Pub Date : 2024-05-09DOI: 10.1186/s40168-024-01791-3
Ming Yan, Zhongtang Yu
Background: The rumen microbiome enables ruminants to digest otherwise indigestible feedstuffs, thereby facilitating the production of high-quality protein, albeit with suboptimal efficiency and producing methane. Despite extensive research delineating associations between the rumen microbiome and ruminant production traits, the functional roles of the pervasive and diverse rumen virome remain to be determined.
Results: Leveraging a recent comprehensive rumen virome database, this study analyzes virus-microbe linkages, at both species and strain levels, across 551 rumen metagenomes, elucidating patterns of microbial and viral diversity, co-occurrence, and virus-microbe interactions. Additionally, this study assesses the potential role of rumen viruses in microbial diversification by analyzing prophages found in rumen metagenome-assembled genomes. Employing CRISPR-Cas spacer-based matching and virus-microbe co-occurrence network analysis, this study suggests that the viruses in the rumen may regulate microbes at strain and community levels through both antagonistic and mutualistic interactions. Moreover, this study establishes that the rumen virome demonstrates responsiveness to dietary shifts and associations with key animal production traits, including feed efficiency, lactation performance, weight gain, and methane emissions.
Conclusions: These findings provide a substantive framework for further investigations to unravel the functional roles of the virome in the rumen in shaping the microbiome and influencing overall animal production performance. Video Abstract.
{"title":"Viruses contribute to microbial diversification in the rumen ecosystem and are associated with certain animal production traits.","authors":"Ming Yan, Zhongtang Yu","doi":"10.1186/s40168-024-01791-3","DOIUrl":"10.1186/s40168-024-01791-3","url":null,"abstract":"<p><strong>Background: </strong>The rumen microbiome enables ruminants to digest otherwise indigestible feedstuffs, thereby facilitating the production of high-quality protein, albeit with suboptimal efficiency and producing methane. Despite extensive research delineating associations between the rumen microbiome and ruminant production traits, the functional roles of the pervasive and diverse rumen virome remain to be determined.</p><p><strong>Results: </strong>Leveraging a recent comprehensive rumen virome database, this study analyzes virus-microbe linkages, at both species and strain levels, across 551 rumen metagenomes, elucidating patterns of microbial and viral diversity, co-occurrence, and virus-microbe interactions. Additionally, this study assesses the potential role of rumen viruses in microbial diversification by analyzing prophages found in rumen metagenome-assembled genomes. Employing CRISPR-Cas spacer-based matching and virus-microbe co-occurrence network analysis, this study suggests that the viruses in the rumen may regulate microbes at strain and community levels through both antagonistic and mutualistic interactions. Moreover, this study establishes that the rumen virome demonstrates responsiveness to dietary shifts and associations with key animal production traits, including feed efficiency, lactation performance, weight gain, and methane emissions.</p><p><strong>Conclusions: </strong>These findings provide a substantive framework for further investigations to unravel the functional roles of the virome in the rumen in shaping the microbiome and influencing overall animal production performance. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-05-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11080232/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140898813","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 : 2024-05-09DOI: 10.1186/s40168-024-01805-0
Yao Pei, Marcus Ho-Hin Shum, Yunshi Liao, Vivian W Leung, Yu-Nong Gong, David K Smith, Xiaole Yin, Yi Guan, Ruibang Luo, Tong Zhang, Tommy Tsan-Yuk Lam
Background: Emergence of antibiotic resistance in bacteria is an important threat to global health. Antibiotic resistance genes (ARGs) are some of the key components to define bacterial resistance and their spread in different environments. Identification of ARGs, particularly from high-throughput sequencing data of the specimens, is the state-of-the-art method for comprehensively monitoring their spread and evolution. Current computational methods to identify ARGs mainly rely on alignment-based sequence similarities with known ARGs. Such approaches are limited by choice of reference databases and may potentially miss novel ARGs. The similarity thresholds are usually simple and could not accommodate variations across different gene families and regions. It is also difficult to scale up when sequence data are increasing.
Results: In this study, we developed ARGNet, a deep neural network that incorporates an unsupervised learning autoencoder model to identify ARGs and a multiclass classification convolutional neural network to classify ARGs that do not depend on sequence alignment. This approach enables a more efficient discovery of both known and novel ARGs. ARGNet accepts both amino acid and nucleotide sequences of variable lengths, from partial (30-50 aa; 100-150 nt) sequences to full-length protein or genes, allowing its application in both target sequencing and metagenomic sequencing. Our performance evaluation showed that ARGNet outperformed other deep learning models including DeepARG and HMD-ARG in most of the application scenarios especially quasi-negative test and the analysis of prediction consistency with phylogenetic tree. ARGNet has a reduced inference runtime by up to 57% relative to DeepARG.
Conclusions: ARGNet is flexible, efficient, and accurate at predicting a broad range of ARGs from the sequencing data. ARGNet is freely available at https://github.com/id-bioinfo/ARGNet , with an online service provided at https://ARGNet.hku.hk . Video Abstract.
{"title":"ARGNet: using deep neural networks for robust identification and classification of antibiotic resistance genes from sequences.","authors":"Yao Pei, Marcus Ho-Hin Shum, Yunshi Liao, Vivian W Leung, Yu-Nong Gong, David K Smith, Xiaole Yin, Yi Guan, Ruibang Luo, Tong Zhang, Tommy Tsan-Yuk Lam","doi":"10.1186/s40168-024-01805-0","DOIUrl":"10.1186/s40168-024-01805-0","url":null,"abstract":"<p><strong>Background: </strong>Emergence of antibiotic resistance in bacteria is an important threat to global health. Antibiotic resistance genes (ARGs) are some of the key components to define bacterial resistance and their spread in different environments. Identification of ARGs, particularly from high-throughput sequencing data of the specimens, is the state-of-the-art method for comprehensively monitoring their spread and evolution. Current computational methods to identify ARGs mainly rely on alignment-based sequence similarities with known ARGs. Such approaches are limited by choice of reference databases and may potentially miss novel ARGs. The similarity thresholds are usually simple and could not accommodate variations across different gene families and regions. It is also difficult to scale up when sequence data are increasing.</p><p><strong>Results: </strong>In this study, we developed ARGNet, a deep neural network that incorporates an unsupervised learning autoencoder model to identify ARGs and a multiclass classification convolutional neural network to classify ARGs that do not depend on sequence alignment. This approach enables a more efficient discovery of both known and novel ARGs. ARGNet accepts both amino acid and nucleotide sequences of variable lengths, from partial (30-50 aa; 100-150 nt) sequences to full-length protein or genes, allowing its application in both target sequencing and metagenomic sequencing. Our performance evaluation showed that ARGNet outperformed other deep learning models including DeepARG and HMD-ARG in most of the application scenarios especially quasi-negative test and the analysis of prediction consistency with phylogenetic tree. ARGNet has a reduced inference runtime by up to 57% relative to DeepARG.</p><p><strong>Conclusions: </strong>ARGNet is flexible, efficient, and accurate at predicting a broad range of ARGs from the sequencing data. ARGNet is freely available at https://github.com/id-bioinfo/ARGNet , with an online service provided at https://ARGNet.hku.hk . Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-05-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11080312/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140898804","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 : 2024-05-07DOI: 10.1186/s40168-024-01792-2
Beatriz Jorrin, Timothy L Haskett, Hayley E Knights, Anna Martyn, Thomas J Underwood, Jessica Dolliver, Raphael Ledermann, Philip S Poole
Background: After two decades of extensive microbiome research, the current forefront of scientific exploration involves moving beyond description and classification to uncovering the intricate mechanisms underlying the coalescence of microbial communities. Deciphering microbiome assembly has been technically challenging due to their vast microbial diversity but establishing a synthetic community (SynCom) serves as a key strategy in unravelling this process. Achieving absolute quantification is crucial for establishing causality in assembly dynamics. However, existing approaches are primarily designed to differentiate a specific group of microorganisms within a particular SynCom.
Results: To address this issue, we have developed the differential fluorescent marking (DFM) strategy, employing three distinguishable fluorescent proteins in single and double combinations. Building on the mini-Tn7 transposon, DFM capitalises on enhanced stability and broad applicability across diverse Proteobacteria species. The various DFM constructions are built using the pTn7-SCOUT plasmid family, enabling modular assembly, and facilitating the interchangeability of expression and antibiotic cassettes in a single reaction. DFM has no detrimental effects on fitness or community assembly dynamics, and through the application of flow cytometry, we successfully differentiated, quantified, and tracked a diverse six-member SynCom under various complex conditions like root rhizosphere showing a different colonisation assembly dynamic between pea and barley roots.
Conclusions: DFM represents a powerful resource that eliminates dependence on sequencing and/or culturing, thereby opening new avenues for studying microbiome assembly. Video Abstract.
{"title":"Stable, fluorescent markers for tracking synthetic communities and assembly dynamics.","authors":"Beatriz Jorrin, Timothy L Haskett, Hayley E Knights, Anna Martyn, Thomas J Underwood, Jessica Dolliver, Raphael Ledermann, Philip S Poole","doi":"10.1186/s40168-024-01792-2","DOIUrl":"10.1186/s40168-024-01792-2","url":null,"abstract":"<p><strong>Background: </strong>After two decades of extensive microbiome research, the current forefront of scientific exploration involves moving beyond description and classification to uncovering the intricate mechanisms underlying the coalescence of microbial communities. Deciphering microbiome assembly has been technically challenging due to their vast microbial diversity but establishing a synthetic community (SynCom) serves as a key strategy in unravelling this process. Achieving absolute quantification is crucial for establishing causality in assembly dynamics. However, existing approaches are primarily designed to differentiate a specific group of microorganisms within a particular SynCom.</p><p><strong>Results: </strong>To address this issue, we have developed the differential fluorescent marking (DFM) strategy, employing three distinguishable fluorescent proteins in single and double combinations. Building on the mini-Tn7 transposon, DFM capitalises on enhanced stability and broad applicability across diverse Proteobacteria species. The various DFM constructions are built using the pTn7-SCOUT plasmid family, enabling modular assembly, and facilitating the interchangeability of expression and antibiotic cassettes in a single reaction. DFM has no detrimental effects on fitness or community assembly dynamics, and through the application of flow cytometry, we successfully differentiated, quantified, and tracked a diverse six-member SynCom under various complex conditions like root rhizosphere showing a different colonisation assembly dynamic between pea and barley roots.</p><p><strong>Conclusions: </strong>DFM represents a powerful resource that eliminates dependence on sequencing and/or culturing, thereby opening new avenues for studying microbiome assembly. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-05-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11075435/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140876818","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 : 2024-05-07DOI: 10.1186/s40168-024-01795-z
Yuehui Hong, Hao Li, Linkang Chen, Hongtian Su, Bin Zhang, Yu Luo, Chengji Li, Zuguo Zhao, Yiming Shao, Lianxian Guo
Background: Antibiotic exposure can occur in medical settings and from environmental sources. Long-term effects of brief antibiotic exposure in early life are largely unknown.
Results: Post a short-term treatment by ceftriaxone to C57BL/6 mice in early life, a 14-month observation was performed using 16S rRNA gene-sequencing technique, metabolomics analysis, and metagenomics analysis on the effects of ceftriaxone exposure. Firstly, the results showed that antibiotic pre-treatment significantly disturbed gut microbial α and β diversities (P < 0.05). Both Chao1 indices and Shannon indices manifested recovery trends over time, but they didn't entirely recover to the baseline of control throughout the experiment. Secondly, antibiotic pre-treatment reduced the complexity of gut molecular ecological networks (MENs). Various network parameters were affected and manifested recovery trends over time with different degrees, such as nodes (P < 0.001, R2 = 0.6563), links (P < 0.01, R2 = 0.4543), number of modules (P = 0.0672, R2 = 0.2523), relative modularity (P = 0.6714, R2 = 0.0155), number of keystones (P = 0.1003, R2 = 0.2090), robustness_random (P = 0.79, R2 = 0.0063), and vulnerability (P = 0.0528, R2 = 0.28). The network parameters didn't entirely recover. Antibiotic exposure obviously reduced the number of key species in gut MENs. Interestingly, new keystones appeared during the recovery process of network complexity. Changes in network stability might be caused by variations in network complexity, which supports the ecological theory that complexity begets stability. Besides, the metabolism profiles of the antibiotic group and control were significantly different. Correlation analysis showed that antibiotic-induced differences in gut microbial metabolism were related to MEN changes. Antibiotic exposure also caused long-term effects on gut microbial functional networks in mice.
Conclusions: These results suggest that short-term antibiotic exposure in early life will cause long-term negative impacts on gut microbial diversity, MENs, and microbial metabolism. Therefore, great concern should be raised about children's brief exposure to antibiotics if the results observed in mice are applicable to humans. Video Abstract.
{"title":"Short-term exposure to antibiotics begets long-term disturbance in gut microbial metabolism and molecular ecological networks.","authors":"Yuehui Hong, Hao Li, Linkang Chen, Hongtian Su, Bin Zhang, Yu Luo, Chengji Li, Zuguo Zhao, Yiming Shao, Lianxian Guo","doi":"10.1186/s40168-024-01795-z","DOIUrl":"10.1186/s40168-024-01795-z","url":null,"abstract":"<p><strong>Background: </strong>Antibiotic exposure can occur in medical settings and from environmental sources. Long-term effects of brief antibiotic exposure in early life are largely unknown.</p><p><strong>Results: </strong>Post a short-term treatment by ceftriaxone to C57BL/6 mice in early life, a 14-month observation was performed using 16S rRNA gene-sequencing technique, metabolomics analysis, and metagenomics analysis on the effects of ceftriaxone exposure. Firstly, the results showed that antibiotic pre-treatment significantly disturbed gut microbial α and β diversities (P < 0.05). Both Chao1 indices and Shannon indices manifested recovery trends over time, but they didn't entirely recover to the baseline of control throughout the experiment. Secondly, antibiotic pre-treatment reduced the complexity of gut molecular ecological networks (MENs). Various network parameters were affected and manifested recovery trends over time with different degrees, such as nodes (P < 0.001, R<sup>2</sup> = 0.6563), links (P < 0.01, R<sup>2</sup> = 0.4543), number of modules (P = 0.0672, R<sup>2</sup> = 0.2523), relative modularity (P = 0.6714, R<sup>2</sup> = 0.0155), number of keystones (P = 0.1003, R<sup>2</sup> = 0.2090), robustness_random (P = 0.79, R<sup>2</sup> = 0.0063), and vulnerability (P = 0.0528, R<sup>2</sup> = 0.28). The network parameters didn't entirely recover. Antibiotic exposure obviously reduced the number of key species in gut MENs. Interestingly, new keystones appeared during the recovery process of network complexity. Changes in network stability might be caused by variations in network complexity, which supports the ecological theory that complexity begets stability. Besides, the metabolism profiles of the antibiotic group and control were significantly different. Correlation analysis showed that antibiotic-induced differences in gut microbial metabolism were related to MEN changes. Antibiotic exposure also caused long-term effects on gut microbial functional networks in mice.</p><p><strong>Conclusions: </strong>These results suggest that short-term antibiotic exposure in early life will cause long-term negative impacts on gut microbial diversity, MENs, and microbial metabolism. Therefore, great concern should be raised about children's brief exposure to antibiotics if the results observed in mice are applicable to humans. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-05-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11075301/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140876817","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 : 2024-05-06DOI: 10.1186/s40168-024-01802-3
Stephanie D Jurburg, Shane A Blowes, Ashley Shade, Nico Eisenhauer, Jonathan M Chase
Background: Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns.
Results: To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle.
Conclusions: This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective. Video Abstract.
{"title":"Synthesis of recovery patterns in microbial communities across environments.","authors":"Stephanie D Jurburg, Shane A Blowes, Ashley Shade, Nico Eisenhauer, Jonathan M Chase","doi":"10.1186/s40168-024-01802-3","DOIUrl":"10.1186/s40168-024-01802-3","url":null,"abstract":"<p><strong>Background: </strong>Disturbances alter the diversity and composition of microbial communities. Yet a generalized empirical assessment of microbiome responses to disturbance across different environments is needed to understand the factors driving microbiome recovery, and the role of the environment in driving these patterns.</p><p><strong>Results: </strong>To this end, we combined null models with Bayesian generalized linear models to examine 86 time series of disturbed mammalian, aquatic, and soil microbiomes up to 50 days following disturbance. Overall, disturbances had the strongest effect on mammalian microbiomes, which lost taxa and later recovered their richness, but not their composition. In contrast, following disturbance, aquatic microbiomes tended away from their pre-disturbance composition over time. Surprisingly, across all environments, we found no evidence of increased compositional dispersion (i.e., variance) following disturbance, in contrast to the expectations of the Anna Karenina Principle.</p><p><strong>Conclusions: </strong>This is the first study to systematically compare secondary successional dynamics across disturbed microbiomes, using a consistent temporal scale and modeling approach. Our findings show that the recovery of microbiomes is environment-specific, and helps to reconcile existing, environment-specific research into a unified perspective. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11071242/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140851861","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 : 2024-04-27DOI: 10.1186/s40168-024-01790-4
Elena A. Alexa, J. F. Cobo-Díaz, Erica Renes, Tom F. O´Callaghan, Kieran Kilcawley, David Mannion, Iwona Skibinska, Lorena Ruiz, Abelardo Margolles, Paula Fernández-Gómez, Adrián Alvarez-Molina, Paula Puente-Gómez, F. Crispie, Mercedes López, Miguel Prieto, Paul D. Cotter, A. Álvarez‐Ordoñez
{"title":"The detailed analysis of the microbiome and resistome of artisanal blue-veined cheeses provides evidence on sources and patterns of succession linked with quality and safety traits","authors":"Elena A. Alexa, J. F. Cobo-Díaz, Erica Renes, Tom F. O´Callaghan, Kieran Kilcawley, David Mannion, Iwona Skibinska, Lorena Ruiz, Abelardo Margolles, Paula Fernández-Gómez, Adrián Alvarez-Molina, Paula Puente-Gómez, F. Crispie, Mercedes López, Miguel Prieto, Paul D. Cotter, A. Álvarez‐Ordoñez","doi":"10.1186/s40168-024-01790-4","DOIUrl":"https://doi.org/10.1186/s40168-024-01790-4","url":null,"abstract":"","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-04-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140652203","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-23DOI: 10.1186/s40168-024-01798-w
C. Danne, B. Lamas, A. Lavelle, M-L. Michel, G. Da Costa, Hang-Phuong Pham, A. Lefevre, C. Bridonneau, M. Bredon, J. Planchais, M. Straube, P. Emond, P. Langella, H. Sokol
{"title":"Dissecting the respective roles of microbiota and host genetics in the susceptibility of Card9−/− mice to colitis","authors":"C. Danne, B. Lamas, A. Lavelle, M-L. Michel, G. Da Costa, Hang-Phuong Pham, A. Lefevre, C. Bridonneau, M. Bredon, J. Planchais, M. Straube, P. Emond, P. Langella, H. Sokol","doi":"10.1186/s40168-024-01798-w","DOIUrl":"https://doi.org/10.1186/s40168-024-01798-w","url":null,"abstract":"","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-04-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140666071","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-17DOI: 10.1186/s40168-023-01683-y
Jake Williams, Nathalie Pettorelli, Aaron C. Hartmann, Robert A. Quinn, Laetitia Plaisance, Michael O’Mahoney, Chris P. Meyer, Katharina E. Fabricius, Nancy Knowlton, Emma Ransome
Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH — an important global coral reef stressor — can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed.
微生物在整个珊瑚礁的环境、大型生物(整体生物)内部和其上都发挥着至关重要的作用,支持着营养和免疫系统调节等关键功能。这些作用凸显了微生物在生态系统层面的潜在重要性,然而有关珊瑚礁上微生物功能的大部分知识都来自珊瑚和海绵等一小部分整体生物。海水 pH 值的下降是全球珊瑚礁面临的一个重要压力,它能引起珊瑚礁生态系统层面的变化,从而为研究微生物在这一尺度上的作用提供了机会。我们采用原位实验的方法来验证这样一个假设:在这种海洋酸化(OA)的情况下,已知的大型生物营养群和功能群之间的变化可能会驱动一种扩展到大型生物和微生物的总体生态系统级响应,从而导致底栖整体生物群落微生物组和环境微生物组之间的差异减小。我们利用从巴布亚新几内亚二氧化碳渗流的 pH 值梯度上采样的底栖珊瑚礁群落全生物体的遗传和化学数据来验证这一假设。我们发现我们的假设得到了支持;在 OA 条件下,底栖整体生物群落的微生物组和代谢组与沉积物微生物组和代谢组的组成差异越来越小,这表明在 OA 条件下,底栖大型生物群落被环境微生物定殖的程度更高。我们还发现底栖光合群落的简化和同质化,以及肉质大型藻类数量的增加,这与之前观察到的珊瑚礁微生物化是一致的。我们证明了珊瑚礁中涉及大型生物和微生物的一种新的结构转变:在 OA 条件下,底栖整体生物群落的微生物组与沉积物微生物组的区别越来越小。我们的研究结果表明,微生物化和大型生物营养网络的破坏是相互交织的对环境压力的一般反应,指向一种普遍的、不可取的和可测量的生态系统变化形式。
{"title":"Decline of a distinct coral reef holobiont community under ocean acidification","authors":"Jake Williams, Nathalie Pettorelli, Aaron C. Hartmann, Robert A. Quinn, Laetitia Plaisance, Michael O’Mahoney, Chris P. Meyer, Katharina E. Fabricius, Nancy Knowlton, Emma Ransome","doi":"10.1186/s40168-023-01683-y","DOIUrl":"https://doi.org/10.1186/s40168-023-01683-y","url":null,"abstract":"Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH — an important global coral reef stressor — can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. ","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-04-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140613244","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-15DOI: 10.1186/s40168-024-01785-1
C. M. Whitfield-Cargile, H. C. Chung, M. C. Coleman, N. D. Cohen, A. M. Chamoun-Emanuelli, I. Ivanov, J. S. Goldsby, L. A. Davidson, I. Gaynanova, Y. Ni, R. S. Chapkin
The equine gastrointestinal (GI) microbiome has been described in the context of various diseases. The observed changes, however, have not been linked to host function and therefore it remains unclear how specific changes in the microbiome alter cellular and molecular pathways within the GI tract. Further, non-invasive techniques to examine the host gene expression profile of the GI mucosa have been described in horses but not evaluated in response to interventions. Therefore, the objectives of our study were to (1) profile gene expression and metabolomic changes in an equine model of non-steroidal anti-inflammatory drug (NSAID)-induced intestinal inflammation and (2) apply computational data integration methods to examine host-microbiota interactions. Twenty horses were randomly assigned to 1 of 2 groups (n = 10): control (placebo paste) or NSAID (phenylbutazone 4.4 mg/kg orally once daily for 9 days). Fecal samples were collected on days 0 and 10 and analyzed with respect to microbiota (16S rDNA gene sequencing), metabolomic (untargeted metabolites), and host exfoliated cell transcriptomic (exfoliome) changes. Data were analyzed and integrated using a variety of computational techniques, and underlying regulatory mechanisms were inferred from features that were commonly identified by all computational approaches. Phenylbutazone induced alterations in the microbiota, metabolome, and host transcriptome. Data integration identified correlation of specific bacterial genera with expression of several genes and metabolites that were linked to oxidative stress. Concomitant microbiota and metabolite changes resulted in the initiation of endoplasmic reticulum stress and unfolded protein response within the intestinal mucosa. Results of integrative analysis identified an important role for oxidative stress, and subsequent cell signaling responses, in a large animal model of GI inflammation. The computational approaches for combining non-invasive platforms for unbiased assessment of host GI responses (e.g., exfoliomics) with metabolomic and microbiota changes have broad application for the field of gastroenterology.
{"title":"Integrated analysis of gut metabolome, microbiome, and exfoliome data in an equine model of intestinal injury","authors":"C. M. Whitfield-Cargile, H. C. Chung, M. C. Coleman, N. D. Cohen, A. M. Chamoun-Emanuelli, I. Ivanov, J. S. Goldsby, L. A. Davidson, I. Gaynanova, Y. Ni, R. S. Chapkin","doi":"10.1186/s40168-024-01785-1","DOIUrl":"https://doi.org/10.1186/s40168-024-01785-1","url":null,"abstract":"The equine gastrointestinal (GI) microbiome has been described in the context of various diseases. The observed changes, however, have not been linked to host function and therefore it remains unclear how specific changes in the microbiome alter cellular and molecular pathways within the GI tract. Further, non-invasive techniques to examine the host gene expression profile of the GI mucosa have been described in horses but not evaluated in response to interventions. Therefore, the objectives of our study were to (1) profile gene expression and metabolomic changes in an equine model of non-steroidal anti-inflammatory drug (NSAID)-induced intestinal inflammation and (2) apply computational data integration methods to examine host-microbiota interactions. Twenty horses were randomly assigned to 1 of 2 groups (n = 10): control (placebo paste) or NSAID (phenylbutazone 4.4 mg/kg orally once daily for 9 days). Fecal samples were collected on days 0 and 10 and analyzed with respect to microbiota (16S rDNA gene sequencing), metabolomic (untargeted metabolites), and host exfoliated cell transcriptomic (exfoliome) changes. Data were analyzed and integrated using a variety of computational techniques, and underlying regulatory mechanisms were inferred from features that were commonly identified by all computational approaches. Phenylbutazone induced alterations in the microbiota, metabolome, and host transcriptome. Data integration identified correlation of specific bacterial genera with expression of several genes and metabolites that were linked to oxidative stress. Concomitant microbiota and metabolite changes resulted in the initiation of endoplasmic reticulum stress and unfolded protein response within the intestinal mucosa. Results of integrative analysis identified an important role for oxidative stress, and subsequent cell signaling responses, in a large animal model of GI inflammation. The computational approaches for combining non-invasive platforms for unbiased assessment of host GI responses (e.g., exfoliomics) with metabolomic and microbiota changes have broad application for the field of gastroenterology. ","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":15.5,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140593212","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}