Wilhelm Furnon, Vanessa M. Cowton, Giuditta De Lorenzo, Richard Orton, Vanessa Herder, Diego Cantoni, Georgios Ilia, Diogo Correa Mendonca, Karen Kerr, Jay Allan, Nicole Upfold, Gavin R. Meehan, Siddharth Bakshi, Udeet Ranjan Das, Sergi Molina Arias, Marion McElwee, Sarah Little, Nicola Logan, Kirsty Kwok, Katherine Smollett, Brian J. Willett, Ana Da Silva Filipe, David L. Robertson, Joe Grove, Arvind H. Patel, Massimo Palmarini
{"title":"Phenotypic evolution of SARS-CoV-2 spike during the COVID-19 pandemic","authors":"Wilhelm Furnon, Vanessa M. Cowton, Giuditta De Lorenzo, Richard Orton, Vanessa Herder, Diego Cantoni, Georgios Ilia, Diogo Correa Mendonca, Karen Kerr, Jay Allan, Nicole Upfold, Gavin R. Meehan, Siddharth Bakshi, Udeet Ranjan Das, Sergi Molina Arias, Marion McElwee, Sarah Little, Nicola Logan, Kirsty Kwok, Katherine Smollett, Brian J. Willett, Ana Da Silva Filipe, David L. Robertson, Joe Grove, Arvind H. Patel, Massimo Palmarini","doi":"10.1038/s41564-024-01878-5","DOIUrl":"10.1038/s41564-024-01878-5","url":null,"abstract":"SARS-CoV-2 variants are mainly defined by mutations in their spike. It is therefore critical to understand how the evolutionary trajectories of spike affect virus phenotypes. So far, it has been challenging to comprehensively compare the many spikes that emerged during the pandemic in a single experimental platform. Here we generated a panel of recombinant viruses carrying different spike proteins from 27 variants circulating between 2020 and 2024 in the same genomic background. We then assessed several of their phenotypic traits both in vitro and in vivo. We found distinct phenotypic trajectories of spike among and between variants circulating before and after the emergence of Omicron variants. Spike of post-Omicron variants maintained enhanced tropism for the nasal epithelium and large airways but displayed, over time, several phenotypic traits typical of the pre-Omicron variants. Hence, spike with phenotypic features of both pre- and post-Omicron variants may continue to emerge in the future. Systematic comparison of SARS-CoV-2 spike proteins from pre- and post-Omicron variants in cell lines, primary respiratory epithelial cells and Syrian hamsters show distinct phenotypic trajectories in replication kinetics, cell tropism, cell-to-cell fusion, spike processing, cell entry routes and virulence.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"77-93"},"PeriodicalIF":20.5,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01878-5.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142917050","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xueliang Wang, Yi Fang, Wei Liang, Yuhong Cai, Chi Chun Wong, Junlin Wang, Na Wang, Harry Cheuk-Hay Lau, Ying Jiao, Xingyu Zhou, Liufang Ye, Mengmiao Mo, Tao Yang, Miao Fan, Lei Song, Heming Zhou, Qiang Zhao, Eagle Siu-Hong Chu, Meinong Liang, Weixin Liu, Xin Liu, Shuaiyin Zhang, Haitao Shang, Hong Wei, Xiaoxing Li, Lixia Xu, Bing Liao, Joseph J. Y. Sung, Ming Kuang, Jun Yu
{"title":"Gut–liver translocation of pathogen Klebsiella pneumoniae promotes hepatocellular carcinoma in mice","authors":"Xueliang Wang, Yi Fang, Wei Liang, Yuhong Cai, Chi Chun Wong, Junlin Wang, Na Wang, Harry Cheuk-Hay Lau, Ying Jiao, Xingyu Zhou, Liufang Ye, Mengmiao Mo, Tao Yang, Miao Fan, Lei Song, Heming Zhou, Qiang Zhao, Eagle Siu-Hong Chu, Meinong Liang, Weixin Liu, Xin Liu, Shuaiyin Zhang, Haitao Shang, Hong Wei, Xiaoxing Li, Lixia Xu, Bing Liao, Joseph J. Y. Sung, Ming Kuang, Jun Yu","doi":"10.1038/s41564-024-01890-9","DOIUrl":"10.1038/s41564-024-01890-9","url":null,"abstract":"Hepatocellular carcinoma (HCC) is accompanied by an altered gut microbiota but whether the latter contributes to carcinogenesis is unclear. Here we show that faecal microbiota transplantation (FMT) using stool samples from patients with HCC spontaneously initiate liver inflammation, fibrosis and dysplasia in wild-type mice, and accelerate disease progression in a mouse model of HCC. We find that HCC-FMT results in gut barrier injury and translocation of live bacteria to the liver. Metagenomic analyses and bacterial culture of liver tissues reveal enrichment of the gut pathogen Klebsiella pneumoniae in patients with HCC and mice transplanted with the HCC microbiota. Moreover, K. pneumoniae monocolonization recapitulates the effect of HCC-FMT in promoting liver inflammation and hepatocarcinogenesis. Mechanistically, K. pneumoniae surface protein PBP1B interacts with and activates TLR4 on HCC cells, leading to increased cell proliferation and activation of oncogenic signalling. Targeting gut colonization using K. oxytoca or TLR4 inhibition represses K. pneumoniae-induced HCC progression. These findings indicate a role for an altered gut microbiota in hepatocarcinogenesis. Transfer of faecal microbiota from hepatocellular carcinoma patients to mice promotes carcinogenesis via live gut pathogenic Klebsiella pneumoniae translocating to the liver.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"169-184"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01890-9.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911428","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Megan M. Tu, Lindsey A. Carfrae, Kenneth Rachwalski, Shawn French, Denise Catacutan, Rodion Gordzevich, Craig R. MacNair, Melissa E. Speagle, Firas Werah, Jonathan M. Stokes, Eric D. Brown
{"title":"Exploiting the fitness cost of metallo-β-lactamase expression can overcome antibiotic resistance in bacterial pathogens","authors":"Megan M. Tu, Lindsey A. Carfrae, Kenneth Rachwalski, Shawn French, Denise Catacutan, Rodion Gordzevich, Craig R. MacNair, Melissa E. Speagle, Firas Werah, Jonathan M. Stokes, Eric D. Brown","doi":"10.1038/s41564-024-01883-8","DOIUrl":"10.1038/s41564-024-01883-8","url":null,"abstract":"Carbapenems are last-resort antibiotics for treating bacterial infections. The widespread acquisition of metallo-β-lactamases, such as VIM-2, contributes to the emergence of carbapenem-resistant pathogens, and currently, no metallo-β-lactamase inhibitors are available in the clinic. Here we show that bacteria expressing VIM-2 have impaired growth in zinc-deprived environments, including human serum and murine infection models. Using transcriptomic, genomic and chemical probes, we identified molecular pathways critical for VIM-2 expression under zinc limitation. In particular, disruption of envelope stress response pathways reduced the growth of VIM-2-expressing bacteria in vitro and in vivo. Furthermore, we showed that VIM-2 expression disrupts the integrity of the outer membrane, rendering VIM-2-expressing bacteria more susceptible to azithromycin. Using a systemic murine infection model, we showed azithromycin’s therapeutic potential against VIM-2-expressing pathogens. In all, our findings provide a framework to exploit the fitness trade-offs of resistance, potentially accelerating the discovery of additional treatments for infections caused by multidrug-resistant bacteria. Expression of VIM-2 leads to physiological trade-offs for bacterial pathogens that can be exploited to treat infections caused by multidrug-resistant bacteria.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"53-65"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911426","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tiffany Y. Hsu, Etienne Nzabarushimana, Dennis Wong, Chengwei Luo, Robert G. Beiko, Morgan Langille, Curtis Huttenhower, Long H. Nguyen, Eric A. Franzosa
{"title":"Profiling lateral gene transfer events in the human microbiome using WAAFLE","authors":"Tiffany Y. Hsu, Etienne Nzabarushimana, Dennis Wong, Chengwei Luo, Robert G. Beiko, Morgan Langille, Curtis Huttenhower, Long H. Nguyen, Eric A. Franzosa","doi":"10.1038/s41564-024-01881-w","DOIUrl":"10.1038/s41564-024-01881-w","url":null,"abstract":"Lateral gene transfer (LGT), also known as horizontal gene transfer, facilitates genomic diversification in microbial populations. While previous work has surveyed LGT in human-associated microbial isolate genomes, the landscape of LGT arising in personal microbiomes is not well understood, as there are no widely adopted methods to characterize LGT from complex communities. Here we developed, benchmarked and validated a computational algorithm (WAAFLE or Workflow to Annotate Assemblies and Find LGT Events) to profile LGT from assembled metagenomes. WAAFLE prioritizes specificity while maintaining high sensitivity for intergenus LGT. Applying WAAFLE to >2,000 human metagenomes from diverse body sites, we identified >100,000 high-confidence previously uncharacterized LGT (~2 per microbial genome-equivalent). These were enriched for mobile elements, as well as restriction–modification functions associated with the destruction of foreign DNA. LGT frequency was influenced by biogeography, phylogenetic similarity of involved pairs (for example, Fusobacterium periodonticum and F. nucleatum) and donor abundance. These forces manifest as networks in which hub taxa donate unequally with phylogenetic neighbours. Our findings suggest that human microbiome LGT may be more ubiquitous than previously described. Applying WAAFLE to metagenomic data from human samples reveals over 100,000 putative LGTs not currently found in reference genomes, highlighting an underappreciated microbiome phenomenon.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"94-111"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911429","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Grégoire Michoud, Hannes Peter, Susheel Bhanu Busi, Massimo Bourquin, Tyler J. Kohler, Aileen Geers, Leila Ezzat, The Vanishing Glaciers Field Team, Tom J. Battin
{"title":"Mapping the metagenomic diversity of the multi-kingdom glacier-fed stream microbiome","authors":"Grégoire Michoud, Hannes Peter, Susheel Bhanu Busi, Massimo Bourquin, Tyler J. Kohler, Aileen Geers, Leila Ezzat, The Vanishing Glaciers Field Team, Tom J. Battin","doi":"10.1038/s41564-024-01874-9","DOIUrl":"10.1038/s41564-024-01874-9","url":null,"abstract":"Glacier-fed streams (GFS) feature among Earth’s most extreme aquatic ecosystems marked by pronounced oligotrophy and environmental fluctuations. Microorganisms mainly organize in biofilms within them, but how they cope with such conditions is unknown. Here, leveraging 156 metagenomes from the Vanishing Glaciers project obtained from sediment samples in GFS from 9 mountains ranges, we report thousands of metagenome-assembled genomes (MAGs) encompassing prokaryotes, algae, fungi and viruses, that shed light on biotic interactions within glacier-fed stream biofilms. A total of 2,855 bacterial MAGs were characterized by diverse strategies to exploit inorganic and organic energy sources, in part via functional redundancy and mixotrophy. We show that biofilms probably become more complex and switch from chemoautotrophy to heterotrophy as algal biomass increases in GFS owing to glacier shrinkage. Our MAG compendium sheds light on the success of microbial life in GFS and provides a resource for future research on a microbiome potentially impacted by climate change. Thousands of metagenome-assembled genomes from the Vanishing Glaciers project showcase the interactions between prokaryotes, algae, fungi and viruses in glacier-fed stream environments.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"217-230"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911430","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hugo Vaysset, Chance Meers, Jean Cury, Aude Bernheim, Samuel H. Sternberg
{"title":"Evolutionary origins of archaeal and eukaryotic RNA-guided RNA modification in bacterial IS110 transposons","authors":"Hugo Vaysset, Chance Meers, Jean Cury, Aude Bernheim, Samuel H. Sternberg","doi":"10.1038/s41564-024-01889-2","DOIUrl":"10.1038/s41564-024-01889-2","url":null,"abstract":"Transposase genes are ubiquitous in all domains of life and provide a rich reservoir for the evolution of novel protein functions. Here we report deep evolutionary links between bacterial IS110-family transposases, which catalyse RNA-guided DNA recombination using bridge RNAs, and archaeal/eukaryotic Nop5-family proteins, which promote RNA-guided RNA 2′-O-methylation using C/D-box snoRNAs. On the basis of conservation of protein sequence, domain architecture, three-dimensional structure and non-coding RNA features, alongside phylogenetic analyses, we propose that programmable RNA modification emerged through the exaptation of components derived from IS110-like transposons. These findings underscore how recurrent domestication events of transposable elements have driven the evolution of RNA-guided mechanisms. Structural and phylogenetic analyses show that programmable RNA modifications ubiquitous in archaea and eukarya arose from bacterial transposons.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"20-27"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911431","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Matthew R. Olm, Sean P. Spencer, Tadashi Takeuchi, Evelyn Lemus Silva, Justin L. Sonnenburg
{"title":"Metagenomic immunoglobulin sequencing reveals IgA coating of microbial strains in the healthy human gut","authors":"Matthew R. Olm, Sean P. Spencer, Tadashi Takeuchi, Evelyn Lemus Silva, Justin L. Sonnenburg","doi":"10.1038/s41564-024-01887-4","DOIUrl":"10.1038/s41564-024-01887-4","url":null,"abstract":"IgA, the primary human antibody secreted from the gut mucosa, shapes the intestinal microbiota. Methodological limitations have hindered defining which microbial strains are targeted by IgA and the implications of binding. Here we develop a technique, metagenomic immunoglobulin sequencing (MIg-seq), that provides strain-level resolution of microbes coated by IgA and use it to determine IgA coating levels for 3,520 gut microbiome strains in healthy human faeces. We find that both health and disease-associated bacteria are targeted by IgA. Microbial genes are highly predictive of IgA binding levels; in particular, mucus degradation genes are correlated with high binding, and replication rates are significantly reduced for microbes bound by IgA. We demonstrate that IgA binding is more correlated with host immune status than traditional relative abundance measures of microbial community composition. This study introduces a powerful technique for assessing strain-level IgA binding in human stool, paving the way for deeper understanding of IgA-based host–microbe interactions. Metagenomic immunoglobulin sequencing (MIg-seq) uncovered patterns of IgA antibody binding of bacterial strains in the healthy human gut microbiome.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"112-125"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911425","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jérémy Dufloo, Iván Andreu-Moreno, Jorge Moreno-García, Ana Valero-Rello, Rafael Sanjuán
{"title":"Receptor-binding proteins from animal viruses are broadly compatible with human cell entry factors","authors":"Jérémy Dufloo, Iván Andreu-Moreno, Jorge Moreno-García, Ana Valero-Rello, Rafael Sanjuán","doi":"10.1038/s41564-024-01879-4","DOIUrl":"10.1038/s41564-024-01879-4","url":null,"abstract":"Cross-species transmission of animal viruses poses a threat to human health. However, systematic experimental assessments of these risks remain scarce. A critical step in viral infection is cellular internalization mediated by viral receptor-binding proteins (RBPs). Here we constructed viral pseudotypes bearing the RBPs of 102 enveloped RNA viruses and assayed their infectivity across 5,202 RBP–cell combinations. This showed that most of the tested viruses have the potential to enter human cells. Pseudotype infectivity varied widely among the 14 viral families examined and was influenced by RBP characteristics, host of origin and target cell type. Cellular gene expression data revealed that the availability of specific cell-surface receptors is not necessarily the main factor limiting viral entry and that additional host factors must be considered. Altogether, these results suggest weak interspecies barriers in the early stages of infection and advance our understanding of the molecular interactions driving viral zoonosis. Functional systematic pseudotype virus-based analysis of the ability of diverse animal viruses to enter into a panel of well-characterized human cell lines shows a broad compatibility between animal virus receptor-binding proteins and human cell entry factors.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 2","pages":"405-419"},"PeriodicalIF":20.5,"publicationDate":"2025-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01879-4.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142911427","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Potato crop performance is predicted by tuber microbiome","authors":"","doi":"10.1038/s41564-024-01893-6","DOIUrl":"10.1038/s41564-024-01893-6","url":null,"abstract":"A predictive model developed using machine learning, high-throughput sequencing of the microbiomes associated with seed tubers and drone imaging of the crops growing from the tubers can forecast the performance of potato plants based on the microbiome composition of their seed tubers. In addition, this model can identify the best microbial predictors of potato plant growth.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"8-9"},"PeriodicalIF":20.5,"publicationDate":"2024-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142901650","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yang Song, Elisa Atza, Juan J. Sánchez-Gil, Doretta Akkermans, Ronnie de Jonge, Peter G. H. de Rooij, David Kakembo, Peter A. H. M. Bakker, Corné M. J. Pieterse, Neil V. Budko, Roeland L. Berendsen
{"title":"Seed tuber microbiome can predict growth potential of potato varieties","authors":"Yang Song, Elisa Atza, Juan J. Sánchez-Gil, Doretta Akkermans, Ronnie de Jonge, Peter G. H. de Rooij, David Kakembo, Peter A. H. M. Bakker, Corné M. J. Pieterse, Neil V. Budko, Roeland L. Berendsen","doi":"10.1038/s41564-024-01872-x","DOIUrl":"10.1038/s41564-024-01872-x","url":null,"abstract":"Potato vigour, the growth potential of seed potatoes, is a key agronomic trait that varies significantly across production fields due to factors such as genetic background and environmental conditions. Seed tuber microbiomes are thought to influence plant health and crop performance, yet the precise relationships between microbiome composition and potato vigour remain unclear. Here we conducted microbiome sequencing on seed tuber eyes and heel ends from 6 potato varieties grown in 240 fields. By using time-resolved drone imaging of three trial fields in the next season to track crop development, we were able to link microbiome composition with potato vigour. We used microbiome data at varying taxonomic resolutions to build random forest predictive models and found that amplicon sequence variants provided the highest predictive accuracy for potato vigour. The model revealed variety-specific relationships between the seed tuber microbiome and next season’s crop vigour in independent trial fields. With a coefficient of determination value of 0.69 for the best-performing variety, the model accurately predicted vigour in seed tubers from fields not previously included in the analysis. Moreover, the model identified key microbial indicators of vigour from which a Streptomyces, an Acinetobacter and a Cellvibrio amplicon sequence variant stood out as the most important contributors to the model’s accuracy. This study shows that seed potato vigour can be reliably predicted based on the microbiota associated with seed tuber eyes, potentially guiding future microbiome-informed breeding strategies. Time-resolved drone imaging of potato crop development and seed tuber microbiome data can be used to predict potato vigour, or growth potential, in next-season crops in trial fields.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"10 1","pages":"28-40"},"PeriodicalIF":20.5,"publicationDate":"2024-12-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142887345","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}