Pub Date : 2024-04-19eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae057
James D Brunner, Aaron J Robinson, Patrick S G Chain
Microbial communities are diverse biological systems that include taxa from across multiple kingdoms of life. Notably, interactions between bacteria and fungi play a significant role in determining community structure. However, these statistical associations across kingdoms are more difficult to infer than intra-kingdom associations due to the nature of the data involved using standard network inference techniques. We quantify the challenges of cross-kingdom network inference from both theoretical and practical points of view using synthetic and real-world microbiome data. We detail the theoretical issue presented by combining compositional data sets drawn from the same environment, e.g. 16S and ITS sequencing of a single set of samples, and we survey common network inference techniques for their ability to handle this error. We then test these techniques for the accuracy and usefulness of their intra- and inter-kingdom associations by inferring networks from a set of simulated samples for which a ground-truth set of associations is known. We show that while the two methods mitigate the error of cross-kingdom inference, there is little difference between techniques for key practical applications including identification of strong correlations and identification of possible keystone taxa (i.e. hub nodes in the network). Furthermore, we identify a signature of the error caused by transkingdom network inference and demonstrate that it appears in networks constructed using real-world environmental microbiome data.
微生物群落是一个多样化的生物系统,包括来自多个生命领域的类群。值得注意的是,细菌和真菌之间的相互作用在决定群落结构方面发挥着重要作用。然而,由于使用标准网络推断技术所涉及数据的性质,这些跨生物界的统计关联比生物界内的关联更难推断。我们利用合成和真实世界的微生物组数据,从理论和实践角度量化了跨王国网络推断所面临的挑战。我们详细介绍了将来自同一环境的组成数据集(如单个样本集的 16S 和 ITS 测序)结合起来所带来的理论问题,并考察了常见网络推断技术处理这一误差的能力。然后,我们通过从一组已知关联的模拟样本中推断网络,测试这些技术在内部和部门间关联方面的准确性和实用性。我们发现,虽然这两种方法都能减少跨领域推断的误差,但在关键的实际应用中,包括识别强相关性和识别可能的基石类群(即网络中的枢纽节点)方面,这两种技术的差别并不大。此外,我们还发现了跨王国网络推断所造成的误差特征,并证明它出现在使用真实世界环境微生物组数据构建的网络中。
{"title":"Combining compositional data sets introduces error in covariance network reconstruction.","authors":"James D Brunner, Aaron J Robinson, Patrick S G Chain","doi":"10.1093/ismeco/ycae057","DOIUrl":"10.1093/ismeco/ycae057","url":null,"abstract":"<p><p>Microbial communities are diverse biological systems that include taxa from across multiple kingdoms of life. Notably, interactions between bacteria and fungi play a significant role in determining community structure. However, these statistical associations across kingdoms are more difficult to infer than intra-kingdom associations due to the nature of the data involved using standard network inference techniques. We quantify the challenges of cross-kingdom network inference from both theoretical and practical points of view using synthetic and real-world microbiome data. We detail the theoretical issue presented by combining compositional data sets drawn from the same environment, e.g. 16S and ITS sequencing of a single set of samples, and we survey common network inference techniques for their ability to handle this error. We then test these techniques for the accuracy and usefulness of their intra- and inter-kingdom associations by inferring networks from a set of simulated samples for which a ground-truth set of associations is known. We show that while the two methods mitigate the error of cross-kingdom inference, there is little difference between techniques for key practical applications including identification of strong correlations and identification of possible keystone taxa (i.e. hub nodes in the network). Furthermore, we identify a signature of the error caused by transkingdom network inference and demonstrate that it appears in networks constructed using real-world environmental microbiome data.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11135214/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141176745","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Candidatus Accumulibacter, a key genus of polyphosphate-accumulating organisms, plays key roles in lab- and full-scale enhanced biological phosphorus removal (EBPR) systems. A total of 10 high-quality Ca. Accumulibacter genomes were recovered from EBPR systems operated at high temperatures, providing significantly updated phylogenetic and genomic insights into the Ca. Accumulibacter lineage. Among these genomes, clade IIF members SCELSE-3, SCELSE-4, and SCELSE-6 represent the to-date known genomes encoding a complete denitrification pathway, suggesting that Ca. Accumulibacter alone could achieve complete denitrification. Clade IIC members SSA1, SCUT-1, SCELCE-2, and SCELSE-8 lack the entire set of denitrifying genes, representing to-date known non-denitrifying Ca. Accumulibacter. A pan-genomic analysis with other Ca. Accumulibacter members suggested that all Ca. Accumulibacter likely has the potential to use dicarboxylic amino acids. Ca. Accumulibacter aalborgensis AALB and Ca. Accumulibacter affinis BAT3C720 seemed to be the only two members capable of using glucose for EBPR. A heat shock protein Hsp20 encoding gene was found exclusively in genomes recovered at high temperatures, which was absent in clades IA, IC, IG, IIA, IIB, IID, IIG, and II-I members. High transcription of this gene in clade IIC members SCUT-2 and SCUT-3 suggested its role in surviving high temperatures for Ca. Accumulibacter. Ambiguous clade identity was observed for newly recovered genomes (SCELSE-9 and SCELSE-10). Five machine learning models were developed using orthogroups as input features. Prediction results suggested that they belong to a new clade (IIK). The phylogeny of Ca. Accumulibacter was re-evaluated based on the laterally derived polyphosphokinase 2 gene, showing improved resolution in differentiating different clades.
{"title":"Two new clades recovered at high temperatures provide novel phylogenetic and genomic insights into <i>Candidatus</i> Accumulibacter.","authors":"Xiaojing Xie, Xuhan Deng, Jinling Chen, Liping Chen, Jing Yuan, Hang Chen, Chaohai Wei, Xianghui Liu, Guanglei Qiu","doi":"10.1093/ismeco/ycae049","DOIUrl":"10.1093/ismeco/ycae049","url":null,"abstract":"<p><p><i>Candidatus</i> Accumulibacter, a key genus of polyphosphate-accumulating organisms, plays key roles in lab- and full-scale enhanced biological phosphorus removal (EBPR) systems. A total of 10 high-quality <i>Ca</i>. Accumulibacter genomes were recovered from EBPR systems operated at high temperatures, providing significantly updated phylogenetic and genomic insights into the <i>Ca</i>. Accumulibacter lineage. Among these genomes, clade IIF members SCELSE-3, SCELSE-4, and SCELSE-6 represent the to-date known genomes encoding a complete denitrification pathway, suggesting that <i>Ca</i>. Accumulibacter alone could achieve complete denitrification. Clade IIC members SSA1, SCUT-1, SCELCE-2, and SCELSE-8 lack the entire set of denitrifying genes, representing to-date known non-denitrifying <i>Ca</i>. Accumulibacter. A pan-genomic analysis with other <i>Ca</i>. Accumulibacter members suggested that all <i>Ca</i>. Accumulibacter likely has the potential to use dicarboxylic amino acids. <i>Ca</i>. Accumulibacter aalborgensis AALB and <i>Ca</i>. Accumulibacter affinis BAT3C720 seemed to be the only two members capable of using glucose for EBPR. A heat shock protein Hsp20 encoding gene was found exclusively in genomes recovered at high temperatures, which was absent in clades IA, IC, IG, IIA, IIB, IID, IIG, and II-I members. High transcription of this gene in clade IIC members SCUT-2 and SCUT-3 suggested its role in surviving high temperatures for <i>Ca</i>. Accumulibacter. Ambiguous clade identity was observed for newly recovered genomes (SCELSE-9 and SCELSE-10). Five machine learning models were developed using orthogroups as input features. Prediction results suggested that they belong to a new clade (IIK). The phylogeny of <i>Ca</i>. Accumulibacter was re-evaluated based on the laterally derived polyphosphokinase 2 gene, showing improved resolution in differentiating different clades.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11131965/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141163080","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Weihong Zhang, Shuxin Liang, H. Grossart, Joseph Alexander Christie-Oleza, Geoffrey Michael Gadd, Yuyi Yang
Succession is a fundamental aspect of ecological theory, but studies on temporal succession trajectories and ecological driving mechanisms of plastisphere microbial communities across diverse colonization environments remain scarce and poorly understood. To fill this knowledge gap, we assessed the primary colonizers, succession trajectories, assembly, and turnover mechanisms of plastisphere prokaryotes and eukaryotes from four freshwater lakes. Our results show that differences in microbial composition similarity, temporal turnover rate, and assembly processes in the plastisphere do not exclusively occur at the kingdom level (prokaryotes and eukaryotes), but also depend on environmental conditions and colonization time. Thereby, the time of plastisphere colonization has a stronger impact on community composition and assembly of prokaryotes than eukaryoties, whereas for environmental conditions the opposite pattern holds true. Across all lakes, deterministic processes shaped the assembly of the prokaryotes, but stochastic processes that of the eukaryotes. Yet, they share similar assembly processes throughout the temporal succession: Species turnover over time causes the loss of any priority effect, which leads to a convergent succession of plastisphere microbial communities. The increase and loss of microbial diversity in different kingdoms during succession in the plastisphere potentially impacts the stability of entire microbial communities and related biogeochemical cycles. Therefore, research needs to integrate temporal dynamics along with spatial turnovers of the plastisphere microbiome. Taking the heterogeneity of global lakes and the diversity of global climate patterns into account, we highlight the urgency to investigate the spatiotemporal succession mechanism of plastisphere prokaryotes and eukaryotes in more lakes around the world.
{"title":"Convergence effect during spatiotemporal succession of lacustrine plastisphere: loss of priority effects and turnover of microbial species","authors":"Weihong Zhang, Shuxin Liang, H. Grossart, Joseph Alexander Christie-Oleza, Geoffrey Michael Gadd, Yuyi Yang","doi":"10.1093/ismeco/ycae056","DOIUrl":"https://doi.org/10.1093/ismeco/ycae056","url":null,"abstract":"\u0000 Succession is a fundamental aspect of ecological theory, but studies on temporal succession trajectories and ecological driving mechanisms of plastisphere microbial communities across diverse colonization environments remain scarce and poorly understood. To fill this knowledge gap, we assessed the primary colonizers, succession trajectories, assembly, and turnover mechanisms of plastisphere prokaryotes and eukaryotes from four freshwater lakes. Our results show that differences in microbial composition similarity, temporal turnover rate, and assembly processes in the plastisphere do not exclusively occur at the kingdom level (prokaryotes and eukaryotes), but also depend on environmental conditions and colonization time. Thereby, the time of plastisphere colonization has a stronger impact on community composition and assembly of prokaryotes than eukaryoties, whereas for environmental conditions the opposite pattern holds true. Across all lakes, deterministic processes shaped the assembly of the prokaryotes, but stochastic processes that of the eukaryotes. Yet, they share similar assembly processes throughout the temporal succession: Species turnover over time causes the loss of any priority effect, which leads to a convergent succession of plastisphere microbial communities. The increase and loss of microbial diversity in different kingdoms during succession in the plastisphere potentially impacts the stability of entire microbial communities and related biogeochemical cycles. Therefore, research needs to integrate temporal dynamics along with spatial turnovers of the plastisphere microbiome. Taking the heterogeneity of global lakes and the diversity of global climate patterns into account, we highlight the urgency to investigate the spatiotemporal succession mechanism of plastisphere prokaryotes and eukaryotes in more lakes around the world.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140689188","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-15eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae055
Solène L Y Moulin, Sarah Frail, Thomas Braukmann, Jon Doenier, Melissa Steele-Ogus, Jane C Marks, Matthew M Mills, Ellen Yeh
Epithemia spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or diazoplasts, derived from cyanobacteria. These algae are a rare example of photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, E. clementina, as a model to investigate endosymbiotic acquisition of nitrogen fixation. We demonstrate that the diazoplast, which has lost photosynthesis, provides fixed nitrogen to the diatom host in exchange for fixed carbon. To identify the metabolic changes associated with this endosymbiotic specialization, we compared the Epithemia diazoplast with its close, free-living cyanobacterial relative, Crocosphaera subtropica. Unlike C. subtropica, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to C. subtropica with retention of the oxidative pentose phosphate pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. Altogether, we establish a new model for studying endosymbiosis, perform a functional characterization of this diazotroph endosymbiosis, and identify metabolic adaptations for endosymbiotic acquisition of a critical biological function.
Epithemia spp.硅藻含有来自蓝藻的强制性固氮内共生体或重氮体。这些藻类是光合真核生物中成功将含氧光合作用与氧敏感的氮酶活性结合起来的罕见例子。在这里,我们报告了一个新分离出来的物种--克莱门特藻(E. clementina),并将其作为研究内共生获得固氮作用的模型。我们证明,失去光合作用的重氮质体向硅藻宿主提供固定氮以交换固定碳。为了确定与这种内共生特化相关的代谢变化,我们将重氮原生质表皮藻与其近亲、自由生活的蓝藻--亚热带栉水母(Crocosphaera subtropica)进行了比较。与亚热带蓝藻不同的是,重氮质体中的氮酶活动与光合作用在时间上是分离的,而我们的研究表明,重氮质体中的氮酶活动在白天(与寄主光合作用同时进行)和夜间都是持续进行的。宿主和重氮酵母的新陈代谢紧密耦合,以支持氮酶的活性:抑制光合作用会取消白天的氮酶活性,而夜间的氮酶活性不再需要蓝藻糖原储存途径。相反,在整个昼夜周期中,宿主碳水化合物的输入支持着氮酶的活性。与亚热带蓝藻相比,重氮藻体中的碳水化合物代谢得到了简化,保留了磷酸戊糖氧化途径和氧化磷酸化作用。与杂囊类似,这些途径可能经过优化,以支持氮酶活性,提供还原当量和 ATP 并消耗氧气。我们的研究结果表明,重氮质体专门用于内共生固氮。总之,我们建立了一个研究内共生的新模型,对这种重氮内共生进行了功能表征,并确定了内共生获得关键生物功能的代谢适应性。
{"title":"The endosymbiont of <i>Epithemia clementina</i> is specialized for nitrogen fixation within a photosynthetic eukaryote.","authors":"Solène L Y Moulin, Sarah Frail, Thomas Braukmann, Jon Doenier, Melissa Steele-Ogus, Jane C Marks, Matthew M Mills, Ellen Yeh","doi":"10.1093/ismeco/ycae055","DOIUrl":"10.1093/ismeco/ycae055","url":null,"abstract":"<p><p><i>Epithemia</i> spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or diazoplasts, derived from cyanobacteria. These algae are a rare example of photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, <i>E. clementina</i>, as a model to investigate endosymbiotic acquisition of nitrogen fixation. We demonstrate that the diazoplast, which has lost photosynthesis, provides fixed nitrogen to the diatom host in exchange for fixed carbon. To identify the metabolic changes associated with this endosymbiotic specialization, we compared the <i>Epithemia</i> diazoplast with its close, free-living cyanobacterial relative, <i>Crocosphaera subtropica</i>. Unlike <i>C. subtropica</i>, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to <i>C. subtropica</i> with retention of the oxidative pentose phosphate pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. Altogether, we establish a new model for studying endosymbiosis, perform a functional characterization of this diazotroph endosymbiosis, and identify metabolic adaptations for endosymbiotic acquisition of a critical biological function.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11070190/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140869764","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-15eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae053
Víctor Hugo Jarquín-Díaz, Susana Carolina Martins Ferreira, Alice Balard, Ľudovít Ďureje, Milos Macholán, Jaroslav Piálek, Johan Bengtsson-Palme, Stephanie Kramer-Schadt, Sofia Kirke Forslund-Startceva, Emanuel Heitlinger
Antibiotic resistance is a priority public health problem resulting from eco-evolutionary dynamics within microbial communities and their interaction at a mammalian host interface or geographical scale. The links between mammalian host genetics, bacterial gut community, and antimicrobial resistance gene (ARG) content must be better understood in natural populations inhabiting heterogeneous environments. Hybridization, the interbreeding of genetically divergent populations, influences different components of the gut microbial communities. However, its impact on bacterial traits such as antibiotic resistance is unknown. Here, we present that hybridization might shape bacterial communities and ARG occurrence. We used amplicon sequencing to study the gut microbiome and to predict ARG composition in natural populations of house mice (Mus musculus). We compared gastrointestinal bacterial and ARG diversity, composition, and abundance across a gradient of pure and hybrid genotypes in the European House Mouse Hybrid Zone. We observed an increased overall predicted richness of ARG in hybrid mice. We found bacteria-ARG interactions by their co-abundance and detected phenotypes of extreme abundances in hybrid mice at the level of specific bacterial taxa and ARGs, mainly multidrug resistance genes. Our work suggests that mammalian host genetic variation impacts the gut microbiome and chromosomal ARGs. However, it raises further questions on how the mammalian host genetics impact ARGs via microbiome dynamics or environmental covariates.
{"title":"Aberrant microbiomes are associated with increased antibiotic resistance gene load in hybrid mice.","authors":"Víctor Hugo Jarquín-Díaz, Susana Carolina Martins Ferreira, Alice Balard, Ľudovít Ďureje, Milos Macholán, Jaroslav Piálek, Johan Bengtsson-Palme, Stephanie Kramer-Schadt, Sofia Kirke Forslund-Startceva, Emanuel Heitlinger","doi":"10.1093/ismeco/ycae053","DOIUrl":"10.1093/ismeco/ycae053","url":null,"abstract":"<p><p>Antibiotic resistance is a priority public health problem resulting from eco-evolutionary dynamics within microbial communities and their interaction at a mammalian host interface or geographical scale. The links between mammalian host genetics, bacterial gut community, and antimicrobial resistance gene (ARG) content must be better understood in natural populations inhabiting heterogeneous environments. Hybridization, the interbreeding of genetically divergent populations, influences different components of the gut microbial communities. However, its impact on bacterial traits such as antibiotic resistance is unknown. Here, we present that hybridization might shape bacterial communities and ARG occurrence. We used amplicon sequencing to study the gut microbiome and to predict ARG composition in natural populations of house mice (<i>Mus musculus</i>). We compared gastrointestinal bacterial and ARG diversity, composition, and abundance across a gradient of pure and hybrid genotypes in the European House Mouse Hybrid Zone. We observed an increased overall predicted richness of ARG in hybrid mice. We found bacteria-ARG interactions by their co-abundance and detected phenotypes of extreme abundances in hybrid mice at the level of specific bacterial taxa and ARGs, mainly multidrug resistance genes. Our work suggests that mammalian host genetic variation impacts the gut microbiome and chromosomal ARGs. However, it raises further questions on how the mammalian host genetics impact ARGs via microbiome dynamics or environmental covariates.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11128261/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141155248","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-15eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae054
Justin Maire, Astrid Collingro, Matthias Horn, Madeleine J H van Oppen
Cnidarians, such as corals and sea anemones, associate with a wide range of bacteria that have essential functions, including nutrient cycling and the production of antimicrobial compounds. Within cnidarians, bacteria can colonize all microhabitats including the tissues. Among them are obligate intracellular bacteria of the phylum Chlamydiota (chlamydiae) whose impact on cnidarian hosts and holobionts, especially corals, remain unknown. Here, we conducted a meta-analysis of previously published 16S rRNA gene metabarcoding data from cnidarians (e.g. coral, jellyfish, and anemones), eight metagenome-assembled genomes (MAGs) of coral-associated chlamydiae, and one MAG of jellyfish-associated chlamydiae to decipher their diversity and functional potential. While the metabarcoding dataset showed an enormous diversity of cnidarian-associated chlamydiae, six out of nine MAGs were affiliated with the Simkaniaceae family. The other three MAGs were assigned to the Parasimkaniaceae, Rhabdochlamydiaceae, and Anoxychlamydiaceae, respectively. All MAGs lacked the genes necessary for an independent existence, lacking any nucleotide or vitamin and most amino acid biosynthesis pathways. Hallmark chlamydial genes, such as a type III secretion system, nucleotide transporters, and genes for host interaction, were encoded in all MAGs. Together these observations suggest an obligate intracellular lifestyle of coral-associated chlamydiae. No unique genes were found in coral-associated chlamydiae, suggesting a lack of host specificity. Additional studies are needed to understand how chlamydiae interact with their coral host, and other microbes in coral holobionts. This first study of the diversity and functional potential of coral-associated chlamydiae improves our understanding of both the coral microbiome and the chlamydial lifestyle and host range.
{"title":"Chlamydiae in corals: shared functional potential despite broad taxonomic diversity.","authors":"Justin Maire, Astrid Collingro, Matthias Horn, Madeleine J H van Oppen","doi":"10.1093/ismeco/ycae054","DOIUrl":"https://doi.org/10.1093/ismeco/ycae054","url":null,"abstract":"<p><p>Cnidarians, such as corals and sea anemones, associate with a wide range of bacteria that have essential functions, including nutrient cycling and the production of antimicrobial compounds. Within cnidarians, bacteria can colonize all microhabitats including the tissues. Among them are obligate intracellular bacteria of the phylum Chlamydiota (chlamydiae) whose impact on cnidarian hosts and holobionts, especially corals, remain unknown. Here, we conducted a meta-analysis of previously published 16S rRNA gene metabarcoding data from cnidarians (e.g. coral, jellyfish, and anemones), eight metagenome-assembled genomes (MAGs) of coral-associated chlamydiae, and one MAG of jellyfish-associated chlamydiae to decipher their diversity and functional potential. While the metabarcoding dataset showed an enormous diversity of cnidarian-associated chlamydiae, six out of nine MAGs were affiliated with the Simkaniaceae family. The other three MAGs were assigned to the Parasimkaniaceae, Rhabdochlamydiaceae, and Anoxychlamydiaceae, respectively. All MAGs lacked the genes necessary for an independent existence, lacking any nucleotide or vitamin and most amino acid biosynthesis pathways. Hallmark chlamydial genes, such as a type III secretion system, nucleotide transporters, and genes for host interaction, were encoded in all MAGs. Together these observations suggest an obligate intracellular lifestyle of coral-associated chlamydiae. No unique genes were found in coral-associated chlamydiae, suggesting a lack of host specificity. Additional studies are needed to understand how chlamydiae interact with their coral host, and other microbes in coral holobionts. This first study of the diversity and functional potential of coral-associated chlamydiae improves our understanding of both the coral microbiome and the chlamydial lifestyle and host range.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11070183/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140853788","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-11eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae037
Haidi Xu, Nicholas A Pudlo, Thaisa M Cantu-Jungles, Yunus E Tuncil, Xin Nie, Amandeep Kaur, Bradley L Reuhs, Eric C Martens, Bruce R Hamaker
Structurally complex corn bran arabinoxylan (CAX) was used as a model glycan to investigate gut bacteria growth and competition on different AX-based fine structures. Nine hydrolyzate segments of the CAX polymer varying in chemical structure (sugars and linkages), CAX, five less complex non-corn arabinoxylans, and xylose and glucose were ranked from structurally complex to simple. The substrate panel promoted different overall growth and rates of growth of eight Bacteroides xylan-degrading strains. For example, Bacteroides cellulosilyticus DSM 14838 (Bacteroides cellulosilyticus) grew well on an array of complex and simple structures, while Bacteroides ovatus 3-1-23 grew well only on the simple structures. In a competition experiment, B. cellulosilyticus growth was favored over B. ovatus on the complex AX-based structure. On the other hand, on the simple structure, B. ovatus strongly outcompeted B. cellulosilyticus, which was eliminated from the competitive environment by Day 11. This adaptation to fine structure and resulting competition dynamics indicate that dietary fiber chemical structures, whether complex or simple, favor certain gut bacteria. Overall, this work supports a concept that fiber degraders diversify their competitive abilities to access substrates across the spectrum of heterogeneity of fine structural features of dietary fibers.
{"title":"When simplicity triumphs: niche specialization of gut bacteria exists even for simple fiber structures.","authors":"Haidi Xu, Nicholas A Pudlo, Thaisa M Cantu-Jungles, Yunus E Tuncil, Xin Nie, Amandeep Kaur, Bradley L Reuhs, Eric C Martens, Bruce R Hamaker","doi":"10.1093/ismeco/ycae037","DOIUrl":"https://doi.org/10.1093/ismeco/ycae037","url":null,"abstract":"<p><p>Structurally complex corn bran arabinoxylan (CAX) was used as a model glycan to investigate gut bacteria growth and competition on different AX-based fine structures. Nine hydrolyzate segments of the CAX polymer varying in chemical structure (sugars and linkages), CAX, five less complex non-corn arabinoxylans, and xylose and glucose were ranked from structurally complex to simple. The substrate panel promoted different overall growth and rates of growth of eight <i>Bacteroides</i> xylan-degrading strains. For example, <i>Bacteroides cellulosilyticus</i> DSM 14838 (<i>Bacteroides cellulosilyticus</i>) grew well on an array of complex and simple structures, while <i>Bacteroides ovatus</i> 3-1-23 grew well only on the simple structures. In a competition experiment, <i>B. cellulosilyticus</i> growth was favored over <i>B. ovatus</i> on the complex AX-based structure. On the other hand, on the simple structure, <i>B. ovatus</i> strongly outcompeted <i>B. cellulosilyticus</i>, which was eliminated from the competitive environment by Day 11. This adaptation to fine structure and resulting competition dynamics indicate that dietary fiber chemical structures, whether complex or simple, favor certain gut bacteria. Overall, this work supports a concept that fiber degraders diversify their competitive abilities to access substrates across the spectrum of heterogeneity of fine structural features of dietary fibers.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11032216/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140874311","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The phylum Chloroflexota has been found to exhibit high abundance in the microbial communities from wastewater treatment plants (WWTPs) in both aerobic and anaerobic systems. However, its metabolic role has not been fully explored due to the lack of cultured isolates. To address this gap, we use publicly available metagenome datasets from both activated sludge (AS) and methanogenic (MET) full-scale wastewater treatment reactors to assembled genomes. Using this strategy, 264 dereplicated, medium- and high-quality metagenome-assembled genomes (MAGs) classified within Chloroflexota were obtained. Taxonomic classification revealed that AS and MET reactors harbored distinct Chloroflexota families. Nonetheless, the majority of the annotated MAGs (166 MAGs with >85% completeness and < 5% contamination) shared most of the metabolic potential features, including the ability to degrade simple sugars and complex polysaccharides, fatty acids and amino acids, as well as perform fermentation of different products. While Chloroflexota MAGs from MET reactors showed the potential for strict fermentation, MAGs from AS harbored the potential for facultatively aerobic metabolism. Metabolic reconstruction of Chloroflexota members from AS unveiled their versatile metabolism and suggested a primary role in hydrolysis, carbon removal and involvement in nitrogen cycling, thus establishing them as fundamental components of the ecosystem. Microbial reference genomes are essential resources for understanding the potential functional role of uncultured organisms in WWTPs. Our study provides a comprehensive genome catalog of Chloroflexota for future analyses aimed at elucidating their role in these ecosystems.
在好氧和厌氧系统的污水处理厂(WWTPs)微生物群落中,人们发现了大量的绿藻门(Chloroflexota)。然而,由于缺乏培养分离物,人们尚未充分探索其代谢作用。为了填补这一空白,我们利用从活性污泥(AS)和产甲烷(MET)全规模废水处理反应器中公开获得的元基因组数据集来组装基因组。利用这一策略,获得了 264 个去复制的、中等质量和高质量的元基因组组装基因组(MAGs),并将其归类为 Chloroflexota。分类学分类显示,AS 和 MET 反应物蕴藏着不同的 Chloroflexota 家族。不过,大多数已注释的 MAGs(166 个 MAGs 的完整性大于 85%,污染率小于 5%)都具有大多数代谢潜能特征,包括降解单糖和复杂多糖、脂肪酸和氨基酸的能力,以及对不同产物进行发酵的能力。来自 MET 反应器的绿僵菌 MAGs 具有严格发酵的潜力,而来自 AS 的 MAGs 则具有兼氧代谢的潜力。对来自 AS 的 Chloroflexota 成员的代谢重建揭示了它们的多功能代谢,并表明它们在水解、碳清除和氮循环中的主要作用,从而将它们确立为生态系统的基本组成部分。微生物参考基因组是了解污水处理厂中未培养生物潜在功能作用的重要资源。我们的研究为今后旨在阐明它们在这些生态系统中的作用的分析提供了一个全面的绿僵菌基因组目录。
{"title":"Unveiling the hidden diversity and functional role of Chloroflexota in full-scale wastewater treatment plants through genome-centric analyses","authors":"P. Bovio-Winkler, A. Cabezas, C. Etchebehere","doi":"10.1093/ismeco/ycae050","DOIUrl":"https://doi.org/10.1093/ismeco/ycae050","url":null,"abstract":"\u0000 The phylum Chloroflexota has been found to exhibit high abundance in the microbial communities from wastewater treatment plants (WWTPs) in both aerobic and anaerobic systems. However, its metabolic role has not been fully explored due to the lack of cultured isolates. To address this gap, we use publicly available metagenome datasets from both activated sludge (AS) and methanogenic (MET) full-scale wastewater treatment reactors to assembled genomes. Using this strategy, 264 dereplicated, medium- and high-quality metagenome-assembled genomes (MAGs) classified within Chloroflexota were obtained. Taxonomic classification revealed that AS and MET reactors harbored distinct Chloroflexota families. Nonetheless, the majority of the annotated MAGs (166 MAGs with >85% completeness and < 5% contamination) shared most of the metabolic potential features, including the ability to degrade simple sugars and complex polysaccharides, fatty acids and amino acids, as well as perform fermentation of different products. While Chloroflexota MAGs from MET reactors showed the potential for strict fermentation, MAGs from AS harbored the potential for facultatively aerobic metabolism. Metabolic reconstruction of Chloroflexota members from AS unveiled their versatile metabolism and suggested a primary role in hydrolysis, carbon removal and involvement in nitrogen cycling, thus establishing them as fundamental components of the ecosystem. Microbial reference genomes are essential resources for understanding the potential functional role of uncultured organisms in WWTPs. Our study provides a comprehensive genome catalog of Chloroflexota for future analyses aimed at elucidating their role in these ecosystems.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140714359","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-04-09eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae044
Zhe Pan, Tao Ma, Michael Steele, Le Luo Guan
Perturbations and modulations during early life are vital to affect gut microbiome assembly and establishment. In this study, we assessed how microbial communities shifted during calf diarrhea and with probiotic yeast supplementation (Saccharomyces cerevisiae var. boulardii, SCB) and determined the key bacterial taxa contributing to the microbial assembly shifts using a total of 393 fecal samples collected from 84 preweaned calves during an 8-week trial. Our results revealed that the microbial assembly patterns differed between healthy and diarrheic calves at 6- and 8-week of the trial, with healthy calves being stochastic-driven and diarrheic calves being deterministic-driven. The two-state Markov model revealed that SCB supplementation had a higher possibility to shift microbial assembly from deterministic- to stochastic-driven in diarrheic calves. Furthermore, a total of 23 and 21 genera were specific ecotypes to assembly patterns in SCB-responsive (SCB-fed calves did not exhibit diarrhea) and nonresponsive (SCB-fed calves occurred diarrhea) calves, respectively. Among these ecotypes, the area under a receiver operating characteristic curve revealed that Blautia and Ruminococcaceae UCG 014, two unidentified genera from the Ruminococcaceae family, had the highest predictiveness for microbial assembly patterns in SCB-responsive calves, while Prevotellaceae, Blautia, and Escherichia-Shigella were the most predictive bacterial taxa for microbial assembly patterns in SCB-nonresponsive calves. Our study suggests that microbiome perturbations and probiotic yeast supplementation serving as deterministic factors influenced assembly patterns during early life with critical genera being predictive for assembly patterns, which sheds light on mechanisms of microbial community establishment in the gut of neonatal calves during early life.
{"title":"Varied microbial community assembly and specialization patterns driven by early life microbiome perturbation and modulation in young ruminants.","authors":"Zhe Pan, Tao Ma, Michael Steele, Le Luo Guan","doi":"10.1093/ismeco/ycae044","DOIUrl":"https://doi.org/10.1093/ismeco/ycae044","url":null,"abstract":"<p><p>Perturbations and modulations during early life are vital to affect gut microbiome assembly and establishment. In this study, we assessed how microbial communities shifted during calf diarrhea and with probiotic yeast supplementation (<i>Saccharomyces cerevisiae var. boulardii</i>, SCB) and determined the key bacterial taxa contributing to the microbial assembly shifts using a total of 393 fecal samples collected from 84 preweaned calves during an 8-week trial. Our results revealed that the microbial assembly patterns differed between healthy and diarrheic calves at 6- and 8-week of the trial, with healthy calves being stochastic-driven and diarrheic calves being deterministic-driven. The two-state Markov model revealed that SCB supplementation had a higher possibility to shift microbial assembly from deterministic- to stochastic-driven in diarrheic calves. Furthermore, a total of 23 and 21 genera were specific ecotypes to assembly patterns in SCB-responsive (SCB-fed calves did not exhibit diarrhea) and nonresponsive (SCB-fed calves occurred diarrhea) calves, respectively. Among these ecotypes, the area under a receiver operating characteristic curve revealed that <i>Blautia</i> and <i>Ruminococcaceae</i> UCG 014, two unidentified genera from the <i>Ruminococcaceae</i> family, had the highest predictiveness for microbial assembly patterns in SCB-responsive calves, while <i>Prevotellaceae</i>, <i>Blautia</i>, and <i>Escherichia-Shigella</i> were the most predictive bacterial taxa for microbial assembly patterns in SCB-nonresponsive calves. Our study suggests that microbiome perturbations and probiotic yeast supplementation serving as deterministic factors influenced assembly patterns during early life with critical genera being predictive for assembly patterns, which sheds light on mechanisms of microbial community establishment in the gut of neonatal calves during early life.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11033733/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140869765","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Noritaka Aoki, T. Shimasaki, Wataru Yazaki, Tomoaki Sato, Masaru Nakayasu, A. Ando, S. Kishino, Jun Ogawa, Sachiko Masuda, Arisa Shibata, Ken Shirasu, K. Yazaki, A. Sugiyama
Plant roots secrete various metabolites, including plant specialized metabolites, into the rhizosphere, and shape the rhizosphere microbiome, which is crucial for the plant health and growth. Isoflavones are major plant specialized metabolites found in legume plants, and are involved in interactions with soil microorganisms as initiation signals in rhizobial symbiosis and as modulators of the legume root microbiota. However, it remains largely unknown the molecular basis underlying the isoflavone-mediated interkingdom interactions in the legume rhizosphere. Here, we isolated Variovorax sp. strain V35, a member of the Comamonadaceae that harbors isoflavone-degrading activity, from soybean roots and discovered a gene cluster responsible for isoflavone degradation named ifc. The characterization of ifc mutants and heterologously expressed Ifc enzymes revealed that isoflavones undergo oxidative catabolism, which is different from the reductive metabolic pathways observed in gut microbiota. We further demonstrated that the ifc genes are frequently found in bacterial strains isolated from legume plants, including mutualistic rhizobia, and contribute to the detoxification of the antibacterial activity of isoflavones. Taken together, our findings reveal an isoflavone catabolism gene cluster in the soybean root microbiota, providing molecular insights into isoflavone-mediated legume–microbiota interactions.
{"title":"An Isoflavone catabolism gene cluster underlying Interkingdom interactions in the soybean rhizosphere","authors":"Noritaka Aoki, T. Shimasaki, Wataru Yazaki, Tomoaki Sato, Masaru Nakayasu, A. Ando, S. Kishino, Jun Ogawa, Sachiko Masuda, Arisa Shibata, Ken Shirasu, K. Yazaki, A. Sugiyama","doi":"10.1093/ismeco/ycae052","DOIUrl":"https://doi.org/10.1093/ismeco/ycae052","url":null,"abstract":"\u0000 Plant roots secrete various metabolites, including plant specialized metabolites, into the rhizosphere, and shape the rhizosphere microbiome, which is crucial for the plant health and growth. Isoflavones are major plant specialized metabolites found in legume plants, and are involved in interactions with soil microorganisms as initiation signals in rhizobial symbiosis and as modulators of the legume root microbiota. However, it remains largely unknown the molecular basis underlying the isoflavone-mediated interkingdom interactions in the legume rhizosphere. Here, we isolated Variovorax sp. strain V35, a member of the Comamonadaceae that harbors isoflavone-degrading activity, from soybean roots and discovered a gene cluster responsible for isoflavone degradation named ifc. The characterization of ifc mutants and heterologously expressed Ifc enzymes revealed that isoflavones undergo oxidative catabolism, which is different from the reductive metabolic pathways observed in gut microbiota. We further demonstrated that the ifc genes are frequently found in bacterial strains isolated from legume plants, including mutualistic rhizobia, and contribute to the detoxification of the antibacterial activity of isoflavones. Taken together, our findings reveal an isoflavone catabolism gene cluster in the soybean root microbiota, providing molecular insights into isoflavone-mediated legume–microbiota interactions.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140725783","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}