Background: Soybean seeds are rich in protein and oil. The selection of varieties that produce high-quality seeds has been one of the priorities of soybean breeding programs. However, the influence of improved seed quality on the rhizosphere microbiota and whether the microbiota is involved in determining seed quality are still unclear. Here, we analyzed the structures of the rhizospheric bacterial communities of 100 soybean varieties, including 53 landraces and 47 modern cultivars, and evaluated the interactions between seed quality traits and rhizospheric bacteria.
Results: We found that rhizospheric bacterial structures differed between landraces and cultivars and that this difference was directly related to their oil content. Seven bacterial families (Sphingomonadaceae, Gemmatimonadaceae, Nocardioidaceae, Xanthobacteraceae, Chitinophagaceae, Oxalobacteraceae, and Streptomycetaceae) were obviously enriched in the rhizospheres of the high-oil cultivars. Among them, Oxalobacteraceae (Massilia) was assembled specifically by the root exudates of high-oil cultivars and was associated with the phenolic acids and flavonoids in plant phenylpropanoid biosynthetic pathways. Furthermore, we showed that Massilia affected auxin signaling or interfered with active oxygen-related metabolism. In addition, Massilia activated glycolysis pathway, thereby promoting seed oil accumulation.
Conclusions: These results provide a solid theoretical basis for the breeding of revolutionary soybean cultivars with desired seed quality and optimal microbiomes and the development of new cultivation strategies for increasing the oil content of seeds. Video Abstract.
{"title":"Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content.","authors":"Qin Han, Guanghui Zhu, Hongmei Qiu, Mingbo Li, Jiaming Zhang, Xinying Wu, Renhao Xiao, Yan Zhang, Wei Yang, Bing Tian, Lanxi Xu, Jiayang Zhou, Yutong Li, Yueqiang Wang, Yang Bai, Xia Li","doi":"10.1186/s40168-024-01933-7","DOIUrl":"10.1186/s40168-024-01933-7","url":null,"abstract":"<p><strong>Background: </strong>Soybean seeds are rich in protein and oil. The selection of varieties that produce high-quality seeds has been one of the priorities of soybean breeding programs. However, the influence of improved seed quality on the rhizosphere microbiota and whether the microbiota is involved in determining seed quality are still unclear. Here, we analyzed the structures of the rhizospheric bacterial communities of 100 soybean varieties, including 53 landraces and 47 modern cultivars, and evaluated the interactions between seed quality traits and rhizospheric bacteria.</p><p><strong>Results: </strong>We found that rhizospheric bacterial structures differed between landraces and cultivars and that this difference was directly related to their oil content. Seven bacterial families (Sphingomonadaceae, Gemmatimonadaceae, Nocardioidaceae, Xanthobacteraceae, Chitinophagaceae, Oxalobacteraceae, and Streptomycetaceae) were obviously enriched in the rhizospheres of the high-oil cultivars. Among them, Oxalobacteraceae (Massilia) was assembled specifically by the root exudates of high-oil cultivars and was associated with the phenolic acids and flavonoids in plant phenylpropanoid biosynthetic pathways. Furthermore, we showed that Massilia affected auxin signaling or interfered with active oxygen-related metabolism. In addition, Massilia activated glycolysis pathway, thereby promoting seed oil accumulation.</p><p><strong>Conclusions: </strong>These results provide a solid theoretical basis for the breeding of revolutionary soybean cultivars with desired seed quality and optimal microbiomes and the development of new cultivation strategies for increasing the oil content of seeds. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"224"},"PeriodicalIF":13.8,"publicationDate":"2024-10-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11526559/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546239","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 : 2024-10-30DOI: 10.1186/s40168-024-01944-4
Xueshuang Lai, Shuang Liu, Jian Miao, Ran Shen, Zhen Wang, Zhe Zhang, Huanfa Gong, Meng Li, Yuchun Pan, Qishan Wang
Background: Obesity in humans can lead to chronic diseases such as diabetes and cardiovascular disease. Similarly, subcutaneous fat (SCF) in pigs affects feed utilization, and excessive SCF can reduce the feed efficiency of pigs. Therefore, identifying factors that suppress fat deposition is particularly important. Numerous studies have implicated the gut microbiome in pigs' fat deposition, but research into its suppression remains scarce. The Lulai black pig (LL) is a hybrid breed derived from the Laiwu pig (LW) and the Yorkshire pig, with lower levels of SCF compared to the LW. In this study, we focused on these breeds to identify microbiota that regulate fat deposition. The key questions were: Which microbial populations reduce fat in LL pigs compared to LW pigs, and what is the underlying regulatory mechanism?
Results: In this study, we identified four different microbial strains, Eubacterium siraeum, Treponema bryantii, Clostridium sp. CAG:413, and Jeotgalibaca dankookensis, prevalent in both LW and LL pigs. Blood metabolome analysis revealed 49 differential metabolites, including tanshinone IIA and royal jelly acid, known for their anti-adipogenic properties. E. siraeum was strongly correlated with these metabolites, and its genes and metabolites were enriched in pathways linked to fatty acid degradation, glycerophospholipid, and glycerolipid metabolism. In vivo mouse experiments confirmed that E. siraeum metabolites curb weight gain, reduce SCF adipocyte size, increase the number of brown adipocytes, and regulate leptin, IL-6, and insulin secretion. Finally, we found that one important pathway through which E. siraeum inhibits fat deposition is by suppressing the phosphorylation of key proteins in the PI3K/AKT signaling pathway through the reduction of tyrosine.
Conclusions: We compared LW and LL pigs using fecal metagenomics, metabolomics, and blood metabolomics, identifying E. siraeum as a strain linked to fat deposition. Oral administration experiments in mice demonstrated that E. siraeum effectively inhibits fat accumulation, primarily through the suppression of the PI3K/AKT signaling pathway, a critical regulator of lipid metabolism. These findings provide a valuable theoretical basis for improving pork quality and offer insights relevant to the study of human obesity and related chronic metabolic diseases. Video Abstract.
{"title":"Eubacterium siraeum suppresses fat deposition via decreasing the tyrosine-mediated PI3K/AKT signaling pathway in high-fat diet-induced obesity.","authors":"Xueshuang Lai, Shuang Liu, Jian Miao, Ran Shen, Zhen Wang, Zhe Zhang, Huanfa Gong, Meng Li, Yuchun Pan, Qishan Wang","doi":"10.1186/s40168-024-01944-4","DOIUrl":"10.1186/s40168-024-01944-4","url":null,"abstract":"<p><strong>Background: </strong>Obesity in humans can lead to chronic diseases such as diabetes and cardiovascular disease. Similarly, subcutaneous fat (SCF) in pigs affects feed utilization, and excessive SCF can reduce the feed efficiency of pigs. Therefore, identifying factors that suppress fat deposition is particularly important. Numerous studies have implicated the gut microbiome in pigs' fat deposition, but research into its suppression remains scarce. The Lulai black pig (LL) is a hybrid breed derived from the Laiwu pig (LW) and the Yorkshire pig, with lower levels of SCF compared to the LW. In this study, we focused on these breeds to identify microbiota that regulate fat deposition. The key questions were: Which microbial populations reduce fat in LL pigs compared to LW pigs, and what is the underlying regulatory mechanism?</p><p><strong>Results: </strong>In this study, we identified four different microbial strains, Eubacterium siraeum, Treponema bryantii, Clostridium sp. CAG:413, and Jeotgalibaca dankookensis, prevalent in both LW and LL pigs. Blood metabolome analysis revealed 49 differential metabolites, including tanshinone IIA and royal jelly acid, known for their anti-adipogenic properties. E. siraeum was strongly correlated with these metabolites, and its genes and metabolites were enriched in pathways linked to fatty acid degradation, glycerophospholipid, and glycerolipid metabolism. In vivo mouse experiments confirmed that E. siraeum metabolites curb weight gain, reduce SCF adipocyte size, increase the number of brown adipocytes, and regulate leptin, IL-6, and insulin secretion. Finally, we found that one important pathway through which E. siraeum inhibits fat deposition is by suppressing the phosphorylation of key proteins in the PI3K/AKT signaling pathway through the reduction of tyrosine.</p><p><strong>Conclusions: </strong>We compared LW and LL pigs using fecal metagenomics, metabolomics, and blood metabolomics, identifying E. siraeum as a strain linked to fat deposition. Oral administration experiments in mice demonstrated that E. siraeum effectively inhibits fat accumulation, primarily through the suppression of the PI3K/AKT signaling pathway, a critical regulator of lipid metabolism. These findings provide a valuable theoretical basis for improving pork quality and offer insights relevant to the study of human obesity and related chronic metabolic diseases. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"223"},"PeriodicalIF":13.8,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11526712/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546238","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 : 2024-10-29DOI: 10.1186/s40168-024-01921-x
Ana-Belen Martin-Cuadrado, Esther Rubio-Portillo, Francesc Rosselló, Josefa Antón
Background: Extensive research on the diversity and functional roles of the microorganisms associated with reef-building corals has been promoted as a consequence of the rapid global decline of coral reefs attributed to climate change. Several studies have highlighted the importance of coral-associated algae (Symbiodinium) and bacteria and their potential roles in promoting coral host fitness and survival. However, the complex coral holobiont extends beyond these components to encompass other entities such as protists, fungi, and viruses. While each constituent has been individually investigated in corals, a comprehensive understanding of their collective roles is imperative for a holistic comprehension of coral health and resilience.
Results: The metagenomic analysis of the microbiome of the coral Oculina patagonica has revealed that fungi of the genera Aspergillus, Fusarium, and Rhizofagus together with the prokaryotic genera Streptomyces, Pseudomonas, and Bacillus were abundant members of the coral holobiont. This study also assessed changes in microeukaryotic, prokaryotic, and viral communities under three stress conditions: aquaria confinement, heat stress, and Vibrio infections. In general, stress conditions led to an increase in Rhodobacteraceae, Flavobacteraceae, and Vibrionaceae families, accompanied by a decrease in Streptomycetaceae. Concurrently, there was a significant decline in both the abundance and richness of microeukaryotic species and a reduction in genes associated with antimicrobial compound production by the coral itself, as well as by Symbiodinium and fungi.
Conclusion: Our findings suggest that the interplay between microeukaryotic and prokaryotic components of the coral holobiont may be disrupted by stress conditions, such as confinement, increase of seawater temperature, or Vibrio infection, leading to a dysbiosis in the global microbial community that may increase coral susceptibility to diseases. Further, microeukaryotic community seems to exert influence on the prokaryotic community dynamics, possibly through predation or the production of secondary metabolites with anti-bacterial activity. Video Abstract.
{"title":"The coral Oculina patagonica holobiont and its response to confinement, temperature, and Vibrio infections.","authors":"Ana-Belen Martin-Cuadrado, Esther Rubio-Portillo, Francesc Rosselló, Josefa Antón","doi":"10.1186/s40168-024-01921-x","DOIUrl":"10.1186/s40168-024-01921-x","url":null,"abstract":"<p><strong>Background: </strong>Extensive research on the diversity and functional roles of the microorganisms associated with reef-building corals has been promoted as a consequence of the rapid global decline of coral reefs attributed to climate change. Several studies have highlighted the importance of coral-associated algae (Symbiodinium) and bacteria and their potential roles in promoting coral host fitness and survival. However, the complex coral holobiont extends beyond these components to encompass other entities such as protists, fungi, and viruses. While each constituent has been individually investigated in corals, a comprehensive understanding of their collective roles is imperative for a holistic comprehension of coral health and resilience.</p><p><strong>Results: </strong>The metagenomic analysis of the microbiome of the coral Oculina patagonica has revealed that fungi of the genera Aspergillus, Fusarium, and Rhizofagus together with the prokaryotic genera Streptomyces, Pseudomonas, and Bacillus were abundant members of the coral holobiont. This study also assessed changes in microeukaryotic, prokaryotic, and viral communities under three stress conditions: aquaria confinement, heat stress, and Vibrio infections. In general, stress conditions led to an increase in Rhodobacteraceae, Flavobacteraceae, and Vibrionaceae families, accompanied by a decrease in Streptomycetaceae. Concurrently, there was a significant decline in both the abundance and richness of microeukaryotic species and a reduction in genes associated with antimicrobial compound production by the coral itself, as well as by Symbiodinium and fungi.</p><p><strong>Conclusion: </strong>Our findings suggest that the interplay between microeukaryotic and prokaryotic components of the coral holobiont may be disrupted by stress conditions, such as confinement, increase of seawater temperature, or Vibrio infection, leading to a dysbiosis in the global microbial community that may increase coral susceptibility to diseases. Further, microeukaryotic community seems to exert influence on the prokaryotic community dynamics, possibly through predation or the production of secondary metabolites with anti-bacterial activity. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"222"},"PeriodicalIF":13.8,"publicationDate":"2024-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11520598/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546240","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: Fertilization practices control bacterial wilt-causing Ralstonia solanacearum by shaping the soil microbiome. This microbiome is the start of food webs, in which nematodes act as major microbiome predators. However, the multitrophic links between nematodes and the performance of R. solanacearum and plant health, and how these links are affected by fertilization practices, remain unknown.
Results: Here, we performed a field experiment under no-, chemical-, and bio-organic-fertilization regimes to investigate the potential role of nematodes in suppressing tomato bacterial wilt. We found that bio-organic fertilizers changed nematode community composition and increased abundances of bacterivorous nematodes (e.g., Protorhabditis spp.). We also observed that pathogen-antagonistic bacteria, such as Bacillus spp., positively correlated with abundances of bacterivorous nematodes. In subsequent laboratory and greenhouse experiments, we demonstrated that bacterivorous nematodes preferentially preyed on non-pathogen-antagonistic bacteria over Bacillus. These changes increased the performance of pathogen-antagonistic bacteria that subsequently suppressed R. solanacearum.
Conclusions: Overall, bacterivorous nematodes can reduce the abundance of plant pathogens, which might provide a novel protection strategy to promote plant health. Video Abstract.
背景:施肥方法通过塑造土壤微生物群来控制导致细菌枯萎病的 Ralstonia solanacearum。该微生物群是食物网的起点,其中线虫是微生物群的主要捕食者。然而,线虫与 R. solanacearum 的表现和植物健康之间的多营养联系,以及这些联系如何受到施肥方法的影响,仍是未知数:结果:在此,我们进行了一项田间试验,研究线虫在抑制番茄细菌性萎蔫病中的潜在作用。我们发现,生物有机肥改变了线虫群落的组成,增加了食菌线虫(如原生线虫)的数量。我们还观察到,病原拮抗细菌(如芽孢杆菌)与食菌线虫的数量呈正相关。在随后的实验室和温室实验中,我们证明细菌线虫优先捕食非病原拮抗细菌,而不是芽孢杆菌。这些变化提高了病原拮抗细菌的性能,从而抑制了茄碱菌:总之,食菌线虫可以减少植物病原体的数量,这可能为促进植物健康提供了一种新的保护策略。视频摘要
{"title":"Protorhabditis nematodes and pathogen-antagonistic bacteria interactively promote plant health.","authors":"Xu Xu, Renqiang Jiang, Xinling Wang, Shanshan Liu, Menghui Dong, Hancheng Mao, Xingrui Li, Ziyu Ni, Nana Lv, Xuhui Deng, Wu Xiong, Chengyuan Tao, Rong Li, Qirong Shen, Stefan Geisen","doi":"10.1186/s40168-024-01947-1","DOIUrl":"10.1186/s40168-024-01947-1","url":null,"abstract":"<p><strong>Background: </strong>Fertilization practices control bacterial wilt-causing Ralstonia solanacearum by shaping the soil microbiome. This microbiome is the start of food webs, in which nematodes act as major microbiome predators. However, the multitrophic links between nematodes and the performance of R. solanacearum and plant health, and how these links are affected by fertilization practices, remain unknown.</p><p><strong>Results: </strong>Here, we performed a field experiment under no-, chemical-, and bio-organic-fertilization regimes to investigate the potential role of nematodes in suppressing tomato bacterial wilt. We found that bio-organic fertilizers changed nematode community composition and increased abundances of bacterivorous nematodes (e.g., Protorhabditis spp.). We also observed that pathogen-antagonistic bacteria, such as Bacillus spp., positively correlated with abundances of bacterivorous nematodes. In subsequent laboratory and greenhouse experiments, we demonstrated that bacterivorous nematodes preferentially preyed on non-pathogen-antagonistic bacteria over Bacillus. These changes increased the performance of pathogen-antagonistic bacteria that subsequently suppressed R. solanacearum.</p><p><strong>Conclusions: </strong>Overall, bacterivorous nematodes can reduce the abundance of plant pathogens, which might provide a novel protection strategy to promote plant health. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"221"},"PeriodicalIF":13.8,"publicationDate":"2024-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11520073/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142522303","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 : 2024-10-26DOI: 10.1186/s40168-024-01945-3
Sven Kleine Bardenhorst, Daniel Hagenfeld, Johannes Matern, Karola Prior, Inga Harks, Peter Eickholz, Katrin Lorenz, Ti-Sun Kim, Thomas Kocher, Jörg Meyle, Doğan Kaner, Yvonne Jockel-Schneider, Dag Harmsen, Benjamin Ehmke
Background: Periodontitis, a prevalent chronic inflammatory disease, offers insights into the broader landscape of chronic inflammatory conditions. The progression and treatment outcomes of periodontitis are closely related to the oral microbiota's composition. Adjunctive systemic Amoxicillin 500 mg and Metronidazole 400 mg, often prescribed thrice daily for 7 days to enhance periodontal therapy's efficacy, have lasting effects on the oral microbiome. However, the precise mechanism through which the oral microbiome influences clinical outcomes in periodontitis patients remains debated. This investigation explores the pivotal role of the oral microbiome's composition in mediating the outcomes of adjunctive systemic antibiotic treatment.
Methods: Subgingival plaque samples from 10 periodontally healthy and 163 periodontitis patients from a randomized clinical trial on periodontal therapy were analyzed. Patients received either adjunctive amoxicillin/metronidazole or a placebo after mechanical periodontal treatment. Microbial samples were collected at various intervals up to 26 months post-therapy. Using topic models, we identified microbial communities associated with normobiotic and dysbiotic states, validated with 86 external and 40 internal samples. Logistic regression models evaluated the association between these microbial communities and clinical periodontitis parameters. A Directed Acyclic Graph (DAG) determined the mediating role of oral microbiota in the causal path of antibiotic treatment effects on clinical outcomes.
Results: We identified clear distinctions between dysbiotic and normobiotic microbial communities, differentiating healthy from periodontitis subjects. Dysbiotic states consistently associated with below median %Pocket Probing Depth ≥ 5 mm (OR = 1.26, 95% CI [1.14-1.42]) and %Bleeding on Probing (OR = 1.09, 95% CI [1.00-1.18]). Factors like microbial response to treatment, smoking, and age were predictors of clinical attachment loss progression, whereas sex and antibiotic treatment were not. Further, we showed that the oral microbial treatment response plays a crucial role in the causal effect of antibiotic treatment on clinical treatment outcomes.
Conclusions: The shift towards a normobiotic subgingival microbiome, primarily induced by adjunctive antibiotics, underscores the potential for microbiome-targeted interventions to enhance therapeutic efficacy in chronic inflammatory conditions. This study reaffirms the importance of understanding the oral microbiome's role in periodontal health and paves the way for future research exploring personalized treatment strategies based on individual microbiome profiles. Video Abstract.
{"title":"The role of the oral microbiota in the causal effect of adjunctive antibiotics on clinical outcomes in stage III-IV periodontitis patients.","authors":"Sven Kleine Bardenhorst, Daniel Hagenfeld, Johannes Matern, Karola Prior, Inga Harks, Peter Eickholz, Katrin Lorenz, Ti-Sun Kim, Thomas Kocher, Jörg Meyle, Doğan Kaner, Yvonne Jockel-Schneider, Dag Harmsen, Benjamin Ehmke","doi":"10.1186/s40168-024-01945-3","DOIUrl":"10.1186/s40168-024-01945-3","url":null,"abstract":"<p><strong>Background: </strong>Periodontitis, a prevalent chronic inflammatory disease, offers insights into the broader landscape of chronic inflammatory conditions. The progression and treatment outcomes of periodontitis are closely related to the oral microbiota's composition. Adjunctive systemic Amoxicillin 500 mg and Metronidazole 400 mg, often prescribed thrice daily for 7 days to enhance periodontal therapy's efficacy, have lasting effects on the oral microbiome. However, the precise mechanism through which the oral microbiome influences clinical outcomes in periodontitis patients remains debated. This investigation explores the pivotal role of the oral microbiome's composition in mediating the outcomes of adjunctive systemic antibiotic treatment.</p><p><strong>Methods: </strong>Subgingival plaque samples from 10 periodontally healthy and 163 periodontitis patients from a randomized clinical trial on periodontal therapy were analyzed. Patients received either adjunctive amoxicillin/metronidazole or a placebo after mechanical periodontal treatment. Microbial samples were collected at various intervals up to 26 months post-therapy. Using topic models, we identified microbial communities associated with normobiotic and dysbiotic states, validated with 86 external and 40 internal samples. Logistic regression models evaluated the association between these microbial communities and clinical periodontitis parameters. A Directed Acyclic Graph (DAG) determined the mediating role of oral microbiota in the causal path of antibiotic treatment effects on clinical outcomes.</p><p><strong>Results: </strong>We identified clear distinctions between dysbiotic and normobiotic microbial communities, differentiating healthy from periodontitis subjects. Dysbiotic states consistently associated with below median %Pocket Probing Depth ≥ 5 mm (OR = 1.26, 95% CI [1.14-1.42]) and %Bleeding on Probing (OR = 1.09, 95% CI [1.00-1.18]). Factors like microbial response to treatment, smoking, and age were predictors of clinical attachment loss progression, whereas sex and antibiotic treatment were not. Further, we showed that the oral microbial treatment response plays a crucial role in the causal effect of antibiotic treatment on clinical treatment outcomes.</p><p><strong>Conclusions: </strong>The shift towards a normobiotic subgingival microbiome, primarily induced by adjunctive antibiotics, underscores the potential for microbiome-targeted interventions to enhance therapeutic efficacy in chronic inflammatory conditions. This study reaffirms the importance of understanding the oral microbiome's role in periodontal health and paves the way for future research exploring personalized treatment strategies based on individual microbiome profiles. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"220"},"PeriodicalIF":13.8,"publicationDate":"2024-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515798/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503493","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 : 2024-10-24DOI: 10.1186/s40168-024-01935-5
Xichuan Zhai, Alex Gobbi, Witold Kot, Lukasz Krych, Dennis Sandris Nielsen, Ling Deng
Background: The gut virome is an integral component of the gut microbiome, playing a crucial role in maintaining gut health. However, accurately depicting the entire gut virome is challenging due to the inherent diversity of genome types (dsDNA, ssDNA, dsRNA, and ssRNA) and topologies (linear, circular, or fragments), with subsequently biases associated with current sequencing library preparation methods. To overcome these problems and improve reproducibility and comparability across studies, universal or standardized virome sequencing library construction methods are highly needed in the gut virome study.
Results: We repurposed the ligation-based single-stranded library (SSLR) preparation method for virome studies. We demonstrate that the SSLR method exhibits exceptional efficiency in quantifying viral DNA genomes (both dsDNA and ssDNA) and outperforms existing double-stranded (Nextera) and single-stranded (xGen, MDA + Nextera) library preparation approaches in terms of minimal amplification bias, evenness of coverage, and integrity of assembling viral genomes. The SSLR method can be utilized for the simultaneous library preparation of both DNA and RNA viral genomes. Furthermore, the SSLR method showed its ability to capture highly modified phage genomes, which were often lost using other library preparation approaches.
Conclusion: We introduce and improve a fast, simple, and efficient ligation-based single-stranded DNA library preparation for gut virome study. This method is compatible with Illumina sequencing platforms and only requires ligation reagents within 3-h library preparation, which is similar or even better than the advanced library preparation method (xGen). We hope this method can be further optimized, validated, and widely used to make gut virome study more comparable and reproducible. Video Abstract.
背景:肠道病毒组是肠道微生物组不可或缺的组成部分,在维持肠道健康方面发挥着至关重要的作用。然而,由于基因组类型(dsDNA、ssDNA、dsRNA 和 ssRNA)和拓扑结构(线性、环状或片段)固有的多样性,以及随后与当前测序文库制备方法相关的偏差,准确描绘整个肠道病毒组具有挑战性。为了克服这些问题,提高各项研究的可重复性和可比性,肠道病毒组研究亟需通用或标准化的病毒组测序文库构建方法:结果:我们将基于连接的单链文库(SSLR)制备方法重新用于病毒组研究。结果:我们将基于连接的单链文库(SSLR)制备方法重新用于病毒组研究,结果表明,SSLR方法在量化病毒DNA基因组(dsDNA和ssDNA)方面表现出卓越的效率,并且在扩增偏差最小化、覆盖率均匀性和组装病毒基因组的完整性方面优于现有的双链(Nextera)和单链(xGen、MDA + Nextera)文库制备方法。SSLR 方法可用于同时制备 DNA 和 RNA 病毒基因组文库。此外,SSLR 方法还能捕获高度修饰的噬菌体基因组,而其他文库制备方法往往会丢失这些基因组:我们介绍并改进了一种用于肠道病毒组研究的快速、简单、高效的基于连接的单链 DNA 文库制备方法。该方法与 Illumina 测序平台兼容,在 3 小时的文库制备过程中只需连接试剂,与先进的文库制备方法(xGen)相似甚至更好。我们希望这种方法能得到进一步优化、验证和广泛应用,使肠道病毒组研究更具可比性和可重复性。视频摘要。
{"title":"A single-stranded based library preparation method for virome characterization.","authors":"Xichuan Zhai, Alex Gobbi, Witold Kot, Lukasz Krych, Dennis Sandris Nielsen, Ling Deng","doi":"10.1186/s40168-024-01935-5","DOIUrl":"10.1186/s40168-024-01935-5","url":null,"abstract":"<p><strong>Background: </strong>The gut virome is an integral component of the gut microbiome, playing a crucial role in maintaining gut health. However, accurately depicting the entire gut virome is challenging due to the inherent diversity of genome types (dsDNA, ssDNA, dsRNA, and ssRNA) and topologies (linear, circular, or fragments), with subsequently biases associated with current sequencing library preparation methods. To overcome these problems and improve reproducibility and comparability across studies, universal or standardized virome sequencing library construction methods are highly needed in the gut virome study.</p><p><strong>Results: </strong>We repurposed the ligation-based single-stranded library (SSLR) preparation method for virome studies. We demonstrate that the SSLR method exhibits exceptional efficiency in quantifying viral DNA genomes (both dsDNA and ssDNA) and outperforms existing double-stranded (Nextera) and single-stranded (xGen, MDA + Nextera) library preparation approaches in terms of minimal amplification bias, evenness of coverage, and integrity of assembling viral genomes. The SSLR method can be utilized for the simultaneous library preparation of both DNA and RNA viral genomes. Furthermore, the SSLR method showed its ability to capture highly modified phage genomes, which were often lost using other library preparation approaches.</p><p><strong>Conclusion: </strong>We introduce and improve a fast, simple, and efficient ligation-based single-stranded DNA library preparation for gut virome study. This method is compatible with Illumina sequencing platforms and only requires ligation reagents within 3-h library preparation, which is similar or even better than the advanced library preparation method (xGen). We hope this method can be further optimized, validated, and widely used to make gut virome study more comparable and reproducible. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"219"},"PeriodicalIF":13.8,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515303/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503478","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 : 2024-10-24DOI: 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":"12 1","pages":"218"},"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":"12 1","pages":"217"},"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":"12 1","pages":"214"},"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":"12 1","pages":"215"},"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}