Marie Le Geay, Kyle Mayers, Martin Küttim, Béatrice Lauga, Vincent E. J. Jassey
{"title":"Development of a digital droplet PCR approach for the quantification of soil micro-organisms involved in atmospheric CO2 fixation","authors":"Marie Le Geay, Kyle Mayers, Martin Küttim, Béatrice Lauga, Vincent E. J. Jassey","doi":"10.1111/1462-2920.16666","DOIUrl":"10.1111/1462-2920.16666","url":null,"abstract":"<p>Carbon-fixing micro-organisms (CFMs) play a pivotal role in soil carbon cycling, contributing to carbon uptake and sequestration through various metabolic pathways. Despite their importance, accurately quantifying the absolute abundance of these micro-organisms in soils has been challenging. This study used a digital droplet polymerase chain reaction (ddPCR) approach to measure the abundance of key and emerging CFMs pathways in fen and bog soils at different depths, ranging from 0 to 15 cm. We targeted total prokaryotes, oxygenic phototrophs, aerobic anoxygenic phototrophic bacteria and chemoautotrophs, optimizing the conditions to achieve absolute quantification of these genes. Our results revealed that oxygenic phototrophs were the most abundant CFMs, making up 15% of the total prokaryotic abundance. They were followed by chemoautotrophs at 10% and aerobic anoxygenic phototrophic bacteria at 9%. We observed higher gene concentrations in fen than in bog. There were also variations in depth, which differed between fen and bog for all genes. Our findings underscore the abundance of oxygenic phototrophs and chemoautotrophs in peatlands, challenging previous estimates that relied solely on oxygenic phototrophs for microbial carbon dioxide fixation assessments. Incorporating absolute gene quantification is essential for a comprehensive understanding of microbial contributions to soil processes. This approach sheds light on the complex mechanisms of soil functioning in peatlands.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16666","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141418414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Manan Shah, Till L. V. Bornemann, Julia K. Nuy, Martin W. Hahn, Alexander J. Probst, Daniela Beisser, Jens Boenigk
{"title":"Genome-resolved metagenomics reveals the effect of nutrient availability on bacterial genomic properties across 44 European freshwater lakes","authors":"Manan Shah, Till L. V. Bornemann, Julia K. Nuy, Martin W. Hahn, Alexander J. Probst, Daniela Beisser, Jens Boenigk","doi":"10.1111/1462-2920.16634","DOIUrl":"10.1111/1462-2920.16634","url":null,"abstract":"<p>Understanding intricate microbial interactions in the environment is crucial. This is especially true for the relationships between nutrients and bacteria, as phosphorus, nitrogen and organic carbon availability are known to influence bacterial population dynamics. It has been suggested that low nutrient conditions prompt the evolutionary process of genome streamlining. This process helps conserve scarce nutrients and allows for proliferation. Genome streamlining is associated with genomic properties such as %GC content, genes encoding sigma factors, percent coding regions, gene redundancy, and functional shifts in processes like cell motility and ATP binding cassette transporters, among others. The current study aims to unveil the impact of nutrition on the genome size, %GC content, and functional properties of pelagic freshwater bacteria. We do this at finer taxonomic resolutions for many metagenomically characterized communities. Our study confirms the interplay of trophic level and genomic properties. It also highlights that different nutrient types, particularly phosphorus and nitrogen, impact these properties differently. We observed a covariation of functional traits with genome size. Larger genomes exhibit enriched pathways for motility, environmental interaction, and regulatory genes. ABC transporter genes reflect the availability of nutrients in the environment, with small genomes presumably relying more on metabolites from other organisms. We also discuss the distinct strategies different phyla adopt to adapt to oligotrophic environments. The findings contribute to our understanding of genomic adaptations within complex microbial communities.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16634","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141330559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carla Greco, Dale T. Andersen, Marian L. Yallop, Gary Barker, Anne D. Jungblut
{"title":"Genome-resolved metagenomics reveals diverse taxa and metabolic complexity in Antarctic lake microbial structures","authors":"Carla Greco, Dale T. Andersen, Marian L. Yallop, Gary Barker, Anne D. Jungblut","doi":"10.1111/1462-2920.16663","DOIUrl":"10.1111/1462-2920.16663","url":null,"abstract":"<p>Lake Untersee, a lake in Antarctica that is perennially covered with ice, is home to unique microbial structures that are not lithified. We have evaluated the structure of the community and its metabolic potential across the pigmented upper layers and the sediment-enriched deeper layers in these pinnacle and cone-shaped microbial structures using metagenomics. These microbial structures are inhabited by distinct communities. The upper layers of the cone-shaped structures have a higher abundance of the cyanobacterial MAG <i>Microcoleus</i>, while the pinnacle-shaped structures have a higher abundance of <i>Elainellacea</i> MAG. This suggests that cyanobacteria influence the morphologies of the mats. We identified stark contrasts in the composition of the community and its metabolic potential between the upper and lower layers of the mat. The upper layers of the mat, which receive light, have an increased abundance of photosynthetic pathways. In contrast, the lower layer has an increased abundance of heterotrophic pathways. Our results also showed that Lake Untersee is the first Antarctic lake with a substantial presence of ammonia-oxidizing <i>Nitrospiracea</i> and <i>amoA</i> genes. The genomic capacity for recycling biological molecules was prevalent across metagenome-assembled genomes (MAGs) that cover 19 phyla. This highlights the importance of nutrient scavenging in ultra-oligotrophic environments. Overall, our study provides new insights into the formation of microbial structures and the potential metabolic complexity of Antarctic laminated microbial mats. These mats are important environments for biodiversity that drives biogeochemical cycling in polar deserts.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16663","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141330635","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Roman A. Barco, N. Merino, B. Lam, B. Budnik, M. Kaplan, F. Wu, J. P. Amend, K. H. Nealson, D. Emerson
{"title":"Comparative proteomics of a versatile, marine, iron-oxidizing chemolithoautotroph","authors":"Roman A. Barco, N. Merino, B. Lam, B. Budnik, M. Kaplan, F. Wu, J. P. Amend, K. H. Nealson, D. Emerson","doi":"10.1111/1462-2920.16632","DOIUrl":"10.1111/1462-2920.16632","url":null,"abstract":"<p>This study conducted a comparative proteomic analysis to identify potential genetic markers for the biological function of chemolithoautotrophic iron oxidation in the marine bacterium <i>Ghiorsea bivora</i>. To date, this is the only characterized species in the class <i>Zetaproteobacteria</i> that is not an obligate iron-oxidizer, providing a unique opportunity to investigate differential protein expression to identify key genes involved in iron-oxidation at circumneutral pH. Over 1000 proteins were identified under both iron- and hydrogen-oxidizing conditions, with differentially expressed proteins found in both treatments. Notably, a gene cluster upregulated during iron oxidation was identified. This cluster contains genes encoding for cytochromes that share sequence similarity with the known iron-oxidase, Cyc2. Interestingly, these cytochromes, conserved in both Bacteria and Archaea, do not exhibit the typical β-barrel structure of Cyc2. This cluster potentially encodes a biological nanowire-like transmembrane complex containing multiple redox proteins spanning the inner membrane, periplasm, outer membrane, and extracellular space. The upregulation of key genes associated with this complex during iron-oxidizing conditions was confirmed by quantitative reverse transcription-PCR. These findings were further supported by electromicrobiological methods, which demonstrated negative current production by <i>G. bivora</i> in a three-electrode system poised at a cathodic potential. This research provides significant insights into the biological function of chemolithoautotrophic iron oxidation.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16632","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141304725","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Age Brauer, Sirli Rosendahl, Anu Kängsep, Alicja Cecylia Lewańczyk, Roger Rikberg, Rita Hõrak, Hedvig Tamman
{"title":"Isolation and characterization of a phage collection against Pseudomonas putida","authors":"Age Brauer, Sirli Rosendahl, Anu Kängsep, Alicja Cecylia Lewańczyk, Roger Rikberg, Rita Hõrak, Hedvig Tamman","doi":"10.1111/1462-2920.16671","DOIUrl":"10.1111/1462-2920.16671","url":null,"abstract":"<p>The environmental bacterium, <i>Pseudomonas putida</i>, possesses a broad spectrum of metabolic pathways. This makes it highly promising for use in biotechnological production as a cell factory, as well as in bioremediation strategies to degrade various aromatic pollutants. For <i>P. putida</i> to flourish in its environment, it must withstand the continuous threats posed by bacteriophages. Interestingly, until now, only a handful of phages have been isolated for the commonly used laboratory strain, <i>P. putida</i> KT2440, and no phage defence mechanisms have been characterized. In this study, we present a new Collection of Environmental <i>P. putida</i> Phages from Estonia, or CEPEST. This collection comprises 67 double-stranded DNA phages, which belong to 22 phage species and 9 phage genera. Our findings reveal that most phages in the CEPEST collection are more infectious at lower temperatures, have a narrow host range, and require an intact lipopolysaccharide for <i>P. putida</i> infection. Furthermore, we show that cryptic prophages present in the <i>P. putida</i> chromosome provide strong protection against the infection of many phages. However, the chromosomal toxin–antitoxin systems do not play a role in the phage defence of <i>P. putida</i>. This research provides valuable insights into the interactions between <i>P. putida</i> and bacteriophages, which could have significant implications for biotechnological and environmental applications.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16671","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141305737","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Anna Doménech-Pascual, Lorena Carrasco-Barea, Frederic Gich, Judit Boadella, Zeus Freixinos Campillo, Rosa Gómez Cerezo, Andrea Butturini, Anna M. Romaní
{"title":"Differential response of bacteria and fungi to drought on the decomposition of Sarcocornia fruticosa woody stems in a saline stream","authors":"Anna Doménech-Pascual, Lorena Carrasco-Barea, Frederic Gich, Judit Boadella, Zeus Freixinos Campillo, Rosa Gómez Cerezo, Andrea Butturini, Anna M. Romaní","doi":"10.1111/1462-2920.16661","DOIUrl":"10.1111/1462-2920.16661","url":null,"abstract":"<p>Inland saline ecosystems suffer multiple stresses (e.g., high radiation, salinity, water scarcity) that may compromise essential ecosystem functions such as organic matter decomposition. Here, we investigated the effects of drought on microbial colonization and decomposition of <i>Sarcocornia fruticosa</i> woody stems across different habitats in a saline watershed: on the dry floodplain, submerged in the stream channel and at the shoreline (first submerged, then emerged). Unexpectedly, weight loss was not enhanced in the submerged stems, while decomposition process differed between habitats. On the floodplain, it was dominated by fungi and high cellulolytic activity; in submerged conditions, a diverse community of bacteria and high ligninolytic activity dominated; and, on the shoreline, enzyme activities were like submerged conditions, but with a fungal community similar to the dry conditions. Results indicate distinct degradation paths being driven by different stress factors: strong water scarcity and photodegradation in dry conditions, and high salinity and reduced oxygen in wet conditions. This suggests that fungi are more resistant to drought, and bacteria to salinity. Overall, in saline watersheds, variations in multiple stress factors exert distinct environmental filters on bacteria and fungi and their role in the decomposition of plant material, affecting carbon cycling and microbial interactions.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16661","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141287983","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Bilge Bahar Camur, Natalia Calixto Mancipe, Brett M. Barney
{"title":"A polyethylene surrogate for microbial community enrichment and characterization","authors":"Bilge Bahar Camur, Natalia Calixto Mancipe, Brett M. Barney","doi":"10.1111/1462-2920.16658","DOIUrl":"10.1111/1462-2920.16658","url":null,"abstract":"<p>Plastic pollution is a vast and increasing problem that has permeated the environment, affecting all aspects of the global food web. Plastics and microplastics have spread to soil, water bodies, and even the atmosphere due to decades of use in a wide range of applications. Plastics include a variety of materials with different properties and chemical characteristics, with polyethylene being a dominant fraction. Polyethylene is also an extremely persistent compound with slow rates of photodegradation or biodegradation. In this study, we developed a method to isolate communities of microbes capable of biodegrading a polyethylene surrogate. This method allows us to study potential polyethylene degradation over much shorter time periods. Using this method, we enriched several communities of microbes that can degrade the polyethylene surrogate within weeks. We also identified specific bacterial strains with a higher propensity to degrade compounds similar to polyethylene. We provide a description of the method, the variability and efficacy of four different communities, and key strains from these communities. This method should serve as a straightforward and adaptable tool for studying polyethylene biodegradation.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16658","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141283332","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Leena Hamberg, Jarno Vanhatalo, Sannakajsa Velmala, Andy F. S. Taylor, John MacKay, Sébastien Caron, Fred O. Asiegbu, Risto Sievänen, Pasi Raumonen, Tuija Hytönen, Taina Pennanen
{"title":"The community of root fungi is associated with the growth rate of Norway spruce (Picea abies)","authors":"Leena Hamberg, Jarno Vanhatalo, Sannakajsa Velmala, Andy F. S. Taylor, John MacKay, Sébastien Caron, Fred O. Asiegbu, Risto Sievänen, Pasi Raumonen, Tuija Hytönen, Taina Pennanen","doi":"10.1111/1462-2920.16662","DOIUrl":"10.1111/1462-2920.16662","url":null,"abstract":"<p>Our study delved into the relationship between root-associated fungi, gene expression and plant morphology in Norway spruce cuttings derived from both slow-and fast-growing trees. We found no clear link between the gene expression patterns of adventitious roots and the growth phenotype, suggesting no fundamental differences in the receptiveness to fungal symbionts between the phenotypes. Interestingly, saplings from slow-growing parental trees exhibited a higher richness of ectomycorrhizal species and larger roots. Some ectomycorrhizal species, typically found on mature spruces, were more prevalent on saplings from slow-growing spruces. The ericoid mycorrhizal fungus, <i>Hyaloscypha hepaticola</i>, showed a stronger association with saplings from fast-growing spruces. Moreover, saplings from slow-growing spruces had a greater number of Ascomycete taxa and free-living saprotrophic fungi. Aboveground sapling stems displayed some phenotypic variation; saplings from fast-growing phenotypes had longer branches but fewer whorls in their stems compared to those from the slow-growing group. In conclusion, the observed root-associated fungi and phenotypic characteristics in young Norway spruces may play a role in their long-term growth rate. This suggests that the early interactions between spruces and fungi could potentially influence their growth trajectory.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16662","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141260920","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sally L. Bornbusch, Hannah E. Shinnerl, Lindsey Gentry, Mia M. Keady, Virginia Glick, Carly R. Muletz-Wolz, Michael L. Power
{"title":"Local environment shapes milk microbiomes while evolutionary history constrains milk macronutrients in captive cercopithecine primates","authors":"Sally L. Bornbusch, Hannah E. Shinnerl, Lindsey Gentry, Mia M. Keady, Virginia Glick, Carly R. Muletz-Wolz, Michael L. Power","doi":"10.1111/1462-2920.16664","DOIUrl":"10.1111/1462-2920.16664","url":null,"abstract":"<p>Milk is a complex biochemical fluid that includes macronutrients and microbiota, which, together, are known to facilitate infant growth, mediate the colonization of infant microbiomes, and promote immune development. Examining factors that shape milk microbiomes and milk-nutrient interplay across host taxa is critical to resolving the evolution of the milk environment. Using a comparative approach across four cercopithecine primate species housed at three facilities under similar management conditions, we test for the respective influences of the local environment (housing facility) and host species on milk (a) macronutrients (fat, sugar, and protein), (b) microbiomes (16S rRNA), and (c) predicted microbial functions. We found that milk macronutrients were structured according to host species, while milk microbiomes and predicted function were strongly shaped by the local environment and, to a lesser extent, host species. The milk microbiomes of rhesus macaques (<i>Macaca mulatta</i>) at two different facilities more closely resembled those of heterospecific facility-mates compared to conspecifics at a different facility. We found similar, facility-driven patterns of microbial functions linked to physiology and immune modulation, suggesting that milk microbiomes may influence infant health and development. These results provide novel insight into the complexity of milk and its potential impact on infants across species and environments.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141237358","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cristobal A. Onetto, Chris M. Ward, Steven Van Den Heuvel, Laura Hale, Kathleen Cuijvers, Anthony R. Borneman
{"title":"Temporal and spatial dynamics within the fungal microbiome of grape fermentation","authors":"Cristobal A. Onetto, Chris M. Ward, Steven Van Den Heuvel, Laura Hale, Kathleen Cuijvers, Anthony R. Borneman","doi":"10.1111/1462-2920.16660","DOIUrl":"10.1111/1462-2920.16660","url":null,"abstract":"<p>Over 6 years, we conducted an extensive survey of spontaneous grape fermentations, examining 3105 fungal microbiomes across 14 distinct grape-growing regions. Our investigation into the biodiversity of these fermentations revealed that a small number of highly abundant genera form the core of the initial grape juice microbiome. Consistent with previous studies, we found that the region of origin had the most significant impact on microbial diversity patterns. We also discovered that certain taxa were consistently associated with specific geographical locations and grape varieties, although these taxa represented only a minor portion of the overall diversity in our dataset. Through unsupervised clustering and dimensionality reduction analysis, we identified three unique community types, each exhibiting variations in the abundance of key genera. When we projected these genera onto global branches, it suggested that microbiomes transition between these three broad community types. We further investigated the microbial community composition throughout the fermentation process. Our observations indicated that the initial microbial community composition could predict the diversity during the early stages of fermentation. Notably, <i>Hanseniaspora uvarum</i> emerged as the primary non-<i>Saccharomyces</i> species within this large collection of samples.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":"26 6","pages":""},"PeriodicalIF":5.1,"publicationDate":"2024-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141185457","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}