Pub Date : 2024-05-08eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae070
Yanchen Sun, Yongchao Yin, Guang He, Gyuhyon Cha, Héctor L Ayala-Del-Río, Grizelle González, Konstantinos T Konstantinidis, Frank E Löffler
Nitrous oxide (N2O), a greenhouse gas with ozone destruction potential, is mitigated by the microbial reduction to dinitrogen catalyzed by N2O reductase (NosZ). Bacteria with NosZ activity have been studied at circumneutral pH but the microbiology of low pH N2O reduction has remained elusive. Acidic (pH < 5) tropical forest soils were collected in the Luquillo Experimental Forest in Puerto Rico, and microcosms maintained with low (0.02 mM) and high (2 mM) N2O assessed N2O reduction at pH 4.5 and 7.3. All microcosms consumed N2O, with lag times of up to 7 months observed in microcosms with 2 mM N2O. Comparative metagenome analysis revealed that Rhodocyclaceae dominated in circumneutral microcosms under both N2O feeding regimes. At pH 4.5, Peptococcaceae dominated in high-N2O, and Hyphomicrobiaceae in low-N2O microcosms. Seventeen high-quality metagenome-assembled genomes (MAGs) recovered from the N2O-reducing microcosms harbored nos operons, with all eight MAGs derived from acidic microcosms carrying the Clade II type nosZ and lacking nitrite reductase genes (nirS/K). Five of the eight MAGs recovered from pH 4.5 microcosms represent novel taxa indicating an unexplored N2O-reducing diversity exists in acidic tropical soils. A survey of pH 3.5-5.7 soil metagenome datasets revealed that nosZ genes commonly occur, suggesting broad distribution of N2O reduction potential in acidic soils.
{"title":"pH selects for distinct N<sub>2</sub>O-reducing microbiomes in tropical soil microcosms.","authors":"Yanchen Sun, Yongchao Yin, Guang He, Gyuhyon Cha, Héctor L Ayala-Del-Río, Grizelle González, Konstantinos T Konstantinidis, Frank E Löffler","doi":"10.1093/ismeco/ycae070","DOIUrl":"10.1093/ismeco/ycae070","url":null,"abstract":"<p><p>Nitrous oxide (N<sub>2</sub>O), a greenhouse gas with ozone destruction potential, is mitigated by the microbial reduction to dinitrogen catalyzed by N<sub>2</sub>O reductase (NosZ). Bacteria with NosZ activity have been studied at circumneutral pH but the microbiology of low pH N<sub>2</sub>O reduction has remained elusive. Acidic (pH < 5) tropical forest soils were collected in the Luquillo Experimental Forest in Puerto Rico, and microcosms maintained with low (0.02 mM) and high (2 mM) N<sub>2</sub>O assessed N<sub>2</sub>O reduction at pH 4.5 and 7.3. All microcosms consumed N<sub>2</sub>O, with lag times of up to 7 months observed in microcosms with 2 mM N<sub>2</sub>O. Comparative metagenome analysis revealed that <i>Rhodocyclaceae</i> dominated in circumneutral microcosms under both N<sub>2</sub>O feeding regimes. At pH 4.5, <i>Peptococcaceae</i> dominated in high-N<sub>2</sub>O, and <i>Hyphomicrobiaceae</i> in low-N<sub>2</sub>O microcosms. Seventeen high-quality metagenome-assembled genomes (MAGs) recovered from the N<sub>2</sub>O-reducing microcosms harbored <i>nos</i> operons, with all eight MAGs derived from acidic microcosms carrying the Clade II type <i>nosZ</i> and lacking nitrite reductase genes (<i>nirS</i>/<i>K</i>). Five of the eight MAGs recovered from pH 4.5 microcosms represent novel taxa indicating an unexplored N<sub>2</sub>O-reducing diversity exists in acidic tropical soils. A survey of pH 3.5-5.7 soil metagenome datasets revealed that <i>nosZ</i> genes commonly occur, suggesting broad distribution of N<sub>2</sub>O reduction potential in acidic soils.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11131594/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141163210","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}
Lichens are remarkable and classic examples of symbiotic organisms that have fascinated scientists for centuries. Yet, it has only been for a couple of decades that significant advances have focused on the diversity of their green algal and/or cyanobacterial photobionts. Cyanolichens, which contain cyanobacteria as their photosynthetic partner, include up to 10% of all known lichens and as such, studies on their cyanobionts are much rarer compared to their green algal counterparts. For the unicellular cyanobionts, i.e., cyanobacteria that do not form filaments, these studies are even scarcer. Nonetheless, these currently include at least 10 different genera in the cosmopolitan lichen order Lichinales. An international consortium (International Network of Cyanobionts; INCb) will tackle this lack of knowledge. In this article, we discuss the status of current unicellular cyanobiont research, compare the taxonomic resolution of photobionts from cyanolichens with those of green algal lichens (chlorolichens), and give a roadmap of research on how to recondition the underestimated fraction of symbiotic unicellular cyanobacteria in lichens.
{"title":"The underestimated fraction: diversity, challenges and novel insights into unicellular cyanobionts of lichens","authors":"Patrick Jung, Laura Briegel-Williams","doi":"10.1093/ismeco/ycae069","DOIUrl":"https://doi.org/10.1093/ismeco/ycae069","url":null,"abstract":"\u0000 Lichens are remarkable and classic examples of symbiotic organisms that have fascinated scientists for centuries. Yet, it has only been for a couple of decades that significant advances have focused on the diversity of their green algal and/or cyanobacterial photobionts. Cyanolichens, which contain cyanobacteria as their photosynthetic partner, include up to 10% of all known lichens and as such, studies on their cyanobionts are much rarer compared to their green algal counterparts. For the unicellular cyanobionts, i.e., cyanobacteria that do not form filaments, these studies are even scarcer. Nonetheless, these currently include at least 10 different genera in the cosmopolitan lichen order Lichinales. An international consortium (International Network of Cyanobionts; INCb) will tackle this lack of knowledge. In this article, we discuss the status of current unicellular cyanobiont research, compare the taxonomic resolution of photobionts from cyanolichens with those of green algal lichens (chlorolichens), and give a roadmap of research on how to recondition the underestimated fraction of symbiotic unicellular cyanobacteria in lichens.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141009015","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}
Particulate carbon (C) degradation in soils is a critical process in the global C cycle governing greenhouse gas fluxes and C storage. Millimeter-scale soil aggregates impose strong controls on particulate C degradation by inducing chemical gradients of e.g., oxygen, as well as limiting microbial mobility in pore structures. To date, experimental models of soil aggregates have incorporated porosity and chemical gradients but not particulate C. Here, we demonstrate a proof-of-concept encapsulating microbial cells and particulate C substrates in hydrogel matrices as a novel experimental model for soil aggregates. Ruminiclostridium cellulolyticum was co-encapsulated with cellulose in millimeter-scale polyethyleneglycol-dimethacrylate (PEGDMA) hydrogel beads. Microbial activity was delayed in hydrogel-encapsulated conditions, with cellulose degradation and fermentation activity being observed after 13 days of incubation. Unexpectedly, hydrogel encapsulation shifted product formation of R. cellulolyticum from an ethanol-lactate-acetate mixture to an acetate-dominated product profile. Fluorescence microscopy enabled simultaneous visualization of the PEGDMA matrix, cellulose particles, and individual cells in the matrix, demonstrating growth on cellulose particles during incubation. Together, these microbe-cellulose-PEGDMA hydrogels present a novel, reproducible experimental soil surrogate to connect single cells to process outcomes at the scale of soil aggregates and ecosystems.
土壤中的微粒碳（C）降解是全球碳循环中的一个关键过程，影响着温室气体通量和碳储存。毫米尺度的土壤团聚体通过诱导氧等化学梯度以及限制孔隙结构中微生物的流动性，对微粒碳降解施加了强有力的控制。迄今为止，土壤团聚体的实验模型都包含孔隙度和化学梯度，但不包括微粒碳。在这里，我们展示了一种概念验证方法，即在水凝胶基质中封装微生物细胞和微粒碳基质，作为土壤团聚体的新型实验模型。纤维素溶解瘤反刍梭菌与纤维素共同被包裹在毫米级聚乙二醇二甲基丙烯酸酯（PEGDMA）水凝胶珠中。在水凝胶包囊条件下，微生物的活性被延迟，培养 13 天后才能观察到纤维素降解和发酵活性。意想不到的是，水凝胶封装使 R. cellulolyticum 的产物形成从乙醇-乳酸-乙酸酯混合物转变为以乙酸酯为主的产物。荧光显微镜可同时观察到 PEGDMA 基质、纤维素颗粒和基质中的单个细胞，显示了培养过程中纤维素颗粒上的生长情况。总之，这些微生物-纤维素-PEGDMA 水凝胶提供了一种新颖、可重复的实验土壤替代物，可将单细胞与土壤聚集体和生态系统规模的过程结果联系起来。
{"title":"Microbe-cellulose hydrogels as a model system for particulate carbon degradation in soil aggregates","authors":"Pieter Candry, Bruce J Godfrey, M. K. Winkler","doi":"10.1093/ismeco/ycae068","DOIUrl":"https://doi.org/10.1093/ismeco/ycae068","url":null,"abstract":"\u0000 Particulate carbon (C) degradation in soils is a critical process in the global C cycle governing greenhouse gas fluxes and C storage. Millimeter-scale soil aggregates impose strong controls on particulate C degradation by inducing chemical gradients of e.g., oxygen, as well as limiting microbial mobility in pore structures. To date, experimental models of soil aggregates have incorporated porosity and chemical gradients but not particulate C. Here, we demonstrate a proof-of-concept encapsulating microbial cells and particulate C substrates in hydrogel matrices as a novel experimental model for soil aggregates. Ruminiclostridium cellulolyticum was co-encapsulated with cellulose in millimeter-scale polyethyleneglycol-dimethacrylate (PEGDMA) hydrogel beads. Microbial activity was delayed in hydrogel-encapsulated conditions, with cellulose degradation and fermentation activity being observed after 13 days of incubation. Unexpectedly, hydrogel encapsulation shifted product formation of R. cellulolyticum from an ethanol-lactate-acetate mixture to an acetate-dominated product profile. Fluorescence microscopy enabled simultaneous visualization of the PEGDMA matrix, cellulose particles, and individual cells in the matrix, demonstrating growth on cellulose particles during incubation. Together, these microbe-cellulose-PEGDMA hydrogels present a novel, reproducible experimental soil surrogate to connect single cells to process outcomes at the scale of soil aggregates and ecosystems.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141013158","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}
Ona Deulofeu-Capo, Marta Sebastián, Adrià Auladell, Clara Cardelús, I. Ferrera, Olga Sánchez, J. Gasol
Marine prokaryotes play crucial roles in ocean biogeochemical cycles, being their contribution strongly influenced by their growth rates. Hence, elucidating the variability and phylogenetic imprint of marine prokaryotes' growth rates are crucial for better determining the role of individual taxa in biogeochemical cycles. Here, we estimated prokaryotic growth rates at high phylogenetic resolution in manipulation experiments using water from the northwestern Mediterranean Sea. Experiments were run in the four seasons with different treatments that reduced growth limiting factors: predators, nutrient availability, viruses, and light. Single-amplicon sequence variants (ASVs)-based growth rates were calculated from changes in estimated absolute abundances using total prokaryotic abundance and the proportion of each individual ASV. The trends obtained for growth rates in the different experiments were consistent with other estimates based on total cell-counts, CARD-FISH subcommunity cell-counts or metagenomic-OTUs. Our calculations unveil a broad range of growth rates [0.3-10 d-1] with significant variability even within closely related ASVs. Likewise, the impact of growth limiting factors changed over the year for individual ASVs. High numbers of responsive ASVs were shared between winter and spring seasons, as well as throughout the year in the treatments with reduced nutrient limitation and viral pressure. The most responsive ASVs were rare in the in situ communities, comprising a large pool of taxa with the potential to rapidly respond to environmental changes. Essentially, our results highlight the lack of phylogenetic coherence in the range of growth rates observed, and differential responses to the various limiting factors, even for closely related taxa.
海洋原核生物在海洋生物地球化学循环中发挥着至关重要的作用，它们的贡献受其生长速率的强烈影响。因此，阐明海洋原核生物生长率的变异性和系统发育印记对于更好地确定各个类群在生物地球化学循环中的作用至关重要。在此，我们利用地中海西北部的海水进行了操纵实验，以较高的系统发育分辨率估算了原核生物的生长率。实验在四季进行，采用了不同的处理方法，减少了限制生长的因素：捕食者、营养供应、病毒和光照。利用原核生物总丰度和每个单个 ASV 的比例，通过估计绝对丰度的变化计算出基于单个扩增子序列变体（ASV）的生长率。不同实验中获得的增长率趋势与其他基于总细胞数、CARD-FISH 子群落细胞数或元基因组-OTU 的估计值一致。我们的计算揭示了一个广泛的生长率范围[0.3-10 d-1]，即使在密切相关的 ASV 中也存在显著的差异。同样，生长限制因素对单个 ASV 的影响在一年中也会发生变化。在营养限制和病毒压力较小的处理中，冬春两季以及全年都有大量反应灵敏的 ASV。反应最灵敏的 ASV 在原位群落中很少见，它们组成了一个庞大的类群，有可能对环境变化做出快速反应。从根本上说，我们的研究结果突显了所观察到的生长率范围缺乏系统发生学上的一致性，以及对各种限制因素的不同反应，即使是对亲缘关系很近的类群也是如此。
{"title":"Growth rates of marine prokaryotes are extremely diverse, even among closely related taxa","authors":"Ona Deulofeu-Capo, Marta Sebastián, Adrià Auladell, Clara Cardelús, I. Ferrera, Olga Sánchez, J. Gasol","doi":"10.1093/ismeco/ycae066","DOIUrl":"https://doi.org/10.1093/ismeco/ycae066","url":null,"abstract":"\u0000 Marine prokaryotes play crucial roles in ocean biogeochemical cycles, being their contribution strongly influenced by their growth rates. Hence, elucidating the variability and phylogenetic imprint of marine prokaryotes' growth rates are crucial for better determining the role of individual taxa in biogeochemical cycles. Here, we estimated prokaryotic growth rates at high phylogenetic resolution in manipulation experiments using water from the northwestern Mediterranean Sea. Experiments were run in the four seasons with different treatments that reduced growth limiting factors: predators, nutrient availability, viruses, and light. Single-amplicon sequence variants (ASVs)-based growth rates were calculated from changes in estimated absolute abundances using total prokaryotic abundance and the proportion of each individual ASV. The trends obtained for growth rates in the different experiments were consistent with other estimates based on total cell-counts, CARD-FISH subcommunity cell-counts or metagenomic-OTUs. Our calculations unveil a broad range of growth rates [0.3-10 d-1] with significant variability even within closely related ASVs. Likewise, the impact of growth limiting factors changed over the year for individual ASVs. High numbers of responsive ASVs were shared between winter and spring seasons, as well as throughout the year in the treatments with reduced nutrient limitation and viral pressure. The most responsive ASVs were rare in the in situ communities, comprising a large pool of taxa with the potential to rapidly respond to environmental changes. Essentially, our results highlight the lack of phylogenetic coherence in the range of growth rates observed, and differential responses to the various limiting factors, even for closely related taxa.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141017682","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}
Single-stranded (ss) DNA viruses are ubiquitous and constitute some of the most diverse entities on Earth. Most studies have focused on ssDNA viruses from terrestrial environments resulting in a significant deficit in benthic ecosystems including aphotic zones of the South Indian Ocean (SIO). Here, we assess the diversity and phylogeny of ssDNA in deep waters of the SIO using a combination of established viral taxonomy tools and a Hidden Markov Model based approach. Replication initiator protein-associated (Rep) phylogenetic reconstruction and sequence similarity networks (SSN) were used to show that the SIO hosts divergent and as yet unknown circular Rep-encoding ssDNA (CRESS-DNA) viruses. Several sequences appear to represent entirely novel families, expanding the repertoire of known ssDNA viruses. Results suggest that a small proportion of these viruses may be circular genetic elements, which may strongly influence the diversity of both eukaryotes and prokaryotes in the SIO. Taken together, our data show that the SIO harbours a diverse assortment of previously unknown ssDNA viruses. Due to their potential to infect a variety of hosts, these viruses may be crucial for marine nutrient recycling through their influence of the biological carbon pump.
{"title":"Phylogenomic analysis expands the known repertoire of single-stranded DNA viruses in benthic zones of the South Indian Ocean","authors":"Oliver Bezuidt, T. Makhalanyane","doi":"10.1093/ismeco/ycae065","DOIUrl":"https://doi.org/10.1093/ismeco/ycae065","url":null,"abstract":"\u0000 Single-stranded (ss) DNA viruses are ubiquitous and constitute some of the most diverse entities on Earth. Most studies have focused on ssDNA viruses from terrestrial environments resulting in a significant deficit in benthic ecosystems including aphotic zones of the South Indian Ocean (SIO). Here, we assess the diversity and phylogeny of ssDNA in deep waters of the SIO using a combination of established viral taxonomy tools and a Hidden Markov Model based approach. Replication initiator protein-associated (Rep) phylogenetic reconstruction and sequence similarity networks (SSN) were used to show that the SIO hosts divergent and as yet unknown circular Rep-encoding ssDNA (CRESS-DNA) viruses. Several sequences appear to represent entirely novel families, expanding the repertoire of known ssDNA viruses. Results suggest that a small proportion of these viruses may be circular genetic elements, which may strongly influence the diversity of both eukaryotes and prokaryotes in the SIO. Taken together, our data show that the SIO harbours a diverse assortment of previously unknown ssDNA viruses. Due to their potential to infect a variety of hosts, these viruses may be crucial for marine nutrient recycling through their influence of the biological carbon pump.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141033610","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 : 2024-05-01eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae063
Tong Wang, Leyuan Li, Daniel Figeys, Yang-Yu Liu
The genome of a microorganism encodes its potential functions that can be implemented through expressed proteins. It remains elusive how a protein's selective expression depends on its metabolic essentiality to microbial growth or its ability to claim resources as ecological niches. To reveal a protein's metabolic or ecological role, we developed a computational pipeline, which pairs metagenomics and metaproteomics data to quantify each protein's gene-level and protein-level functional redundancy simultaneously. We first illustrated the idea behind the pipeline using simulated data of a consumer-resource model. We then validated it using real data from human and mouse gut microbiome samples. In particular, we analyzed ABC-type transporters and ribosomal proteins, confirming that the metabolic and ecological roles predicted by our pipeline agree well with prior knowledge. Finally, we performed in vitro cultures of a human gut microbiome sample and investigated how oversupplying various sugars involved in ecological niches influences the community structure and protein abundance. The presented results demonstrate the performance of our pipeline in identifying proteins' metabolic and ecological roles, as well as its potential to help us design nutrient interventions to modulate the human microbiome.
{"title":"Pairing metagenomics and metaproteomics to characterize ecological niches and metabolic essentiality of gut microbiomes.","authors":"Tong Wang, Leyuan Li, Daniel Figeys, Yang-Yu Liu","doi":"10.1093/ismeco/ycae063","DOIUrl":"10.1093/ismeco/ycae063","url":null,"abstract":"<p><p>The genome of a microorganism encodes its potential functions that can be implemented through expressed proteins. It remains elusive how a protein's selective expression depends on its metabolic essentiality to microbial growth or its ability to claim resources as ecological niches. To reveal a protein's metabolic or ecological role, we developed a computational pipeline, which pairs metagenomics and metaproteomics data to quantify each protein's gene-level and protein-level functional redundancy simultaneously. We first illustrated the idea behind the pipeline using simulated data of a consumer-resource model. We then validated it using real data from human and mouse gut microbiome samples. In particular, we analyzed ABC-type transporters and ribosomal proteins, confirming that the metabolic and ecological roles predicted by our pipeline agree well with prior knowledge. Finally, we performed <i>in vitro</i> cultures of a human gut microbiome sample and investigated how oversupplying various sugars involved in ecological niches influences the community structure and protein abundance. The presented results demonstrate the performance of our pipeline in identifying proteins' metabolic and ecological roles, as well as its potential to help us design nutrient interventions to modulate the human microbiome.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11131966/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141163079","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}
Xing Liu, Yin Ye, Naiming Yang, Chen Cheng, Christopher Rensing, Chao Jin, K. Nealson, Shungui Zhou
Extracellular electron transfer (EET) of microorganisms is a major driver of the microbial growth and metabolism, including reactions involved in the cycling of C, N, and Fe in anaerobic environments such as soils and sediments. Understanding the mechanisms of EET, as well as knowing which organisms are EET-capable (or can become so) is fundamental to electromicrobiology and geomicrobiology. In general, Gram-positive bacteria very seldomly perform EET due to their thick non-conductive cell wall. Here, we report that a Gram-positive Clostridium intestinale (C.i) attained EET-capability for ethanol metabolism only after forming chimera with electroactive Geobacter sulfurreducens (G.s). Mechanism analyses demonstrated that the EET was possible after the cell fusion of the two species was achieved. Under these conditions, the ethanol metabolism pathway of C.i was integrated by the EET pathway of G.s, by which achieved the oxidation of ethanol for the subsequent reduction of extracellular electron acceptors in the coculture. Our study displays a new approach to perform EET for Gram-positive bacteria via recruiting the EET pathway of an electroactive bacterium, which suggests a previously unanticipated prevalence of EET in the microbial world. These findings also provide new perspectives to understand the energetic coupling between bacterial species and the ecology of interspecies mutualisms.
{"title":"Nonelectroactive clostridium obtains extracellular electron transfer-capability after forming chimera with Geobacter","authors":"Xing Liu, Yin Ye, Naiming Yang, Chen Cheng, Christopher Rensing, Chao Jin, K. Nealson, Shungui Zhou","doi":"10.1093/ismeco/ycae058","DOIUrl":"https://doi.org/10.1093/ismeco/ycae058","url":null,"abstract":"\u0000 Extracellular electron transfer (EET) of microorganisms is a major driver of the microbial growth and metabolism, including reactions involved in the cycling of C, N, and Fe in anaerobic environments such as soils and sediments. Understanding the mechanisms of EET, as well as knowing which organisms are EET-capable (or can become so) is fundamental to electromicrobiology and geomicrobiology. In general, Gram-positive bacteria very seldomly perform EET due to their thick non-conductive cell wall. Here, we report that a Gram-positive Clostridium intestinale (C.i) attained EET-capability for ethanol metabolism only after forming chimera with electroactive Geobacter sulfurreducens (G.s). Mechanism analyses demonstrated that the EET was possible after the cell fusion of the two species was achieved. Under these conditions, the ethanol metabolism pathway of C.i was integrated by the EET pathway of G.s, by which achieved the oxidation of ethanol for the subsequent reduction of extracellular electron acceptors in the coculture. Our study displays a new approach to perform EET for Gram-positive bacteria via recruiting the EET pathway of an electroactive bacterium, which suggests a previously unanticipated prevalence of EET in the microbial world. These findings also provide new perspectives to understand the energetic coupling between bacterial species and the ecology of interspecies mutualisms.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140655463","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}
Javier Tamayo-Leiva, J. Alcorta, Felipe Sepúlveda, Sebastián Fuentes-Alburquenque, José Ignacio Arroyo, J. González-Pastor, Beatríz Díez
Mobile genetic elements (MGEs), collectively referred to as the “mobilome”, can have a significant impact on the fitness of microbial communities and therefore on ecological processes. Marine MGEs have mainly been associated with wide geographical and phylogenetic dispersal of adaptative traits. However, whether the structure of this mobilome exhibits deterministic patterns in the natural community is still an open question. The aim of this study was to characterize the structure of the conjugative mobilome in the ocean surface bacterioplankton by searching the publicly available marine metagenomes from the TARA Oceans survey, together with molecular markers, such as relaxases and type IV coupling proteins of the type IV secretion system (T4SS). The T4SS machinery was retrieved in more abundance than relaxases in the surface marine bacterioplankton. Moreover, among the identified MGEs, mobilizable elements were the most abundant, outnumbering self-conjugative sequences. Detection of a high number of incomplete T4SSs provides insight into possible strategies related to trans-acting activity between MGEs, and accessory functions of the T4SS (e.g., protein secretion), allowing the host to maintain a lower metabolic burden in the highly dynamic marine system. Additionally, the results demonstrate a wide geographical dispersion of MGEs throughout oceanic regions, while the Southern Ocean appears segregated from other regions. The marine mobilome also showed a high similarity of functions present in known plasmid databases. Moreover, cargo genes were mostly related to DNA processing, but scarcely associated with antibiotic resistance. Finally, within the MGEs, integrative and conjugative elements showed wider marine geographic dispersion than plasmids.
移动遗传因子（MGEs）统称为 "移动组"，可对微生物群落的适宜性产生重大影响，进而影响生态过程。海洋移动遗传因子主要与适应性特征的广泛地理和系统发育散布有关。然而，这种移动组的结构在自然群落中是否表现出确定性模式仍是一个悬而未决的问题。本研究的目的是通过搜索 TARA 海洋调查中公开的海洋元基因组，并结合分子标记（如松弛酶和 IV 型分泌系统（T4SS）的 IV 型偶联蛋白），描述海洋表层浮游细菌共轭移动组的结构特征。在表层海洋浮游细菌中，T4SS 机制的检索量高于弛缓酶。此外，在已鉴定的 MGEs 中，可移动元素的数量最多，超过了自结合序列。大量不完整 T4SS 的发现使人们深入了解了与 MGE 之间的跨作用活性有关的可能策略，以及 T4SS 的辅助功能（如蛋白质分泌），从而使宿主在高度动态的海洋系统中保持较低的代谢负担。此外，研究结果表明，MGEs 在整个大洋区域的地理分布很广，而南大洋似乎与其他区域有所隔离。海洋移动基因组还显示出与已知质粒数据库中存在的功能高度相似。此外，货物基因大多与 DNA 处理有关，但很少与抗生素抗性相关。最后，在移动基因组中，整合基因和共轭基因显示出比质粒更广泛的海洋地理分布。
{"title":"Structure and dispersion of the conjugative mobilome in surface ocean bacterioplankton","authors":"Javier Tamayo-Leiva, J. Alcorta, Felipe Sepúlveda, Sebastián Fuentes-Alburquenque, José Ignacio Arroyo, J. González-Pastor, Beatríz Díez","doi":"10.1093/ismeco/ycae059","DOIUrl":"https://doi.org/10.1093/ismeco/ycae059","url":null,"abstract":"\u0000 Mobile genetic elements (MGEs), collectively referred to as the “mobilome”, can have a significant impact on the fitness of microbial communities and therefore on ecological processes. Marine MGEs have mainly been associated with wide geographical and phylogenetic dispersal of adaptative traits. However, whether the structure of this mobilome exhibits deterministic patterns in the natural community is still an open question. The aim of this study was to characterize the structure of the conjugative mobilome in the ocean surface bacterioplankton by searching the publicly available marine metagenomes from the TARA Oceans survey, together with molecular markers, such as relaxases and type IV coupling proteins of the type IV secretion system (T4SS). The T4SS machinery was retrieved in more abundance than relaxases in the surface marine bacterioplankton. Moreover, among the identified MGEs, mobilizable elements were the most abundant, outnumbering self-conjugative sequences. Detection of a high number of incomplete T4SSs provides insight into possible strategies related to trans-acting activity between MGEs, and accessory functions of the T4SS (e.g., protein secretion), allowing the host to maintain a lower metabolic burden in the highly dynamic marine system. Additionally, the results demonstrate a wide geographical dispersion of MGEs throughout oceanic regions, while the Southern Ocean appears segregated from other regions. The marine mobilome also showed a high similarity of functions present in known plasmid databases. Moreover, cargo genes were mostly related to DNA processing, but scarcely associated with antibiotic resistance. Finally, within the MGEs, integrative and conjugative elements showed wider marine geographic dispersion than plasmids.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140653447","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}
Ö. C. Onarman Umu, L. Mydland, Chi Chen, Marta Perez de Nanclares, G. Shurson, P. Urriola, Henning Sørum, M. Øverland
Diet-mediated host-microbiota interplay is a key factor in optimizing the gut function and overall health of the host. Gaining insight into the biological mechanisms behind this relationship is fundamental to finding sustainable, environment-friendly feed solutions in livestock production systems. Here, we apply a multi-omics integration approach to elucidate sustainable diet-associated host-gut microbiota interactions in pigs and we demonstrate novel and biologically relevant host-microbe associations in the gut, driven by a rapeseed meal-based feed (RSF). Interestingly, RSF-diet promoted the abundance of segmented filamentous bacteria (SFB) Candidatus Arthromitus that was associated with the maintenance of mucosal immunity in the ileum of pigs. In the colon, RSF diet affected host mRNA splicing functions, which may result in different host gene products, through host-microbiota associations, particularly with the Faecalibacterium population, and through the interaction of dietary components such as sinapic acid with the host cells. Moreover, telomere maintenance and organization functions that may determine the overall health of the host were upregulated and notably associated with Subdoligranulum population in the colon of RSF diet-fed pigs. This integrative multi-omics approach provides more insight into the diet-microbiota-host axis, and a better understanding of mechanisms and opportunities to find new strategies for modulating host health and potentially improving caloric and nutritional efficiency in animal production.
{"title":"Integrated multi-omics approach reveals novel associations in the rapeseed diet-microbiota-host axis in pigs","authors":"Ö. C. Onarman Umu, L. Mydland, Chi Chen, Marta Perez de Nanclares, G. Shurson, P. Urriola, Henning Sørum, M. Øverland","doi":"10.1093/ismeco/ycae061","DOIUrl":"https://doi.org/10.1093/ismeco/ycae061","url":null,"abstract":"\u0000 Diet-mediated host-microbiota interplay is a key factor in optimizing the gut function and overall health of the host. Gaining insight into the biological mechanisms behind this relationship is fundamental to finding sustainable, environment-friendly feed solutions in livestock production systems. Here, we apply a multi-omics integration approach to elucidate sustainable diet-associated host-gut microbiota interactions in pigs and we demonstrate novel and biologically relevant host-microbe associations in the gut, driven by a rapeseed meal-based feed (RSF). Interestingly, RSF-diet promoted the abundance of segmented filamentous bacteria (SFB) Candidatus Arthromitus that was associated with the maintenance of mucosal immunity in the ileum of pigs. In the colon, RSF diet affected host mRNA splicing functions, which may result in different host gene products, through host-microbiota associations, particularly with the Faecalibacterium population, and through the interaction of dietary components such as sinapic acid with the host cells. Moreover, telomere maintenance and organization functions that may determine the overall health of the host were upregulated and notably associated with Subdoligranulum population in the colon of RSF diet-fed pigs. This integrative multi-omics approach provides more insight into the diet-microbiota-host axis, and a better understanding of mechanisms and opportunities to find new strategies for modulating host health and potentially improving caloric and nutritional efficiency in animal production.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140670148","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}
Rui Zhao, Irene H Zhang, A. Jayakumar, B. Ward, A. R. Babbin
Anammox bacteria inhabiting oxygen deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss in the global ocean. However, many basic questions regarding the diversity, broad metabolisms, origin, and adaptive mechanisms of ODZ anammox bacteria remain unaddressed. Here we report two novel metagenome-assembled genomes of anammox bacteria affiliated with the Scalindua genus, which represent most, if not all, of the anammox bacteria in the global ODZs. Metagenomic read recruiting and comparison with historical data show that they are ubiquitously present in all three major ODZs. Beyond the core anammox metabolism, both organisms contain cyanase and the more dominant one encodes a urease, indicating most ODZ anammox bacteria can utilize cyanate and urea in addition to ammonium. Molecular clock analysis suggests that the evolutionary radiation of these bacteria into ODZs occurred no earlier than 310 million years ago, about one billion years after the emergence of the earliest modern-type ODZs. Different strains of the ODZ Scalindua species are also found in benthic sediments, and the first ODZ Scalindua likely derived from the benthos. Compared to benthic strains of the same clade, ODZ Scalindua uniquely encode genes for urea utilization but lost genes related to growth arrest, flagellum synthesis, and chemotaxis, presumably for adaptation to thrive in the global ODZ waters. Our findings expand the known metabolism and evolutionary history of the bacteria controlling the global nitrogen budget.
{"title":"Age, metabolisms, and potential origin of dominant anammox bacteria in the global oxygen deficient zones","authors":"Rui Zhao, Irene H Zhang, A. Jayakumar, B. Ward, A. R. Babbin","doi":"10.1093/ismeco/ycae060","DOIUrl":"https://doi.org/10.1093/ismeco/ycae060","url":null,"abstract":"\u0000 Anammox bacteria inhabiting oxygen deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss in the global ocean. However, many basic questions regarding the diversity, broad metabolisms, origin, and adaptive mechanisms of ODZ anammox bacteria remain unaddressed. Here we report two novel metagenome-assembled genomes of anammox bacteria affiliated with the Scalindua genus, which represent most, if not all, of the anammox bacteria in the global ODZs. Metagenomic read recruiting and comparison with historical data show that they are ubiquitously present in all three major ODZs. Beyond the core anammox metabolism, both organisms contain cyanase and the more dominant one encodes a urease, indicating most ODZ anammox bacteria can utilize cyanate and urea in addition to ammonium. Molecular clock analysis suggests that the evolutionary radiation of these bacteria into ODZs occurred no earlier than 310 million years ago, about one billion years after the emergence of the earliest modern-type ODZs. Different strains of the ODZ Scalindua species are also found in benthic sediments, and the first ODZ Scalindua likely derived from the benthos. Compared to benthic strains of the same clade, ODZ Scalindua uniquely encode genes for urea utilization but lost genes related to growth arrest, flagellum synthesis, and chemotaxis, presumably for adaptation to thrive in the global ODZ waters. Our findings expand the known metabolism and evolutionary history of the bacteria controlling the global nitrogen budget.","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140677229","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}
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