The ISME JournalPub Date : 2025-04-04DOI: 10.1093/ismejo/wraf058
Yue Huang, Xuemei Mao, Xiawan Zheng, Yuxiang Zhao, Dou Wang, Mengying Wang, Yiqiang Chen, Lei Liu, Yulin Wang, Martin F Polz, Tong Zhang
{"title":"Longitudinal dynamics and cross-domain interactions of eukaryotic populations in wastewater treatment plants","authors":"Yue Huang, Xuemei Mao, Xiawan Zheng, Yuxiang Zhao, Dou Wang, Mengying Wang, Yiqiang Chen, Lei Liu, Yulin Wang, Martin F Polz, Tong Zhang","doi":"10.1093/ismejo/wraf058","DOIUrl":"https://doi.org/10.1093/ismejo/wraf058","url":null,"abstract":"Activated sludge is a large reservoir of novel microorganisms and microbial genetic diversity. While much attention has been given to the profile and functions of prokaryotes, the eukaryotic diversity remains largely unexplored. In this study, we analyzed longitudinal activated sludge samples spanning 13 years from the largest secondary wastewater treatment plants in Hong Kong, unveiling a wealth of eukaryotic taxa and 681 856 non-redundant protein-coding genes, the majority (416044) of which appeared novel. Ciliophora was the most dominant phylum with a significant increase after a transient intervention (bleaching event). Our metagenomic analysis reveals close linkage and covariation of eukaryotes, prokaryotes, and prokaryotic viruses (phages), indicating common responses to environmental changes such as transient intervention and intermittent fluctuations. Furthermore, high-resolution cross-domain relationships were interpreted by S-map, demonstrating a predatory role of Arthropoda, Ascomycota, Mucoromycota, and Rotifera. This high-resolution profile of microbial dynamics expands our knowledge on yet-to-be-cultured populations and their cross-domain interactions and highlights the ecological importance of eukaryotes in the activated sludge ecosystem.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"108 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143782690","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}
The ISME JournalPub Date : 2025-04-04DOI: 10.1093/ismejo/wraf063
Charles Bernard, Yannick Labreuche, Carine Diarra, Pauline Daszkowski, Karine Cahier, David Goudenège, Martin G Lamarche, Gregory B Whitfield, Manon Lang, Jeffrey Valencia, Justine Groseille, Damien Piel, Yan-Jiun Lee, Peter Weigele, Yves V Brun, Eduardo P C Rocha, Frédérique Le Roux
{"title":"Adaptive genomic plasticity in large-genome, broad-host-range vibrio phages","authors":"Charles Bernard, Yannick Labreuche, Carine Diarra, Pauline Daszkowski, Karine Cahier, David Goudenège, Martin G Lamarche, Gregory B Whitfield, Manon Lang, Jeffrey Valencia, Justine Groseille, Damien Piel, Yan-Jiun Lee, Peter Weigele, Yves V Brun, Eduardo P C Rocha, Frédérique Le Roux","doi":"10.1093/ismejo/wraf063","DOIUrl":"https://doi.org/10.1093/ismejo/wraf063","url":null,"abstract":"The host range of a bacteriophage—the diversity of hosts it can infect—is central to understanding phage ecology and applications. Whereas most well-characterized phages have narrow host ranges, broad-host-range phages represent an intriguing component of marine ecosystems. The genetic and evolutionary mechanisms driving their generalism remain poorly understood. In this study, we analyzed Schizotequatroviruses and their Vibrio crassostreae hosts, collected from an oyster farm. Schizotequatroviruses exhibit broad host ranges, large genomes (~252 kbp) encoding 26 tRNAs, and conserved genomic organization interspersed with recombination hotspots. These recombination events, particularly in regions encoding receptor-binding proteins and antidefense systems, highlight their adaptability to host resistance. Some lineages demonstrated the ability of receptor-switching between OmpK and LamB. Despite their broad host range, Schizotequatroviruses were rare in the environment. Their scarcity could not be attributed to burst size, which was comparable to other phages in vitro, but may result from ecological constraints or fitness trade-offs, such as their preference for targeting generalist vibrios in seawater rather than the patho-phylotypes selected in oyster farms. Our findings clarify the genetic and ecological variables shaping Schizotequatrovirus generalism and provide a foundation for future phage applications in aquaculture and beyond.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"73 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143782689","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}
The ISME JournalPub Date : 2025-03-23DOI: 10.1093/ismejo/wraf057
Marcos Y Voutsinos, Jillian F Banfield, Harry-Luke O McClelland
{"title":"Extensive and diverse lanthanide-dependent metabolism in the ocean","authors":"Marcos Y Voutsinos, Jillian F Banfield, Harry-Luke O McClelland","doi":"10.1093/ismejo/wraf057","DOIUrl":"https://doi.org/10.1093/ismejo/wraf057","url":null,"abstract":"To date, the only known Lanthanide (Ln)-dependent enzymes are pyrroloquinoline quinone-dependent alcohol dehydrogenases. When compared to their Ca dependent counterparts, there is an emerging picture that Ln-dependent versions of these enzymes are generally more efficient, are preferentially upregulated in the presence of Ln when there is functional redundancy, and may even be evolutionarily older. Ln-utilising microbes have furthermore evolved diverse means of solubilizing and acquiring Ln, enabling them to utilise Ln even at trace concentrations. The ocean is the largest dissolved organic carbon pool on Earth, yet the diversity and prevalence of Ln-dependent carbon metabolisms in the ocean is unknown. Here we show that Ln-utilising methanol-, ethanol- and putative sorbose- and glucose-dehydrogenase genes are ubiquitous in the ocean and are highly transcribed, despite extremely low concentrations of Ln in seawater. These enzymes occur in the genomes of 20% of marine microbes, with several individual organisms hosting dozens of unique Ln-utilising enzymes. We found that active microbial methanol oxidation in the ocean is almost entirely Ln-dependent. The widespread biological utility of Ln may help to explain the nutrient-like vertical concentration profiles of these elements in ocean waters and may exert an influence on rare earth element concentration patterns. Microbial Ln-utilisation is a poorly understood component of marine rare earth element biogeochemistry, with potentially important implications for the carbon cycle. The ocean microbiome will be a rich resource for future research into biologically inspired solutions to lanthanide extraction and purification.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"56 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143675167","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}
The ISME JournalPub Date : 2025-03-23DOI: 10.1093/ismejo/wraf045
Qing Wang, Changzhen Liu, Yan Sun, Xuli Li, Weimin Gu, Na Wang, Shaojing Sun, Yi Luo
{"title":"Dietary intake of enrofloxacin promotes the spread of antibiotic resistance from food to simulated human gut","authors":"Qing Wang, Changzhen Liu, Yan Sun, Xuli Li, Weimin Gu, Na Wang, Shaojing Sun, Yi Luo","doi":"10.1093/ismejo/wraf045","DOIUrl":"https://doi.org/10.1093/ismejo/wraf045","url":null,"abstract":"Antibiotic residues are commonly found in food. The effect of dietary exposure to veterinary antibiotics on the transmission of antibiotic resistant bacteria and antibiotic resistance genes from food to humans is unknown. We found that dietary exposure to enrofloxacin reduced microbial diversity, interactions and the immune responses, weakened the colonization resistance of the resident microbiota, and promoted the colonization of exogenous Escherichia coli K-12 MG1655 in the simulated human intestine both in vitro and in vivo experiments in mice. In addition to the growth advantages for potential most likely bacterial hosts of ARGs under enrofloxacin exposure, the dietary exposure to enrofloxacin promoted horizontal transfer of resistance plasmids and altered the simulated human gut antibiotic resistome in a time-dependent manner. Collectively, these findings demonstrated that dietary intake of enrofloxacin promoted the colonization of E. coli K-12 MG1655 in the simulated human intestine and the horizontal transfer of antibiotic resistance genes, highlighting the risk of antibiotic resistance transmission from food to humans mediated by dietary exposure to veterinary antibiotics.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"27 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143675172","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}
The ISME JournalPub Date : 2025-03-18DOI: 10.1093/ismejo/wraf054
Marcela Tabares, Kazem Kashefi, Gemma Reguera
{"title":"Adaptive responses of Trichlorobacter lovleyi to nitrite detoxification reveal overlooked contributions of Geobacterales to nitrate ammonification","authors":"Marcela Tabares, Kazem Kashefi, Gemma Reguera","doi":"10.1093/ismejo/wraf054","DOIUrl":"https://doi.org/10.1093/ismejo/wraf054","url":null,"abstract":"Poorly understood microorganisms “short-circuit” the nitrogen cycle via the dissimilatory nitrate reduction to ammonium to retain the element in agricultural lands and stimulate crop productivity. The prevalence of Geobacterales closely related to Trichlorobacter lovleyi in nitrate ammonification hotspots motivated us to investigate adaptive responses contributing to ammonification rates in the laboratory type strain T. lovleyi SZ. Here we describe the identification of tightly regulated pathways for efficient nitrate foraging and respiration with acetate, an important intermediate of organic matter degradation that Geobacterales efficiently assimilate and oxidize. Challenging the established dogma that high carbon/nitrate ratios stimulate the reduction of nitrate to ammonium, T. lovleyi doubled rapidly across a wide range of ratios provided nitrate concentrations were low enough to prevent the accumulation of the toxic nitrite intermediate. Yet, excess electrons during hydrogenotrophic growth alleviated nitrite toxicity and stimulated the reduction of nitrate to ammonium even under conditions of severe acetate limitation. These findings underscore the importance of nitrite toxicity in the ammonification of nitrate by Geobacterales and provide much needed mechanistic understanding of microbial adaptations contributing to soil nitrogen conservation. This information is critical to enhance the predictive value of genomic-based traits in environmental surveys and to guide strategies for sustainable management of nitrogen fertilization as well as mitigation of green-house emissions and agrochemical leaching from agricultural lands.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"43 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143653371","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}
The ISME JournalPub Date : 2025-03-17DOI: 10.1093/ismejo/wraf051
Qifeng Zhang, Jie Li, Jinhua Tuo, Shengnan Liu, Yang Liu, Peng Liu, Lin Ye, Xu-Xiang Zhang
{"title":"Long-term metagenomic insights into the roles of antiviral defense systems in stabilizing activated sludge bacterial communities","authors":"Qifeng Zhang, Jie Li, Jinhua Tuo, Shengnan Liu, Yang Liu, Peng Liu, Lin Ye, Xu-Xiang Zhang","doi":"10.1093/ismejo/wraf051","DOIUrl":"https://doi.org/10.1093/ismejo/wraf051","url":null,"abstract":"Bacteria have evolved various antiviral defense systems to protect themselves, but how defense systems respond to the variation of bacteriophages in complex bacterial communities and whether defense systems function effectively in maintaining the stability of bacterial community structure and function remain unknown. Here, we conducted a long-term metagenomic investigation on the composition of bacterial and phage communities of monthly collected activated sludge samples from two full-scale wastewater treatment plants over six years and found that defense systems were widespread in activated sludge, with 91.1% of metagenome-assembled genomes having more than one complete defense system. The stability of the bacterial community was maintained under the fluctuations of the phage community, and defense system abundance and phage abundance were strongly positively correlated; there was a 0–3-month time lag in the responses of defense systems to phage fluctuations. The rapid turnover of CRISPR spacer repertoires further highlighted the dynamic nature of bacterial defense mechanisms. A pan-immunity phenomenon was also observed, with nearly identical metagenome-assembled genomes showing significant differences in defense system composition, which contributed to community stability at the species level. This study provides novel insights into the complexity of phage–bacteria interactions in complex bacterial communities, and reveals the key roles of defense systems in stabilizing bacterial community structure and function.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"25 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143641135","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}
The ISME JournalPub Date : 2025-03-16DOI: 10.1093/ismejo/wraf053
Nicola Fantom, Robin A Dawson, Edina Prondvai, Philippe Constant, Gary M King, Hendrik Schäfer, Marcela Hernández
{"title":"Metabolism of CO and H2 by pioneer bacteria in volcanic soils and the phyllosphere","authors":"Nicola Fantom, Robin A Dawson, Edina Prondvai, Philippe Constant, Gary M King, Hendrik Schäfer, Marcela Hernández","doi":"10.1093/ismejo/wraf053","DOIUrl":"https://doi.org/10.1093/ismejo/wraf053","url":null,"abstract":"Trace gas degradation is a widespread metabolic adaptation in microbial communities, driving chemosynthesis and providing auxiliary energy that enhances persistence during nutrient starvation. In particular, carbon monoxide and hydrogen degradation can be of crucial importance for pioneering microbial communities colonising new, oligotrophic environmental niches, such as fresh volcanic deposits or the aerial interface of the phyllosphere. After volcanic eruptions, trace gas metabolism helps pioneer colonisers to initiate soil formation in ash deposits and on recently solidified lava, a vital ecosystem service. Similarly, in the phyllosphere, bacteria colonising newly emerging leaves and shoots, and/or persisting on the oligotrophic surface of plants, also benefit from trace gas oxidation and, given the global size of this habitat, likely constitute a significant sink for these trace gases affecting atmospheric chemistry. Herein, we review the current state of knowledge surrounding microbial oxidation of carbon monoxide and hydrogen and discuss how this may contribute to niche colonisation in oligotrophic ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"61 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143635586","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}
The ISME JournalPub Date : 2025-03-13DOI: 10.1093/ismejo/wraf050
Johannes Werner, Hartmut Arndt
{"title":"Spatio-temporal pattern formation of living organisms at the edge of chaos","authors":"Johannes Werner, Hartmut Arndt","doi":"10.1093/ismejo/wraf050","DOIUrl":"https://doi.org/10.1093/ismejo/wraf050","url":null,"abstract":"Understanding spatio-temporal dynamics is essential for predicting how populations fluctuate over time and space. Theoretical models have highlighted the ecological complexity of spatio-temporal dynamics, which can lead to the emergence of complex patterns, including nonlinear dynamics and chaotic behavior, important mechanisms for maintaining of biodiversity. However, these dynamics are difficult to observe experimentally due to a lack of temporal and spatial resolution. Here we show that even a single-species system exhibits complex spatio-temporal patterns without external forcing where order and chaos coexist (edge of chaos). Automated analyses of experimental dynamics of cells of a ciliate on a microfluidic chip environment with 50 interconnected patches documented pattern formation, including chaos-like dynamics, using several analytical methods. Different initial conditions caused changes in patterns, revealing the complexity and principal unpredictability of self-organized pattern formation. A model containing the stochastic fluctuations of the experiment verified the deterministic nature of patterns. The results show the intrinsic complexity of ecological systems, challenging predictions in nature conservation. Our results bridge the gap between theoretical models and experimental observations, offering new insights into the fundamental nature of living systems and their spatio-temporal organization.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"22 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143618427","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}
The ISME JournalPub Date : 2025-03-09DOI: 10.1093/ismejo/wraf044
Michael Opoku Adomako, Jing Wu, Fei-Hai Yu
{"title":"Ecological and evolutionary responses of earthworm holobionts to environmental changes","authors":"Michael Opoku Adomako, Jing Wu, Fei-Hai Yu","doi":"10.1093/ismejo/wraf044","DOIUrl":"https://doi.org/10.1093/ismejo/wraf044","url":null,"abstract":"Global environmental change substantially affects soil detritivores, including earthworms, impacting host-microbiota interactions and altering key soil biogeochemical processes such as litter decomposition. As microbial communities are inherently capable of rapid evolution, responses of earthworms and associated microbiota (i.e., earthworm holobionts) to global environmental change may likely involve the interplay of ecological and evolutionary processes and feedbacks. Although species-level responses of earthworms to global environmental change are well-studied, the potential ecological and evolutionary responses of earthworm holobionts to environmental change remain unexplored. Here, we provide a conceptual framework to elaborate on the complex network of earthworm host−microbiota interactions that modify their traits in response to global environmental change, jointly shaping their ecology and evolution. Based on literature, we synthesize evidence of global environmental change impacts on earthworm host-microbiota and discuss evidence of their ecological and evolutionary responses to environmental change. Lastly, we highlight the agro- and eco-system level consequences of environmental change-mediated shift in earthworm host-microbiota functions. Soil legacies of environmental change have cascading detrimental impacts on the abundance, diversity, and functional dynamics of earthworm host-microbiota interactions in agriculture and ecosystems. The primary mechanisms driving such responses of earthworm hosts and associated microbial communities to environmental change include altered litter quality and host dietary preferences, competitive interactions and exclusion, habitat homogenization, and a shift in soil physicochemical and biological processes. Therefore, advancing knowledge of the intricate animal-microorganism interactions is crucial for belowground biodiversity management in a changing global environment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"192 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143583057","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}
The ISME JournalPub Date : 2025-03-09DOI: 10.1093/ismejo/wraf046
Aditya Jeevannavar, Javier Florenza, Anna-Maria Divne, Manu Tamminen, Stefan Bertilsson
{"title":"Cellular heterogeneity in metabolism and associated microbiome of a non-model phytoflagellate","authors":"Aditya Jeevannavar, Javier Florenza, Anna-Maria Divne, Manu Tamminen, Stefan Bertilsson","doi":"10.1093/ismejo/wraf046","DOIUrl":"https://doi.org/10.1093/ismejo/wraf046","url":null,"abstract":"Single-cell transcriptomics is a key tool for unravelling metabolism and tissue diversity in model organisms. Its potential for elucidating the ecological roles of microeukaryotes, especially non-model ones, remains largely unexplored. This study employed the Smart-seq2 protocol on Ochromonas triangulata, a microeukaryote lacking a reference genome, showcasing how transcriptional states align with two distinct growth phases: a fast-growing phase and a slow-growing phase. Besides the two expected expression clusters, each corresponding to either growth phase, a third transcriptional state was identified across both growth phases. Metabolic mapping revealed a boost of photosynthetic activity in the fast growth over the slow growth stage, as well as down-regulation trend in pathways associated with ribosome functioning, CO2 fixation, and carbohydrate catabolism characteristic of the third transcriptional state. In addition, carry-over rRNA reads recapitulated the taxonomic identity of the target while revealing distinct bacterial communities, in co-culture with the eukaryote, each associated with distinct transcriptional states. This study underscores single-cell transcriptomics as a powerful tool for characterizing metabolic states in microeukaryotes without a reference genome, offering insights into unknown physiological states and individual-level interactions with different bacterial taxa. This approach holds broad applicability to describe the ecological roles of environmental microeukaryotes, culture-free and reference-free, surpassing alternative methods like metagenomics or metatranscriptomics.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"4 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-03-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143583058","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}