatives, potentially aiding their survival in BEs and on human skins. The novel strains in the class Xenobia possessed genes for transporting nitrate and nitrite as nitrogen sources and nitrosative stress mitigation induced by nitric oxide during denitrification. The two novel Patescibacteria strains both possessed a broad array of genes for amino acid and trace element transport, while one of them carried genes for carotenoid and ubiquinone biosynthesis. The globally prevalent M. luteus in BEs displayed a large and open pangenome, with high infraspecific genomic diversity contributed by 11 conspecific strains recovered from BEs in a single geographic region. The versatile metabolic functions encoded in the large accessory genomes of M. luteus may contribute to its global ubiquity and specialization in BEs.
Conclusions: This study illustrates that the microbial inhabitants of BEs possess metabolic potentials that enable them to tolerate and counter different biotic and abiotic conditions. Additionally, these microbes can efficiently utilize various limited residual resources from occupant activities, potentially enhancing their survival and persistence within BEs. A better understanding of the metabolic functions of BE microbes will ultimately facilitate the development of strategies to create a healthy indoor microbiome. Video Abstract.
背景:建筑环境(BE)通常被认为是微生物群落在正常、非潮湿条件下的低营养和恶劣环境。然而,人们对建筑环境中微生物群落的代谢功能仍然知之甚少。本研究旨在通过分析从全港 BE 和人类居住者皮肤表面采集的 738 个样本中重建的 860 个代表性元基因组(rMAGs),揭示 BE 中微生物的功能能力。研究特别关注了在系统发育上新颖或在 BE 中普遍存在的 rMAGs 的代谢功能:结果:BE 微生物组的多样性和组成主要受样本类型的影响,其中以黄体微球菌和痤疮杆菌最为普遍。rMAGs的代谢功能因分类而有很大差异,甚至在菌株水平上也是如此。与近亲相比,一种隶属于念珠菌门(Candidatus)Xenobia类的新型菌株和两种隶属于超细菌门(Patescibacteria)的新型菌株表现出独特的功能,这可能有助于它们在BE和人类皮肤上生存。Xenobia类中的新型菌株拥有转运硝酸盐和亚硝酸盐作为氮源的基因,以及在反硝化过程中由一氧化氮诱导的亚硝酸应激缓解基因。两株新型棒状杆菌都拥有一系列氨基酸和微量元素转运基因,其中一株携带类胡萝卜素和泛醌生物合成基因。在 BEs 中全球流行的黄体霉菌显示了一个庞大而开放的泛基因组,在单一地理区域的 BEs 中发现的 11 个同种菌株贡献了高度的种下基因组多样性。黄曲霉大型附属基因组所编码的多功能代谢功能可能是其在BEs中全球普遍存在和专业化的原因:这项研究表明,BEs 中的微生物居民具有新陈代谢潜能,能够耐受和对抗不同的生物和非生物条件。此外,这些微生物还能有效利用居住者活动产生的各种有限的残余资源,从而提高它们在 BEs 中的生存能力和持久性。更好地了解 BE 微生物的新陈代谢功能,最终将有助于制定创建健康室内微生物群的策略。视频摘要。
{"title":"Diverse and specialized metabolic capabilities of microbes in oligotrophic built environments.","authors":"Xinzhao Tong, Danli Luo, Marcus H Y Leung, Justin Y Y Lee, Zhiyong Shen, Wengyao Jiang, Christopher E Mason, Patrick K H Lee","doi":"10.1186/s40168-024-01926-6","DOIUrl":"https://doi.org/10.1186/s40168-024-01926-6","url":null,"abstract":"<p><strong>Background: </strong>Built environments (BEs) are typically considered to be oligotrophic and harsh environments for microbial communities under normal, non-damp conditions. However, the metabolic functions of microbial inhabitants in BEs remain poorly understood. This study aimed to shed light on the functional capabilities of microbes in BEs by analyzing 860 representative metagenome-assembled genomes (rMAGs) reconstructed from 738 samples collected from BEs across the city of Hong Kong and from the skin surfaces of human occupants. The study specifically focused on the metabolic functions of rMAGs that are either phylogenetically novel or prevalent in BEs.</p><p><strong>Results: </strong>The diversity and composition of BE microbiomes were primarily shaped by the sample type, with Micrococcus luteus and Cutibacterium acnes being prevalent. The metabolic functions of rMAGs varied significantly based on taxonomy, even at the strain level. A novel strain affiliated with the Candidatus class Xenobia in the Candidatus phylum Eremiobacterota and two novel strains affiliated with the superphylum Patescibacteria exhibited unique functions compared with their close relatives, potentially aiding their survival in BEs and on human skins. The novel strains in the class Xenobia possessed genes for transporting nitrate and nitrite as nitrogen sources and nitrosative stress mitigation induced by nitric oxide during denitrification. The two novel Patescibacteria strains both possessed a broad array of genes for amino acid and trace element transport, while one of them carried genes for carotenoid and ubiquinone biosynthesis. The globally prevalent M. luteus in BEs displayed a large and open pangenome, with high infraspecific genomic diversity contributed by 11 conspecific strains recovered from BEs in a single geographic region. The versatile metabolic functions encoded in the large accessory genomes of M. luteus may contribute to its global ubiquity and specialization in BEs.</p><p><strong>Conclusions: </strong>This study illustrates that the microbial inhabitants of BEs possess metabolic potentials that enable them to tolerate and counter different biotic and abiotic conditions. Additionally, these microbes can efficiently utilize various limited residual resources from occupant activities, potentially enhancing their survival and persistence within BEs. A better understanding of the metabolic functions of BE microbes will ultimately facilitate the development of strategies to create a healthy indoor microbiome. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11484240/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469532","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-15DOI: 10.1186/s40168-024-01930-w
Miguel de Celis, Javier Ruiz, Belen Benitez-Dominguez, Javier Vicente, Sandra Tomasi, Sergio Izquierdo-Gea, Nicolás Rozés, Candela Ruiz-de-Villa, Jordi Gombau, Fernando Zamora, Alicia Barroso-delJesus, Laura C Terron-Camero, Eduardo Andres-Leon, Antonio Santos, Ignacio Belda
Background: Connecting the composition and function of industrial microbiomes is a major aspiration in microbial biotechnology. Here, we address this question in wine fermentation, a model system where the diversity and functioning of fermenting yeast species are determinant of the flavor and quality of the resulting wines.
Results: First, we surveyed yeast communities associated with grape musts collected across wine appellations, revealing the importance of environmental (i.e., biogeography) and anthropic factors (i.e., farming system) in shaping community composition and structure. Then, we assayed the fermenting yeast communities in synthetic grape must under common winemaking conditions. The dominating yeast species defines the fermentation performance and metabolite profile of the resulting wines, and it is determined by the initial fungal community composition rather than the imposed fermentation conditions. Yeast dominance also had a more pronounced impact on wine meta-transcriptome than fermentation conditions. We unveiled yeast-specific transcriptomic profiles, leveraging different molecular functioning strategies in wine fermentation environments. We further studied the orthologs responsible for metabolite production, revealing modules associated with the dominance of specific yeast species. This emphasizes the unique contributions of yeast species to wine flavor, here summarized in an array of orthologs that defines the individual contribution of yeast species to wine ecosystem functioning.
Conclusions: Our study bridges the gap between yeast community composition and wine metabolite production, providing insights to harness diverse yeast functionalities with the final aim to producing tailored high-quality wines. Video Abstract.
{"title":"Multi-omics framework to reveal the molecular determinants of fermentation performance in wine yeast populations.","authors":"Miguel de Celis, Javier Ruiz, Belen Benitez-Dominguez, Javier Vicente, Sandra Tomasi, Sergio Izquierdo-Gea, Nicolás Rozés, Candela Ruiz-de-Villa, Jordi Gombau, Fernando Zamora, Alicia Barroso-delJesus, Laura C Terron-Camero, Eduardo Andres-Leon, Antonio Santos, Ignacio Belda","doi":"10.1186/s40168-024-01930-w","DOIUrl":"https://doi.org/10.1186/s40168-024-01930-w","url":null,"abstract":"<p><strong>Background: </strong>Connecting the composition and function of industrial microbiomes is a major aspiration in microbial biotechnology. Here, we address this question in wine fermentation, a model system where the diversity and functioning of fermenting yeast species are determinant of the flavor and quality of the resulting wines.</p><p><strong>Results: </strong>First, we surveyed yeast communities associated with grape musts collected across wine appellations, revealing the importance of environmental (i.e., biogeography) and anthropic factors (i.e., farming system) in shaping community composition and structure. Then, we assayed the fermenting yeast communities in synthetic grape must under common winemaking conditions. The dominating yeast species defines the fermentation performance and metabolite profile of the resulting wines, and it is determined by the initial fungal community composition rather than the imposed fermentation conditions. Yeast dominance also had a more pronounced impact on wine meta-transcriptome than fermentation conditions. We unveiled yeast-specific transcriptomic profiles, leveraging different molecular functioning strategies in wine fermentation environments. We further studied the orthologs responsible for metabolite production, revealing modules associated with the dominance of specific yeast species. This emphasizes the unique contributions of yeast species to wine flavor, here summarized in an array of orthologs that defines the individual contribution of yeast species to wine ecosystem functioning.</p><p><strong>Conclusions: </strong>Our study bridges the gap between yeast community composition and wine metabolite production, providing insights to harness diverse yeast functionalities with the final aim to producing tailored high-quality wines. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481383/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469616","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-15DOI: 10.1186/s40168-024-01856-3
Coral Barcenilla, José F Cobo-Díaz, Alba Puente, Vincenzo Valentino, Francesca De Filippis, Danilo Ercolini, Niccolò Carlino, Federica Pinto, Nicola Segata, Miguel Prieto, Mercedes López, Avelino Alvarez-Ordóñez
Background: Processing environments can be an important source of pathogenic and spoilage microorganisms that cross contaminate meat and meat products. The aim of this study was to characterize the microbiome of raw materials, processing environments and end products from 19 facilities producing different meat products.
Results: The taxonomic profiles of the microbial communities evolved along processing, from raw materials to end products, suggesting that food contact (FC) surfaces play an important role in modulating the microbiome of final products. Some species persisted with the highest relative abundance in raw materials, food processing environments and/or in the final product, including species from the genera Pseudomonas, Staphylococcus, Brochothrix, Acinetobacter and Psychrobacter. Processing environments showed a very diverse core microbiota, partially shared with the products. Pseudomonas fragi and Pseudomonas sp. Lz4W (in all sample and facility types) and Brochothrix thermosphacta, Psychrobacter sp. and Psychrobacter sp. P11F6 (in raw materials, FC surfaces and end products) were prominent members of the core microbiota for all facilities, while Latilactobacillus sakei was found as a dominant species exclusively in end products from the facilities producing fermented sausages. Processing environments showed a higher amount of antimicrobial resistance genes and virulence factors than raw materials and end products. One thousand four hundred twenty-one medium/high-quality metagenome-assembled genomes (MAGs) were reconstructed. Of these, 274 high-quality MAGs (completeness > 90%) corresponded to 210 putative new species, mostly found in processing environments. For two relevant taxa in meat curing and fermentation processes (S. equorum and L. sakei, respectively), phylogenetic variation was observed associated with the specific processing facility under study, which suggests that specific strains of these taxa may be selected in different meat processing plants, likely contributing to the peculiar sensorial traits of the end products produced in them.
Conclusions: Overall, our findings provide the most detailed metagenomics-based perspective up to now of the microbes that thrive in meat, meat products and associated environments and open avenues for future research activities to better understand the microbiome functionality and potential contribution to meat quality and safety. Video Abstract.
{"title":"In-depth characterization of food and environmental microbiomes across different meat processing plants.","authors":"Coral Barcenilla, José F Cobo-Díaz, Alba Puente, Vincenzo Valentino, Francesca De Filippis, Danilo Ercolini, Niccolò Carlino, Federica Pinto, Nicola Segata, Miguel Prieto, Mercedes López, Avelino Alvarez-Ordóñez","doi":"10.1186/s40168-024-01856-3","DOIUrl":"https://doi.org/10.1186/s40168-024-01856-3","url":null,"abstract":"<p><strong>Background: </strong>Processing environments can be an important source of pathogenic and spoilage microorganisms that cross contaminate meat and meat products. The aim of this study was to characterize the microbiome of raw materials, processing environments and end products from 19 facilities producing different meat products.</p><p><strong>Results: </strong>The taxonomic profiles of the microbial communities evolved along processing, from raw materials to end products, suggesting that food contact (FC) surfaces play an important role in modulating the microbiome of final products. Some species persisted with the highest relative abundance in raw materials, food processing environments and/or in the final product, including species from the genera Pseudomonas, Staphylococcus, Brochothrix, Acinetobacter and Psychrobacter. Processing environments showed a very diverse core microbiota, partially shared with the products. Pseudomonas fragi and Pseudomonas sp. Lz4W (in all sample and facility types) and Brochothrix thermosphacta, Psychrobacter sp. and Psychrobacter sp. P11F6 (in raw materials, FC surfaces and end products) were prominent members of the core microbiota for all facilities, while Latilactobacillus sakei was found as a dominant species exclusively in end products from the facilities producing fermented sausages. Processing environments showed a higher amount of antimicrobial resistance genes and virulence factors than raw materials and end products. One thousand four hundred twenty-one medium/high-quality metagenome-assembled genomes (MAGs) were reconstructed. Of these, 274 high-quality MAGs (completeness > 90%) corresponded to 210 putative new species, mostly found in processing environments. For two relevant taxa in meat curing and fermentation processes (S. equorum and L. sakei, respectively), phylogenetic variation was observed associated with the specific processing facility under study, which suggests that specific strains of these taxa may be selected in different meat processing plants, likely contributing to the peculiar sensorial traits of the end products produced in them.</p><p><strong>Conclusions: </strong>Overall, our findings provide the most detailed metagenomics-based perspective up to now of the microbes that thrive in meat, meat products and associated environments and open avenues for future research activities to better understand the microbiome functionality and potential contribution to meat quality and safety. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481301/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469555","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-15DOI: 10.1186/s40168-024-01917-7
João Felipe M Salgado, Vincent Hervé, Manuel A G Vera, Gaku Tokuda, Andreas Brune
Background: The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT.
Results: We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall.
Conclusions: The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT. Video Abstract.
{"title":"Unveiling lignocellulolytic potential: a genomic exploration of bacterial lineages within the termite gut.","authors":"João Felipe M Salgado, Vincent Hervé, Manuel A G Vera, Gaku Tokuda, Andreas Brune","doi":"10.1186/s40168-024-01917-7","DOIUrl":"https://doi.org/10.1186/s40168-024-01917-7","url":null,"abstract":"<p><strong>Background: </strong>The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT.</p><p><strong>Results: </strong>We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall.</p><p><strong>Conclusions: </strong>The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481507/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469619","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-15DOI: 10.1186/s40168-024-01928-4
Juan Li, Jiujie Li, Lili Cao, Qinghua Chen, Ding Ding, Le Kang
Background: Entomopathogenic fungal infection-induced dysbiosis of host microbiota offers a window into understanding the complex interactions between pathogenic fungi and host symbionts. Such insights are critical for enhancing the efficacy of mycoinsecticides. However, the utilization of these interactions in pest control remains largely unexplored.
Results: Here, we found that infection by the host-specialist fungus Metarhizium acridum alters the composition of the symbiotic microbiota and increases the dominance of some bacterial symbionts in locusts. Meanwhile, M. acridum also effectively limits the overgrowth of the predominant bacteria. Comparative transcriptomic screening revealed that the fungus upregulates the production of MaCFEM1, an iron-binding protein, in the presence of bacteria. This protein sequesters iron, thereby limiting its availability. Functionally, overexpression of MaCFEM1 in the fungus induces iron deprivation, which significantly suppresses bacterial growth. Conversely, MaCFEM1 knockout relieves the restriction on bacterial iron availability, resulting in iron reallocation. Upon ΔMaCFEM1 infection, some host bacterial symbionts proliferate uncontrollably, turning into opportunistic pathogens and significantly accelerating host death.
Conclusions: This study elucidates the critical role of pathogenic fungal-dominated iron allocation in mediating the shift of host microbes from symbiosis to pathogenicity. It also highlights a unique biocontrol strategy that jointly exploits pathogenic fungi and bacterial symbionts to increase host mortality. Video Abstract.
{"title":"An iron-binding protein of entomopathogenic fungus suppresses the proliferation of host symbiotic bacteria.","authors":"Juan Li, Jiujie Li, Lili Cao, Qinghua Chen, Ding Ding, Le Kang","doi":"10.1186/s40168-024-01928-4","DOIUrl":"https://doi.org/10.1186/s40168-024-01928-4","url":null,"abstract":"<p><strong>Background: </strong>Entomopathogenic fungal infection-induced dysbiosis of host microbiota offers a window into understanding the complex interactions between pathogenic fungi and host symbionts. Such insights are critical for enhancing the efficacy of mycoinsecticides. However, the utilization of these interactions in pest control remains largely unexplored.</p><p><strong>Results: </strong>Here, we found that infection by the host-specialist fungus Metarhizium acridum alters the composition of the symbiotic microbiota and increases the dominance of some bacterial symbionts in locusts. Meanwhile, M. acridum also effectively limits the overgrowth of the predominant bacteria. Comparative transcriptomic screening revealed that the fungus upregulates the production of MaCFEM1, an iron-binding protein, in the presence of bacteria. This protein sequesters iron, thereby limiting its availability. Functionally, overexpression of MaCFEM1 in the fungus induces iron deprivation, which significantly suppresses bacterial growth. Conversely, MaCFEM1 knockout relieves the restriction on bacterial iron availability, resulting in iron reallocation. Upon ΔMaCFEM1 infection, some host bacterial symbionts proliferate uncontrollably, turning into opportunistic pathogens and significantly accelerating host death.</p><p><strong>Conclusions: </strong>This study elucidates the critical role of pathogenic fungal-dominated iron allocation in mediating the shift of host microbes from symbiosis to pathogenicity. It also highlights a unique biocontrol strategy that jointly exploits pathogenic fungi and bacterial symbionts to increase host mortality. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481751/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469529","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}