Pub Date : 2024-10-24DOI: 10.1186/s40168-024-01902-0
Janina Rahlff, George Westmeijer, Julia Weissenbach, Alfred Antson, Karin Holmfeldt
Background: Aquatic viruses act as key players in shaping microbial communities. In polar environments, they face significant challenges such as limited host availability and harsh conditions. However, due to the restricted accessibility of these ecosystems, our understanding of viral diversity, abundance, adaptations, and host interactions remains limited.
Results: To fill this knowledge gap, we studied viruses from atmosphere-close aquatic ecosystems in the Central Arctic and Northern Greenland. Aquatic samples for virus-host analysis were collected from ~60 cm depth and the submillimeter surface microlayer (SML) during the Synoptic Arctic Survey 2021 on icebreaker Oden in the Arctic summer. Water was sampled from a melt pond and open water before undergoing size-fractioned filtration, followed by genome-resolved metagenomic and cultivation investigations. The prokaryotic diversity in the melt pond was considerably lower compared to that of open water. The melt pond was dominated by a Flavobacterium sp. and Aquiluna sp., the latter having a relatively small genome size of 1.2 Mb and the metabolic potential to generate ATP using the phosphate acetyltransferase-acetate kinase pathway. Viral diversity on the host fraction (0.2-5 µm) of the melt pond was strikingly limited compared to that of open water. From the 1154 viral operational taxonomic units (vOTUs), of which two-thirds were predicted bacteriophages, 17.2% encoded for auxiliary metabolic genes (AMGs) with metabolic functions. Some AMGs like glycerol-3-phosphate cytidylyltransferase and ice-binding like proteins might serve to provide cryoprotection for the host. Prophages were often associated with SML genomes, and two active prophages of new viral genera from the Arctic SML strain Leeuwenhoekiella aequorea Arc30 were induced. We found evidence that vOTU abundance in the SML compared to that of ~60 cm depth was more positively correlated with the distribution of a vOTU across five different Arctic stations.
Conclusions: The results indicate that viruses employ elaborate strategies to endure in extreme, host-limited environments. Moreover, our observations suggest that the immediate air-sea interface serves as a platform for viral distribution in the Central Arctic. Video Abstract.
{"title":"Surface microlayer-mediated virome dissemination in the Central Arctic.","authors":"Janina Rahlff, George Westmeijer, Julia Weissenbach, Alfred Antson, Karin Holmfeldt","doi":"10.1186/s40168-024-01902-0","DOIUrl":"10.1186/s40168-024-01902-0","url":null,"abstract":"<p><strong>Background: </strong>Aquatic viruses act as key players in shaping microbial communities. In polar environments, they face significant challenges such as limited host availability and harsh conditions. However, due to the restricted accessibility of these ecosystems, our understanding of viral diversity, abundance, adaptations, and host interactions remains limited.</p><p><strong>Results: </strong>To fill this knowledge gap, we studied viruses from atmosphere-close aquatic ecosystems in the Central Arctic and Northern Greenland. Aquatic samples for virus-host analysis were collected from ~60 cm depth and the submillimeter surface microlayer (SML) during the Synoptic Arctic Survey 2021 on icebreaker Oden in the Arctic summer. Water was sampled from a melt pond and open water before undergoing size-fractioned filtration, followed by genome-resolved metagenomic and cultivation investigations. The prokaryotic diversity in the melt pond was considerably lower compared to that of open water. The melt pond was dominated by a Flavobacterium sp. and Aquiluna sp., the latter having a relatively small genome size of 1.2 Mb and the metabolic potential to generate ATP using the phosphate acetyltransferase-acetate kinase pathway. Viral diversity on the host fraction (0.2-5 µm) of the melt pond was strikingly limited compared to that of open water. From the 1154 viral operational taxonomic units (vOTUs), of which two-thirds were predicted bacteriophages, 17.2% encoded for auxiliary metabolic genes (AMGs) with metabolic functions. Some AMGs like glycerol-3-phosphate cytidylyltransferase and ice-binding like proteins might serve to provide cryoprotection for the host. Prophages were often associated with SML genomes, and two active prophages of new viral genera from the Arctic SML strain Leeuwenhoekiella aequorea Arc30 were induced. We found evidence that vOTU abundance in the SML compared to that of ~60 cm depth was more positively correlated with the distribution of a vOTU across five different Arctic stations.</p><p><strong>Conclusions: </strong>The results indicate that viruses employ elaborate strategies to endure in extreme, host-limited environments. Moreover, our observations suggest that the immediate air-sea interface serves as a platform for viral distribution in the Central Arctic. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515562/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503492","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 : 2024-10-23DOI: 10.1186/s40168-024-01927-5
Stefano Levi Mortera, Valeria Marzano, Federica Rapisarda, Chiara Marangelo, Ilaria Pirona, Pamela Vernocchi, Marta Di Michele, Federica Del Chierico, Maria A Quintero, Irina Fernandez, Hajar Hazime, Rose M Killian, Norma Solis, Mailenys Ortega, Oriana M Damas, Siobhan Proksell, David H Kerman, Amar R Deshpande, Luis Garces, Franco Scaldaferri, Antonio Gasbarrini, Maria T Abreu, Lorenza Putignani
Background: Crohn's disease (CD) is characterized by chronic intestinal inflammation. Diet is a key modifiable factor influencing the gut microbiome (GM) and a risk factor for CD. However, the impact of diet modulation on GM function in CD patients is understudied. Herein, we evaluated the effect of a high-fiber, low-fat diet (the Mi-IBD diet) on GM function in CD patients. All participants were instructed to follow the Mi-IBD diet for 8 weeks. One group of CD patients received one-time diet counseling only (Gr1); catered food was supplied for the other three groups, including CD patients (Gr2) and dyads of CD patients and healthy household controls (HHCs) residing within the same household (Gr3-HHC dyads). Stool samples were collected at baseline, week 8, and week 36, and analyzed by liquid chromatography-tandem mass spectrometry.
Results: At baseline, the metaproteomic profiles of CD patients and HHCs differed. The Mi-IBD diet significantly increased carbohydrate and iron transport and metabolism. The predicted microbial composition underlying the metaproteomic changes differed between patients with ileal only disease (ICD) or colonic involvement: ICD was characterized by decreased Faecalibacterium abundance. Even on the Mi-IBD diet, the CD patient metaproteome displayed significant underrepresentation of carbohydrate and purine/pyrimidine synthesis pathways compared to that of HHCs. Human immune-related proteins were upregulated in CD patients compared to HHCs.
Conclusions: The Mi-IBD diet changed the microbial function of CD patients and enhanced carbohydrate metabolism. Our metaproteomic results highlight functional differences in the microbiome according to disease location. Notably, our dietary intervention yielded the most benefit for CD patients with colonic involvement compared to ileal-only disease. Video Abstract.
背景:克罗恩病(CD)以慢性肠道炎症为特征。饮食是影响肠道微生物组(GM)的一个关键可调节因素,也是克罗恩病的一个危险因素。然而,饮食调节对 CD 患者肠道微生物组功能的影响尚未得到充分研究。在此,我们评估了高纤维、低脂肪饮食(Mi-IBD 饮食)对 CD 患者肠道微生物组功能的影响。所有参与者都被要求遵循 Mi-IBD 饮食 8 周。其中一组 CD 患者只接受一次性饮食指导(Gr1);其他三组包括 CD 患者(Gr2)和居住在同一家庭中的 CD 患者和健康家庭对照组(HHCs)(Gr3-HHC dyads)。在基线、第8周和第36周收集粪便样本,并采用液相色谱-串联质谱法进行分析:结果:基线时,CD 患者和 HHC 的元蛋白组图谱不同。Mi-IBD饮食明显增加了碳水化合物和铁的转运和代谢。回肠疾病(ICD)或结肠受累患者的元蛋白组变化所依据的微生物组成预测不同:回肠疾病患者的粪便杆菌丰度降低。即使使用 Mi-IBD 饮食,CD 患者元蛋白质组中碳水化合物和嘌呤/嘧啶合成途径的代表性也明显低于 HHCs。与HHCs相比,CD患者的人类免疫相关蛋白上调:结论:Mi-IBD饮食改变了CD患者的微生物功能,促进了碳水化合物代谢。我们的元蛋白组学结果凸显了不同疾病部位微生物组的功能差异。值得注意的是,与单纯回肠疾病相比,我们的饮食干预对结肠受累的 CD 患者最有益。视频摘要。
{"title":"Metaproteomics reveals diet-induced changes in gut microbiome function according to Crohn's disease location.","authors":"Stefano Levi Mortera, Valeria Marzano, Federica Rapisarda, Chiara Marangelo, Ilaria Pirona, Pamela Vernocchi, Marta Di Michele, Federica Del Chierico, Maria A Quintero, Irina Fernandez, Hajar Hazime, Rose M Killian, Norma Solis, Mailenys Ortega, Oriana M Damas, Siobhan Proksell, David H Kerman, Amar R Deshpande, Luis Garces, Franco Scaldaferri, Antonio Gasbarrini, Maria T Abreu, Lorenza Putignani","doi":"10.1186/s40168-024-01927-5","DOIUrl":"10.1186/s40168-024-01927-5","url":null,"abstract":"<p><strong>Background: </strong>Crohn's disease (CD) is characterized by chronic intestinal inflammation. Diet is a key modifiable factor influencing the gut microbiome (GM) and a risk factor for CD. However, the impact of diet modulation on GM function in CD patients is understudied. Herein, we evaluated the effect of a high-fiber, low-fat diet (the Mi-IBD diet) on GM function in CD patients. All participants were instructed to follow the Mi-IBD diet for 8 weeks. One group of CD patients received one-time diet counseling only (Gr1); catered food was supplied for the other three groups, including CD patients (Gr2) and dyads of CD patients and healthy household controls (HHCs) residing within the same household (Gr3-HHC dyads). Stool samples were collected at baseline, week 8, and week 36, and analyzed by liquid chromatography-tandem mass spectrometry.</p><p><strong>Results: </strong>At baseline, the metaproteomic profiles of CD patients and HHCs differed. The Mi-IBD diet significantly increased carbohydrate and iron transport and metabolism. The predicted microbial composition underlying the metaproteomic changes differed between patients with ileal only disease (ICD) or colonic involvement: ICD was characterized by decreased Faecalibacterium abundance. Even on the Mi-IBD diet, the CD patient metaproteome displayed significant underrepresentation of carbohydrate and purine/pyrimidine synthesis pathways compared to that of HHCs. Human immune-related proteins were upregulated in CD patients compared to HHCs.</p><p><strong>Conclusions: </strong>The Mi-IBD diet changed the microbial function of CD patients and enhanced carbohydrate metabolism. Our metaproteomic results highlight functional differences in the microbiome according to disease location. Notably, our dietary intervention yielded the most benefit for CD patients with colonic involvement compared to ileal-only disease. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515613/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503491","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 : 2024-10-22DOI: 10.1186/s40168-024-01919-5
Claudio Díaz-García, Elena Moreno, Alba Talavera-Rodríguez, Lucía Martín-Fernández, Sara González-Bodí, Laura Martín-Pedraza, José A Pérez-Molina, Fernando Dronda, María José Gosalbes, Laura Luna, María Jesús Vivancos, Jaime Huerta-Cepas, Santiago Moreno, Sergio Serrano-Villar
Background: Despite effective antiretroviral therapy, people with HIV (PWH) experience persistent systemic inflammation and increased morbidity and mortality. Modulating the gut microbiome through fecal microbiota transplantation (FMT) represents a novel therapeutic strategy. We aimed to evaluate proteomic changes in inflammatory pathways following repeated, low-dose FMT versus placebo.
Methods: This double-masked, placebo-controlled pilot study assessed the proteomic impacts of weekly FMT versus placebo treatment over 8 weeks on systemic inflammation in 29 PWH receiving stable antiretroviral therapy (ART). Three stool donors with high Faecalibacterium and butyrate profiles were selected, and their individual stools were used for FMT capsule preparation. Proteomic changes in 345 inflammatory proteins in plasma were quantified using the proximity extension assay, with samples collected at baseline and at weeks 1, 8, and 24. Concurrently, we characterized shifts in the gut microbiota composition and annotated functions through shotgun metagenomics. We fitted generalized additive models to evaluate the dynamics of protein expression. We selected the most relevant proteins to explore their correlations with microbiome composition and functionality over time using linear mixed models.
Results: FMT significantly reduced the plasma levels of 45 inflammatory proteins, including established mortality predictors such as IL6 and TNF-α. We found notable reductions persisting up to 16 weeks after the final FMT procedure, including in the expression of proteins such as CCL20 and CD22. We identified changes in 46 proteins, including decreases in FT3LG, IL6, IL10RB, IL12B, and IL17A, which correlated with multiple bacterial species. We found that specific bacterial species within the Ruminococcaceae, Succinivibrionaceae, Prevotellaceae families, and the Clostridium genus, in addition to their associated genes and functions, were significantly correlated with changes in inflammatory markers.
Conclusions: Targeting the gut microbiome through FMT effectively decreased inflammatory proteins in PWH, with sustained effects. These findings suggest the potential of the microbiome as a therapeutic target to mitigate inflammation-related complications in this population, encouraging further research and development of microbiome-based interventions. Video Abstract.
{"title":"Fecal microbiota transplantation alters the proteomic landscape of inflammation in HIV: identifying bacterial drivers.","authors":"Claudio Díaz-García, Elena Moreno, Alba Talavera-Rodríguez, Lucía Martín-Fernández, Sara González-Bodí, Laura Martín-Pedraza, José A Pérez-Molina, Fernando Dronda, María José Gosalbes, Laura Luna, María Jesús Vivancos, Jaime Huerta-Cepas, Santiago Moreno, Sergio Serrano-Villar","doi":"10.1186/s40168-024-01919-5","DOIUrl":"https://doi.org/10.1186/s40168-024-01919-5","url":null,"abstract":"<p><strong>Background: </strong>Despite effective antiretroviral therapy, people with HIV (PWH) experience persistent systemic inflammation and increased morbidity and mortality. Modulating the gut microbiome through fecal microbiota transplantation (FMT) represents a novel therapeutic strategy. We aimed to evaluate proteomic changes in inflammatory pathways following repeated, low-dose FMT versus placebo.</p><p><strong>Methods: </strong>This double-masked, placebo-controlled pilot study assessed the proteomic impacts of weekly FMT versus placebo treatment over 8 weeks on systemic inflammation in 29 PWH receiving stable antiretroviral therapy (ART). Three stool donors with high Faecalibacterium and butyrate profiles were selected, and their individual stools were used for FMT capsule preparation. Proteomic changes in 345 inflammatory proteins in plasma were quantified using the proximity extension assay, with samples collected at baseline and at weeks 1, 8, and 24. Concurrently, we characterized shifts in the gut microbiota composition and annotated functions through shotgun metagenomics. We fitted generalized additive models to evaluate the dynamics of protein expression. We selected the most relevant proteins to explore their correlations with microbiome composition and functionality over time using linear mixed models.</p><p><strong>Results: </strong>FMT significantly reduced the plasma levels of 45 inflammatory proteins, including established mortality predictors such as IL6 and TNF-α. We found notable reductions persisting up to 16 weeks after the final FMT procedure, including in the expression of proteins such as CCL20 and CD22. We identified changes in 46 proteins, including decreases in FT3LG, IL6, IL10RB, IL12B, and IL17A, which correlated with multiple bacterial species. We found that specific bacterial species within the Ruminococcaceae, Succinivibrionaceae, Prevotellaceae families, and the Clostridium genus, in addition to their associated genes and functions, were significantly correlated with changes in inflammatory markers.</p><p><strong>Conclusions: </strong>Targeting the gut microbiome through FMT effectively decreased inflammatory proteins in PWH, with sustained effects. These findings suggest the potential of the microbiome as a therapeutic target to mitigate inflammation-related complications in this population, encouraging further research and development of microbiome-based interventions. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11494993/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503480","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 : 2024-10-22DOI: 10.1186/s40168-024-01920-y
Zhengtian Lyu, Gaoxiang Yuan, Yuying Zhang, Fengwenhui Zhang, Yan Liu, Yifan Li, Guang Li, Ying Wang, Ming Zhang, Yongfei Hu, Yuming Guo, Dan Liu
Background: The gut microbiota is a key regulator of bone metabolism. Investigating the relationship between the gut microbiota and bone remodeling has revealed new avenues for the treatment of bone-related disorders. Despite significant progress in understanding gut microbiota-bone interactions in mammals, research on avian species remains limited. Birds have unique bone anatomy and physiology to support egg-laying. However, whether and how the gut microbiota affects bone physiology in birds is still unknown. In this study, we utilized laying hens as a research model to analyze bone development patterns, elucidate the relationships between bone and the gut microbiota, and mine probiotics with osteomodulatory effects.
Results: Aging led to a continuous increase in bone mineral density in the femur of laying hens. The continuous deposition of medullary bone in the bone marrow cavity of aged laying hens led to significant trabecular bone loss and weakened bone metabolism. The cecal microbial composition significantly shifted before and after sexual maturity, with some genera within the class Clostridia potentially linked to postnatal bone development in laying hens. Four bacterial strains associated with bone development, namely Blautia coccoides CML164, Fournierella sp002159185 CML151, Anaerostipes caccae CML199 (ANA), and Romboutsia lituseburensis CML137, were identified and assessed in chicks with low bacterial loads and chicken primary osteoblasts. Among these, ANA demonstrated the most significant promotion of bone formation both in vivo and in vitro, primarily attributed to butyrate in its fermentation products. A long-term feeding experiment of up to 72 weeks confirmed that ANA enhanced bone development during sexual maturity by improving the immune microenvironment of the bone marrow in laying hens. Dietary supplementation of ANA for 50 weeks prevented excessive medullary bone deposition and mitigated aging-induced trabecular bone loss.
Conclusions: These findings highlight the beneficial effects of ANA on bone physiology, offering new perspectives for microbial-based interventions for bone-related disorders in both poultry and possibly extending to human health. Video Abstract.
背景:肠道微生物群是骨代谢的关键调节因子。研究肠道微生物群与骨骼重塑之间的关系为治疗骨骼相关疾病提供了新途径。尽管在了解哺乳动物肠道微生物群与骨骼相互作用方面取得了重大进展,但对鸟类物种的研究仍然有限。鸟类具有独特的骨骼解剖和生理结构,以支持产蛋。然而,肠道微生物群是否以及如何影响鸟类的骨骼生理机能仍是未知数。在这项研究中,我们利用蛋鸡作为研究模型,分析骨骼发育模式,阐明骨骼与肠道微生物群之间的关系,并挖掘具有骨调节作用的益生菌:结果:衰老导致蛋鸡股骨中的骨矿物质密度持续增加。老龄蛋鸡骨髓腔中髓质骨的持续沉积导致骨小梁显著流失和骨代谢减弱。性成熟前后盲肠微生物组成发生了显著变化,梭菌属中的一些菌属可能与蛋鸡出生后的骨骼发育有关。在细菌负荷较低的雏鸡和鸡初级成骨细胞中鉴定并评估了与骨骼发育相关的四种细菌菌株,即Blautia coccoides CML164、Fournierella sp002159185 CML151、Anaerostipes caccae CML199(ANA)和Romboutsia lituseburensis CML137。其中,ANA 对体内和体外骨形成的促进作用最为显著,这主要归功于其发酵产物中的丁酸盐。一项长达 72 周的长期饲喂实验证实,ANA 通过改善蛋鸡骨髓的免疫微环境,促进了性成熟期间的骨骼发育。连续 50 周膳食补充 ANA 可防止髓质骨过度沉积,并减轻衰老引起的小梁骨质流失:这些发现强调了 ANA 对骨生理学的有益影响,为基于微生物的家禽骨相关疾病干预提供了新的视角,并可能扩展到人类健康。视频摘要。
{"title":"Anaerostipes caccae CML199 enhances bone development and counteracts aging-induced bone loss through the butyrate-driven gut-bone axis: the chicken model.","authors":"Zhengtian Lyu, Gaoxiang Yuan, Yuying Zhang, Fengwenhui Zhang, Yan Liu, Yifan Li, Guang Li, Ying Wang, Ming Zhang, Yongfei Hu, Yuming Guo, Dan Liu","doi":"10.1186/s40168-024-01920-y","DOIUrl":"https://doi.org/10.1186/s40168-024-01920-y","url":null,"abstract":"<p><strong>Background: </strong>The gut microbiota is a key regulator of bone metabolism. Investigating the relationship between the gut microbiota and bone remodeling has revealed new avenues for the treatment of bone-related disorders. Despite significant progress in understanding gut microbiota-bone interactions in mammals, research on avian species remains limited. Birds have unique bone anatomy and physiology to support egg-laying. However, whether and how the gut microbiota affects bone physiology in birds is still unknown. In this study, we utilized laying hens as a research model to analyze bone development patterns, elucidate the relationships between bone and the gut microbiota, and mine probiotics with osteomodulatory effects.</p><p><strong>Results: </strong>Aging led to a continuous increase in bone mineral density in the femur of laying hens. The continuous deposition of medullary bone in the bone marrow cavity of aged laying hens led to significant trabecular bone loss and weakened bone metabolism. The cecal microbial composition significantly shifted before and after sexual maturity, with some genera within the class Clostridia potentially linked to postnatal bone development in laying hens. Four bacterial strains associated with bone development, namely Blautia coccoides CML164, Fournierella sp002159185 CML151, Anaerostipes caccae CML199 (ANA), and Romboutsia lituseburensis CML137, were identified and assessed in chicks with low bacterial loads and chicken primary osteoblasts. Among these, ANA demonstrated the most significant promotion of bone formation both in vivo and in vitro, primarily attributed to butyrate in its fermentation products. A long-term feeding experiment of up to 72 weeks confirmed that ANA enhanced bone development during sexual maturity by improving the immune microenvironment of the bone marrow in laying hens. Dietary supplementation of ANA for 50 weeks prevented excessive medullary bone deposition and mitigated aging-induced trabecular bone loss.</p><p><strong>Conclusions: </strong>These findings highlight the beneficial effects of ANA on bone physiology, offering new perspectives for microbial-based interventions for bone-related disorders in both poultry and possibly extending to human health. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495078/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503479","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 maternal gut microbiome is the direct and important source of early colonization and development of the neonatal gut microbiome. However, differences in unique and shared features between mothers with different physiological phenotypes and their newborns still lack exhaustive investigation. Here, using a cow-to-calf model, a comprehensive investigation was conducted to elucidate the pattern and characterization of microbial transfer from the maternal source to the offspring.
Results: The microbiota in the rumen and feces of dairy cows were divided into two clusters via enterotype analysis. The cows from the enterotype distinguished by Prevotella in the rumen had better production performance, whereas no difference was observed in the cows classified by feces enterotype. Furthermore, through a pairwise combination of fecal and ruminal enterotypes, we screened a group of dairy cows with excellent phenotypes. The gastrointestinal microbiomes of cows with different phenotypes and their offspring differed significantly. The rumen was a more important microbial source for meconium than feces. Transmission of beneficial bacteria from mother to offspring was observed. Additionally, the meconium inherits advantageous metabolic functions of the rumen. The resistome features of the rumen, feces, and meconium were consistent, and resistome abundance from cows to calves showed an expanding trend. The interaction between antibiotic-resistance genes and mobile genetic elements from the rumen to meconium was the most remarkable. The diversity of core metabolites from cows to calves was stable and not affected by differences in phenotypes. However, the abundance of specific metabolites varied greatly.
Conclusions: Our study demonstrates the microbial taxa, metabolic function, and resistome characteristics of maternal and neonatal microbiomes, and reveals the potential vertical transmission of the microbiome from a cow-to-calf model. These findings provide new insights into the transgenerational transmission pattern of the microbiome. Video Abstract.
{"title":"Maternal gastrointestinal microbiome shapes gut microbial function and resistome of newborns in a cow-to-calf model.","authors":"Yimin Zhuang, Shuai Liu, Duo Gao, Yiming Xu, Wen Jiang, Guobin Hou, Sumin Li, Xinjie Zhao, Tianyu Chen, Shangru Li, Siyuan Zhang, Yanting Huang, Jingjun Wang, Jianxin Xiao, Mengmeng Li, Wei Wang, Shengli Li, Zhijun Cao","doi":"10.1186/s40168-024-01943-5","DOIUrl":"https://doi.org/10.1186/s40168-024-01943-5","url":null,"abstract":"<p><strong>Background: </strong>The maternal gut microbiome is the direct and important source of early colonization and development of the neonatal gut microbiome. However, differences in unique and shared features between mothers with different physiological phenotypes and their newborns still lack exhaustive investigation. Here, using a cow-to-calf model, a comprehensive investigation was conducted to elucidate the pattern and characterization of microbial transfer from the maternal source to the offspring.</p><p><strong>Results: </strong>The microbiota in the rumen and feces of dairy cows were divided into two clusters via enterotype analysis. The cows from the enterotype distinguished by Prevotella in the rumen had better production performance, whereas no difference was observed in the cows classified by feces enterotype. Furthermore, through a pairwise combination of fecal and ruminal enterotypes, we screened a group of dairy cows with excellent phenotypes. The gastrointestinal microbiomes of cows with different phenotypes and their offspring differed significantly. The rumen was a more important microbial source for meconium than feces. Transmission of beneficial bacteria from mother to offspring was observed. Additionally, the meconium inherits advantageous metabolic functions of the rumen. The resistome features of the rumen, feces, and meconium were consistent, and resistome abundance from cows to calves showed an expanding trend. The interaction between antibiotic-resistance genes and mobile genetic elements from the rumen to meconium was the most remarkable. The diversity of core metabolites from cows to calves was stable and not affected by differences in phenotypes. However, the abundance of specific metabolites varied greatly.</p><p><strong>Conclusions: </strong>Our study demonstrates the microbial taxa, metabolic function, and resistome characteristics of maternal and neonatal microbiomes, and reveals the potential vertical transmission of the microbiome from a cow-to-calf model. These findings provide new insights into the transgenerational transmission pattern of the microbiome. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495063/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503481","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 : 2024-10-22DOI: 10.1186/s40168-024-01913-x
Ralf Rosenstein, Benjamin O Torres Salazar, Claudia Sauer, Simon Heilbronner, Bernhard Krismer, Andreas Peschel
Background: Bacterial pathogens such as Staphylococcus aureus colonize body surfaces of part of the human population, which represents a critical risk factor for skin disorders and invasive infections. However, such pathogens do not belong to the human core microbiomes. Beneficial commensal bacteria can often prevent the invasion and persistence of such pathogens by using molecular strategies that are only superficially understood. We recently reported that the commensal bacterium Staphylococcus lugdunensis produces the novel antibiotic lugdunin, which eradicates S. aureus from the nasal microbiomes of hospitalized patients. However, it has remained unclear if S. lugdunensis may affect S. aureus carriage in the general population and which external factors might promote S. lugdunensis carriage to enhance its S. aureus-eliminating capacity.
Results: We could cultivate S. lugdunensis from the noses of 6.3% of healthy human volunteers. In addition, S. lugdunensis DNA could be identified in metagenomes of many culture-negative nasal samples indicating that cultivation success depends on a specific bacterial threshold density. Healthy S. lugdunensis carriers had a 5.2-fold lower propensity to be colonized by S. aureus indicating that lugdunin can eliminate S. aureus also in healthy humans. S. lugdunensis-positive microbiomes were dominated by either Staphylococcus epidermidis, Corynebacterium species, or Dolosigranulum pigrum. These and further bacterial commensals, whose abundance was positively associated with S. lugdunensis, promoted S. lugdunensis growth in co-culture. Such mutualistic interactions depended on the production of iron-scavenging siderophores by supportive commensals and on the capacity of S. lugdunensis to import siderophores. Video Abstract CONCLUSIONS: These findings underscore the importance of microbiome homeostasis for eliminating pathogen colonization. Elucidating mechanisms that drive microbiome interactions will become crucial for microbiome-precision editing approaches.
背景:金黄色葡萄球菌等细菌病原体定植于部分人群的体表,是导致皮肤病和侵入性感染的重要风险因素。然而,这类病原体并不属于人类核心微生物组。有益的共生细菌通常可以利用分子策略阻止这类病原体的入侵和持续存在,但人们对这些策略的了解还很肤浅。我们最近报告说,共生细菌卢格杜恩葡萄球菌能产生新型抗生素卢格杜宁,它能根除住院患者鼻腔微生物组中的金黄色葡萄球菌。然而,目前仍不清楚卢格杜菌是否会影响普通人群中的金黄色葡萄球菌携带,以及哪些外部因素可能会促进卢格杜菌的携带,从而增强其消灭金黄色葡萄球菌的能力:结果:我们可以从 6.3% 的健康志愿者鼻腔中培养出卢格登氏菌。此外,在许多培养阴性的鼻腔样本的元基因组中可以鉴定出 S. lugdunensis DNA,这表明培养成功与否取决于特定的细菌阈值密度。健康的 S. lugdunensis 携带者被金黄色葡萄球菌定植的可能性降低了 5.2 倍,这表明 lugdunin 也能消灭健康人体内的金黄色葡萄球菌。卢格杜氏菌阳性微生物组主要由表皮葡萄球菌、棒状杆菌或猪多糖所组成。这些细菌和其他细菌共生体(其丰度与 S. lugdunensis 呈正相关)在共培养中促进了 S. lugdunensis 的生长。这种互利的相互作用取决于支持性共生菌产生的铁清除嗜苷酸盐以及卢格氏菌输入嗜苷酸盐的能力。视频摘要 结论:这些发现强调了微生物组平衡对消除病原体定植的重要性。阐明驱动微生物组相互作用的机制将成为微生物组精确编辑方法的关键。
{"title":"The Staphylococcus aureus-antagonizing human nasal commensal Staphylococcus lugdunensis depends on siderophore piracy.","authors":"Ralf Rosenstein, Benjamin O Torres Salazar, Claudia Sauer, Simon Heilbronner, Bernhard Krismer, Andreas Peschel","doi":"10.1186/s40168-024-01913-x","DOIUrl":"https://doi.org/10.1186/s40168-024-01913-x","url":null,"abstract":"<p><strong>Background: </strong>Bacterial pathogens such as Staphylococcus aureus colonize body surfaces of part of the human population, which represents a critical risk factor for skin disorders and invasive infections. However, such pathogens do not belong to the human core microbiomes. Beneficial commensal bacteria can often prevent the invasion and persistence of such pathogens by using molecular strategies that are only superficially understood. We recently reported that the commensal bacterium Staphylococcus lugdunensis produces the novel antibiotic lugdunin, which eradicates S. aureus from the nasal microbiomes of hospitalized patients. However, it has remained unclear if S. lugdunensis may affect S. aureus carriage in the general population and which external factors might promote S. lugdunensis carriage to enhance its S. aureus-eliminating capacity.</p><p><strong>Results: </strong>We could cultivate S. lugdunensis from the noses of 6.3% of healthy human volunteers. In addition, S. lugdunensis DNA could be identified in metagenomes of many culture-negative nasal samples indicating that cultivation success depends on a specific bacterial threshold density. Healthy S. lugdunensis carriers had a 5.2-fold lower propensity to be colonized by S. aureus indicating that lugdunin can eliminate S. aureus also in healthy humans. S. lugdunensis-positive microbiomes were dominated by either Staphylococcus epidermidis, Corynebacterium species, or Dolosigranulum pigrum. These and further bacterial commensals, whose abundance was positively associated with S. lugdunensis, promoted S. lugdunensis growth in co-culture. Such mutualistic interactions depended on the production of iron-scavenging siderophores by supportive commensals and on the capacity of S. lugdunensis to import siderophores. Video Abstract CONCLUSIONS: These findings underscore the importance of microbiome homeostasis for eliminating pathogen colonization. Elucidating mechanisms that drive microbiome interactions will become crucial for microbiome-precision editing approaches.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495082/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503494","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 : 2024-10-21DOI: 10.1186/s40168-024-01914-w
Xingang Zhou, Jingyu Zhang, Jibo Shi, Muhammad Khashi U Rahman, Hongwei Liu, Zhong Wei, Fengzhi Wu, Francisco Dini-Andreote
Background: Volatile organic compounds (VOCs) released by plants can act as signaling molecules mediating ecological interactions. Therefore, the study of VOCs mediated intra- and interspecific interactions with downstream plant physiological responses is critical to advance our understanding of mechanisms underlying information exchange in plants. Here, we investigated how plant-emitted VOCs affect the performance of an interspecific neighboring plant via induced shifts in root exudate chemistry with implications for root-associated microbiota recruitment.
Results: First, we showed that VOCs emitted by potato-onion plants stimulate the growth of adjacent tomato plants. Then, we demonstrated that this positive effect on tomato biomass was attributed to shifts in the tomato rhizosphere microbiota. Specifically, we found potato-onion VOCs to indirectly affect the recruitment of specific bacteria (e.g., Pseudomonas and Bacillus spp.) in the tomato rhizosphere. Second, we identified and validated the compound dipropyl disulfide as the active molecule within the blend of potato-onion VOCs mediating this interspecific plant communication. Third, we showed that the effect on the tomato rhizosphere microbiota occurs via induced changes in root exudates of tomato plants caused by exposure to dipropyl disulfide. Last, Pseudomonas and Bacillus spp. bacteria enriched in the tomato rhizosphere were shown to have plant growth-promoting activities.
Conclusions: Potato-onion VOCs-specifically dipropyl disulfide-can induce shifts in the root exudate of adjacent tomato plants, which results in the recruitment of plant-beneficial bacteria in the rhizosphere. Taken together, this study elucidated a new mechanism of interspecific plant interaction mediated by VOCs resulting in alterations in the rhizosphere microbiota with beneficial outcomes for plant performance. Video Abstract.
{"title":"Volatile-mediated interspecific plant interaction promotes root colonization by beneficial bacteria via induced shifts in root exudation.","authors":"Xingang Zhou, Jingyu Zhang, Jibo Shi, Muhammad Khashi U Rahman, Hongwei Liu, Zhong Wei, Fengzhi Wu, Francisco Dini-Andreote","doi":"10.1186/s40168-024-01914-w","DOIUrl":"10.1186/s40168-024-01914-w","url":null,"abstract":"<p><strong>Background: </strong>Volatile organic compounds (VOCs) released by plants can act as signaling molecules mediating ecological interactions. Therefore, the study of VOCs mediated intra- and interspecific interactions with downstream plant physiological responses is critical to advance our understanding of mechanisms underlying information exchange in plants. Here, we investigated how plant-emitted VOCs affect the performance of an interspecific neighboring plant via induced shifts in root exudate chemistry with implications for root-associated microbiota recruitment.</p><p><strong>Results: </strong>First, we showed that VOCs emitted by potato-onion plants stimulate the growth of adjacent tomato plants. Then, we demonstrated that this positive effect on tomato biomass was attributed to shifts in the tomato rhizosphere microbiota. Specifically, we found potato-onion VOCs to indirectly affect the recruitment of specific bacteria (e.g., Pseudomonas and Bacillus spp.) in the tomato rhizosphere. Second, we identified and validated the compound dipropyl disulfide as the active molecule within the blend of potato-onion VOCs mediating this interspecific plant communication. Third, we showed that the effect on the tomato rhizosphere microbiota occurs via induced changes in root exudates of tomato plants caused by exposure to dipropyl disulfide. Last, Pseudomonas and Bacillus spp. bacteria enriched in the tomato rhizosphere were shown to have plant growth-promoting activities.</p><p><strong>Conclusions: </strong>Potato-onion VOCs-specifically dipropyl disulfide-can induce shifts in the root exudate of adjacent tomato plants, which results in the recruitment of plant-beneficial bacteria in the rhizosphere. Taken together, this study elucidated a new mechanism of interspecific plant interaction mediated by VOCs resulting in alterations in the rhizosphere microbiota with beneficial outcomes for plant performance. 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/PMC11492557/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469621","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 disease resistance phenotype is closely related to immunomodulatory function and immune tolerance and has far-reaching implications in animal husbandry and human health. Microbes play an important role in the initiation, prevention, and treatment of diseases, but the mechanisms of host-microbiota interactions in disease-resistant phenotypes are poorly understood. In this study, we hope to uncover and explain the role of microbes in intestinal diseases and their mechanisms of action to identify new potential treatments.
Methods: First, we established the colitis model of DSS in two breeds of sheep and then collected the samples for multi-omics testing including metagenes, metabolome, and transcriptome. Next, we made the fecal bacteria liquid from the four groups of sheep feces collected from H-CON, H-DSS, E-CON, and E-DSS to transplant the fecal bacteria into mice. H-CON feces were transplanted into mice named HH group and H-DSS feces were transplanted into mice named HD group and Roseburia bacteria treatment named HDR groups. E-CON feces were transplanted into mice named EH group and E-DSS feces were transplanted into mice in the ED group and Roseburia bacteria treatment named EDR groups. After successful modeling, samples were taken for multi-omics testing. Finally, colitis mice in HD group and ED group were administrated with Roseburia bacteria, and the treatment effect was evaluated by H&E, PAS, immunohistochemistry, and other experimental methods.
Results: The difference in disease resistance of sheep to DSS-induced colitis disease is mainly due to the increase in the abundance of Roseburia bacteria and the increase of bile acid secretion in the intestinal tract of Hu sheep in addition to the accumulation of potentially harmful bacteria in the intestine when the disease occurs, which makes the disease resistance of Hu sheep stronger under the same disease conditions. However, the enrichment of harmful microorganisms in East Friesian sheep activated the TNFα signalling pathway, which aggravated the intestinal injury, and then the treatment of FMT mice by culturing Roseburia bacteria found that Roseburia bacteria had a good curative effect on colitis.
Conclusion: Our study showed that in H-DSS-treated sheep, the intestinal barrier is stabilized with an increase in the abundance of beneficial microorganisms. Our data also suggest that Roseburia bacteria have a protective effect on the intestinal barrier of Hu sheep. Accumulating evidence suggests that host-microbiota interactions are associated with IBD disease progression. Video Abstract.
{"title":"Host-microbe interaction-mediated resistance to DSS-induced inflammatory enteritis in sheep.","authors":"Shuo Yan, Ruilin Du, Wenna Yao, Huimin Zhang, Yue Xue, Teligun, Yongfa Li, Hanggai Bao, Yulong Zhao, Shuo Cao, Guifang Cao, Xihe Li, Siqin Bao, Yongli Song","doi":"10.1186/s40168-024-01932-8","DOIUrl":"10.1186/s40168-024-01932-8","url":null,"abstract":"<p><strong>Background: </strong>The disease resistance phenotype is closely related to immunomodulatory function and immune tolerance and has far-reaching implications in animal husbandry and human health. Microbes play an important role in the initiation, prevention, and treatment of diseases, but the mechanisms of host-microbiota interactions in disease-resistant phenotypes are poorly understood. In this study, we hope to uncover and explain the role of microbes in intestinal diseases and their mechanisms of action to identify new potential treatments.</p><p><strong>Methods: </strong>First, we established the colitis model of DSS in two breeds of sheep and then collected the samples for multi-omics testing including metagenes, metabolome, and transcriptome. Next, we made the fecal bacteria liquid from the four groups of sheep feces collected from H-CON, H-DSS, E-CON, and E-DSS to transplant the fecal bacteria into mice. H-CON feces were transplanted into mice named HH group and H-DSS feces were transplanted into mice named HD group and Roseburia bacteria treatment named HDR groups. E-CON feces were transplanted into mice named EH group and E-DSS feces were transplanted into mice in the ED group and Roseburia bacteria treatment named EDR groups. After successful modeling, samples were taken for multi-omics testing. Finally, colitis mice in HD group and ED group were administrated with Roseburia bacteria, and the treatment effect was evaluated by H&E, PAS, immunohistochemistry, and other experimental methods.</p><p><strong>Results: </strong>The difference in disease resistance of sheep to DSS-induced colitis disease is mainly due to the increase in the abundance of Roseburia bacteria and the increase of bile acid secretion in the intestinal tract of Hu sheep in addition to the accumulation of potentially harmful bacteria in the intestine when the disease occurs, which makes the disease resistance of Hu sheep stronger under the same disease conditions. However, the enrichment of harmful microorganisms in East Friesian sheep activated the TNFα signalling pathway, which aggravated the intestinal injury, and then the treatment of FMT mice by culturing Roseburia bacteria found that Roseburia bacteria had a good curative effect on colitis.</p><p><strong>Conclusion: </strong>Our study showed that in H-DSS-treated sheep, the intestinal barrier is stabilized with an increase in the abundance of beneficial microorganisms. Our data also suggest that Roseburia bacteria have a protective effect on the intestinal barrier of Hu sheep. Accumulating evidence suggests that host-microbiota interactions are associated with IBD disease progression. 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/PMC11492479/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469533","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 : 2024-10-21DOI: 10.1186/s40168-024-01934-6
Tong Wang, Nannan Zhou, Feifei Ding, Zhenzhen Hao, Jorge Galindo-Villegas, Zhenyu Du, Xiaoyun Su, Meiling Zhang
Background: Commensal bacteria in the intestine release enzymes to degrade and ferment dietary components, producing beneficial metabolites. However, the regulatory effects of microbial-derived enzymes on the intestinal microbiota composition and the influence on host health remain elusive. Xylanase can degrade xylan into oligosaccharides, showing wide application in feed industry.
Results: To validate the immune-protective effects of xylanase, Nile tilapia was used as the model and fed with xylanase. The results showed that dietary xylanase improved the survival rate of Nile tilapia when they were challenged with Aeromonas hydrophila. The transcriptome analysis showed significant enrichment of genes related to interleukin-17d (il-17d) signaling pathway in the xylanase treatment group. High-throughput sequencing revealed that dietary xylanase altered the composition of the intestinal microbiota and directly promoted the proliferation of Allobaculum stercoricanis which could produce butyrate in vitro. Consequently, dietary xylanase supplementation increased the butyrate level in fish gut. Further experiment verified that butyrate supplementation enhanced the expression of il-17d and regenerating islet-derived 3 gamma (reg3g) in the gut. The knockdown experiment of il-17d confirmed that il-17d is necessary for butyrate to protect Nile tilapia from pathogen resistance. Flow cytometry analysis indicated that butyrate increased the abundance of IL-17D+ intestinal epithelial cells in fish. Mechanistically, butyrate functions as an HDAC3 inhibitor, enhancing il-17d expression and playing a crucial role in pathogen resistance.
Conclusion: Dietary xylanase significantly altered the composition of intestinal microbiota and increased the content of butyrate in the intestine. Butyrate activated the transcription of il-17d in intestinal epithelial cells by inhibiting histone deacetylase 3, thereby protecting the Nile tilapia from pathogen infection. This study elucidated how microbial-derived xylanase regulates host immune function, providing a theoretical basis for the development and application of functional enzymes. Video Abstract.
{"title":"Xylanase enhances gut microbiota-derived butyrate to exert immune-protective effects in a histone deacetylase-dependent manner.","authors":"Tong Wang, Nannan Zhou, Feifei Ding, Zhenzhen Hao, Jorge Galindo-Villegas, Zhenyu Du, Xiaoyun Su, Meiling Zhang","doi":"10.1186/s40168-024-01934-6","DOIUrl":"10.1186/s40168-024-01934-6","url":null,"abstract":"<p><strong>Background: </strong>Commensal bacteria in the intestine release enzymes to degrade and ferment dietary components, producing beneficial metabolites. However, the regulatory effects of microbial-derived enzymes on the intestinal microbiota composition and the influence on host health remain elusive. Xylanase can degrade xylan into oligosaccharides, showing wide application in feed industry.</p><p><strong>Results: </strong>To validate the immune-protective effects of xylanase, Nile tilapia was used as the model and fed with xylanase. The results showed that dietary xylanase improved the survival rate of Nile tilapia when they were challenged with Aeromonas hydrophila. The transcriptome analysis showed significant enrichment of genes related to interleukin-17d (il-17d) signaling pathway in the xylanase treatment group. High-throughput sequencing revealed that dietary xylanase altered the composition of the intestinal microbiota and directly promoted the proliferation of Allobaculum stercoricanis which could produce butyrate in vitro. Consequently, dietary xylanase supplementation increased the butyrate level in fish gut. Further experiment verified that butyrate supplementation enhanced the expression of il-17d and regenerating islet-derived 3 gamma (reg3g) in the gut. The knockdown experiment of il-17d confirmed that il-17d is necessary for butyrate to protect Nile tilapia from pathogen resistance. Flow cytometry analysis indicated that butyrate increased the abundance of IL-17D<sup>+</sup> intestinal epithelial cells in fish. Mechanistically, butyrate functions as an HDAC3 inhibitor, enhancing il-17d expression and playing a crucial role in pathogen resistance.</p><p><strong>Conclusion: </strong>Dietary xylanase significantly altered the composition of intestinal microbiota and increased the content of butyrate in the intestine. Butyrate activated the transcription of il-17d in intestinal epithelial cells by inhibiting histone deacetylase 3, thereby protecting the Nile tilapia from pathogen infection. This study elucidated how microbial-derived xylanase regulates host immune function, providing a theoretical basis for the development and application of functional enzymes. 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/PMC11492574/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469623","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 : 2024-10-21DOI: 10.1186/s40168-024-01918-6
Ciara Keating, Elizabeth Kilbride, Mark A Stalham, Charlotte Nellist, Joel Milner, Sonia Humphris, Ian Toth, Barbara K Mable, Umer Zeeshan Ijaz
Background: Understanding the interaction between environmental conditions, crop yields, and soil health is crucial for sustainable agriculture in a changing climate. Management practices to limit disease are a balancing act. For example, in potato production, dry conditions favour common scab (Streptomyces spp.) and wet conditions favour blackleg disease (Pectobacterium spp.). The exact mechanisms involved and how these link to changes in the soil microbiome are unclear. Our objectives were to test how irrigation management and bacterial pathogen load in potato seed stocks impact: (i) crop yields; (ii) disease development (blackleg or common scab); and (iii) soil microbial community dynamics.
Methods: We used stocks of seed potatoes with varying natural levels of Pectobacterium (Jelly [high load], Jelly [low load] and Estima [Zero - no Pectobacterium]). Stocks were grown under four irrigation regimes that differed in the timing and level of watering. The soil microbial communities were profiled using amplicon sequencing at 50% plant emergence and at harvest. Generalised linear latent variable models and an annotation-free mathematical framework approach (ensemble quotient analysis) were then used to show the interacting microbes with irrigation regime and Pectobacterium pathogen levels.
Results: Irrigation increased blackleg symptoms in the plots planted with stocks with low and high levels of Pectobacterium (22-34%) but not in the zero stock (2-6%). However, withholding irrigation increased common scab symptoms (2-5%) and reduced crop yields. Irrigation did not impact the composition of the soil microbiome, but planting stock with a high Pectobacterium burden resulted in an increased abundance of Planctomycetota, Anaerolinea and Acidobacteria species within the microbiome. Ensemble quotient analysis highlighted the Anaerolinea taxa were highly associated with high levels of Pectobacterium in the seed stock and blackleg symptoms in the field.
Conclusions: We conclude that planting seed stocks with a high Pectobacterium burden alters the abundance of specific microbial species within the soil microbiome and suggest that managing pathogen load in seed stocks could substantially affect soil communities, affecting crop health and productivity. Video Abstract.
{"title":"Balancing the scales: assessing the impact of irrigation and pathogen burden on potato blackleg disease and soil microbial communities.","authors":"Ciara Keating, Elizabeth Kilbride, Mark A Stalham, Charlotte Nellist, Joel Milner, Sonia Humphris, Ian Toth, Barbara K Mable, Umer Zeeshan Ijaz","doi":"10.1186/s40168-024-01918-6","DOIUrl":"10.1186/s40168-024-01918-6","url":null,"abstract":"<p><strong>Background: </strong>Understanding the interaction between environmental conditions, crop yields, and soil health is crucial for sustainable agriculture in a changing climate. Management practices to limit disease are a balancing act. For example, in potato production, dry conditions favour common scab (Streptomyces spp.) and wet conditions favour blackleg disease (Pectobacterium spp.). The exact mechanisms involved and how these link to changes in the soil microbiome are unclear. Our objectives were to test how irrigation management and bacterial pathogen load in potato seed stocks impact: (i) crop yields; (ii) disease development (blackleg or common scab); and (iii) soil microbial community dynamics.</p><p><strong>Methods: </strong>We used stocks of seed potatoes with varying natural levels of Pectobacterium (Jelly [high load], Jelly [low load] and Estima [Zero - no Pectobacterium]). Stocks were grown under four irrigation regimes that differed in the timing and level of watering. The soil microbial communities were profiled using amplicon sequencing at 50% plant emergence and at harvest. Generalised linear latent variable models and an annotation-free mathematical framework approach (ensemble quotient analysis) were then used to show the interacting microbes with irrigation regime and Pectobacterium pathogen levels.</p><p><strong>Results: </strong>Irrigation increased blackleg symptoms in the plots planted with stocks with low and high levels of Pectobacterium (22-34%) but not in the zero stock (2-6%). However, withholding irrigation increased common scab symptoms (2-5%) and reduced crop yields. Irrigation did not impact the composition of the soil microbiome, but planting stock with a high Pectobacterium burden resulted in an increased abundance of Planctomycetota, Anaerolinea and Acidobacteria species within the microbiome. Ensemble quotient analysis highlighted the Anaerolinea taxa were highly associated with high levels of Pectobacterium in the seed stock and blackleg symptoms in the field.</p><p><strong>Conclusions: </strong>We conclude that planting seed stocks with a high Pectobacterium burden alters the abundance of specific microbial species within the soil microbiome and suggest that managing pathogen load in seed stocks could substantially affect soil communities, affecting crop health and productivity. 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/PMC11492761/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469530","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}