Paul G Helfrich, Johnathan Feldman, Eva Andrade-Barahona, Isaiah Robertson, Jordan Foster, Renee Hofacker, Gavin Dahlquist Selking, Cody S Sheik, Alysia Cox
{"title":"Aqueous copper geochemistry shapes the sediment microbial resistome in a recovering stream","authors":"Paul G Helfrich, Johnathan Feldman, Eva Andrade-Barahona, Isaiah Robertson, Jordan Foster, Renee Hofacker, Gavin Dahlquist Selking, Cody S Sheik, Alysia Cox","doi":"10.1111/1758-2229.70045","DOIUrl":"10.1111/1758-2229.70045","url":null,"abstract":"<p>Aqueous metals are pervasive contaminants associated with historical mining. We produced and examined 16 metagenomes from a contaminated creek to investigate how anthropogenic metal contamination shapes the functional profiles of microbial communities. We then incorporated the metagenomic profiles and concurrently collected geochemical context into a multivariate model to examine correlations between stream geochemistry and microbial functional potential. Integrating the metagenomes with full geochemical profiles emphasised that even low metalloid concentrations shaped microbial functionality, seasonal shifts in copper bioavailability and arsenic exposure correlated with genetic variation, and copper resistomes were spatiotemporally distinct. This study provides new insights into microbial metabolic potential and microbe-metal(loid) interactions.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70045","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142737869","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Julia Manetsberger, Natacha Caballero Gómez, Nabil Benomar, Graham Christie, Hikmate Abriouel
{"title":"Phenotypic and Genomic Insights Into Bacillus spp. and Peribacillus spp. of Spanish Olive Groves With Biotechnological Potential","authors":"Julia Manetsberger, Natacha Caballero Gómez, Nabil Benomar, Graham Christie, Hikmate Abriouel","doi":"10.1111/1758-2229.70053","DOIUrl":"10.1111/1758-2229.70053","url":null,"abstract":"<p>Spore-forming organisms are an integral component of the rhizosphere, providing plants with significant advantages. Previous studies determined the antimicrobial activity of the olive sporobiota, identifying five candidates of particular relevance, belonging to the <i>Bacillus subtilis</i>, <i>Peribacillus simplex</i> and <i>Bacillus cereus</i> clade. This study aimed to determine their biotechnological properties, safety aspects, spore structure and resistance, and interaction with the environment through a combined microbiological and genomic approach. We report on the ability of these strains to produce hydrolytic and surface-active enzymes and provide evidence for differences in population behaviour through the formation of strong sessile or floating biofilms. Electron microscopic analysis revealed for the first time the presence of an exosporium layer in olive sporobiota isolates belonging to the <i>P. simplex</i> and <i>B. cereus</i> clade, including numerous pili-like structures on the latter. Spores showed significant differences in their resistance to wet heat, oxidising agents, and UV exposure. Whole genome sequencing of isolate <i>Peribacillus frigoritolerans</i> yielded information on its antimicrobial compound biosynthesis and environmental safety. Overall, our findings provide insights into the phenotypic, morphological and genetic variations of spore-formers from Spanish olive groves, which can be useful for the development of bioactive compounds in sustainable agriculture.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70053","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142737875","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hunter B. Arrington, Sung Gu Lee, Jun Hyuck Lee, Joseph A. Covi
{"title":"Assessment of the cyst wall and surface microbiota in dormant embryos of the Antarctic calanoid copepod, Boeckella poppei","authors":"Hunter B. Arrington, Sung Gu Lee, Jun Hyuck Lee, Joseph A. Covi","doi":"10.1111/1758-2229.70035","DOIUrl":"10.1111/1758-2229.70035","url":null,"abstract":"<p>Embryos of zooplankton from inland waters and estuaries can remain viable for years in an extreme state of metabolic suppression. How these embryos resist microbial attack with limited metabolic capacity for immune defence or repair is unknown. As a first step in evaluating resistance to microbial attack in dormant zooplankton, surface colonization of the Antarctic freshwater copepod, <i>Boeckella poppei</i>, was evaluated. Scanning electron micrographs demonstrate the outer two layers of a five-layered cyst wall in <i>B. poppei</i> fragment and create a complex environment for microbial colonization. By contrast, the third layer remains undamaged during years of embryo storage in native sediment. The absence of damage to the third layer indicates that it is resistant to degradation by microbial enzymes. Scanning electron microscopy and microbiome analysis using the 16S ribosomal subunit gene and internal transcribed spacer (ITS) region demonstrate the presence of a diverse microbial community on the embryo surface. Coverage of the embryos with microbial life varies from a sparse population with individual microbes to complete coverage by a thick biofilm. Extracellular polymeric substance binds debris and provides a structural element for the microbial community. Frequent observation of bacterial fission indicates that the biofilm is viable in stored sediments.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70035","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142737872","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Beatriz Ramírez-Serrano, Marina Querejeta, Zhivko Minchev, María J. Pozo, Géraldine Dubreuil, David Giron
{"title":"Root inoculation with soil-borne microorganisms alters gut bacterial communities and performance of the leaf-chewer Spodoptera exigua","authors":"Beatriz Ramírez-Serrano, Marina Querejeta, Zhivko Minchev, María J. Pozo, Géraldine Dubreuil, David Giron","doi":"10.1111/1758-2229.70049","DOIUrl":"https://doi.org/10.1111/1758-2229.70049","url":null,"abstract":"<p>Soil-borne microorganisms can impact leaf-chewing insect fitness by modifying plant nutrition and defence. Whether the altered insect performance is linked to changes in microbial partners of caterpillars remains unclear. We investigated the effects of root inoculation with soil bacteria or fungi on the gut bacterial community and biomass of the folivore <i>Spodoptera exigua</i>. We also explored the potential correlation between both parameters. We performed herbivory bioassay using leaves of tomato plants (<i>Solanum lycopersicum</i>), measured caterpillar weight gain and characterized the gut bacterial communities via 16S rRNA gene metabarcoding. All soil microbes modified the gut bacterial communities, but the extent of these changes depended on the inoculated species. <i>Rhizophagus irregularis</i> and <i>Bacillus amyloliquefaciens</i> had opposite effects on <i>S. exigua</i> weight. While plant inoculation with the fungus influenced gut bacterial diversity, <i>B. amyloliquefaciens</i> also affected the community composition. A reduced abundance of two <i>S. exigua</i> enterococcal symbionts correlated with decreased insect biomass. Our results show that soil microorganisms can induce plant-mediated changes in the gut bacterial community of foliar-feeding caterpillars. We propose that the impact of these alterations on insect performance might rely on specific adaptations within the gut bacteria, rather than solely on the occurrence of changes.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70049","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142724227","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Beatriz Ramírez-Serrano, Marina Querejeta, Zhivko Minchev, María J. Pozo, Géraldine Dubreuil, David Giron
{"title":"Root inoculation with soil-borne microorganisms alters gut bacterial communities and performance of the leaf-chewer Spodoptera exigua","authors":"Beatriz Ramírez-Serrano, Marina Querejeta, Zhivko Minchev, María J. Pozo, Géraldine Dubreuil, David Giron","doi":"10.1111/1758-2229.70049","DOIUrl":"https://doi.org/10.1111/1758-2229.70049","url":null,"abstract":"<p>Soil-borne microorganisms can impact leaf-chewing insect fitness by modifying plant nutrition and defence. Whether the altered insect performance is linked to changes in microbial partners of caterpillars remains unclear. We investigated the effects of root inoculation with soil bacteria or fungi on the gut bacterial community and biomass of the folivore <i>Spodoptera exigua</i>. We also explored the potential correlation between both parameters. We performed herbivory bioassay using leaves of tomato plants (<i>Solanum lycopersicum</i>), measured caterpillar weight gain and characterized the gut bacterial communities via 16S rRNA gene metabarcoding. All soil microbes modified the gut bacterial communities, but the extent of these changes depended on the inoculated species. <i>Rhizophagus irregularis</i> and <i>Bacillus amyloliquefaciens</i> had opposite effects on <i>S. exigua</i> weight. While plant inoculation with the fungus influenced gut bacterial diversity, <i>B. amyloliquefaciens</i> also affected the community composition. A reduced abundance of two <i>S. exigua</i> enterococcal symbionts correlated with decreased insect biomass. Our results show that soil microorganisms can induce plant-mediated changes in the gut bacterial community of foliar-feeding caterpillars. We propose that the impact of these alterations on insect performance might rely on specific adaptations within the gut bacteria, rather than solely on the occurrence of changes.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70049","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142724223","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kristel Mijnendonckx, Carla Smolders, Deepa Bartak, Trung Le Duc, Mar Morales-Hidalgo, Cristina Povedano-Priego, Fadwa Jroundi, Mohamed L. Merroun, Natalie Leys, Katerina Cerna
{"title":"Comparing the effectiveness of different DNA extraction methods in MX-80 bentonite","authors":"Kristel Mijnendonckx, Carla Smolders, Deepa Bartak, Trung Le Duc, Mar Morales-Hidalgo, Cristina Povedano-Priego, Fadwa Jroundi, Mohamed L. Merroun, Natalie Leys, Katerina Cerna","doi":"10.1111/1758-2229.70047","DOIUrl":"https://doi.org/10.1111/1758-2229.70047","url":null,"abstract":"<p>Approaches to DNA extraction play a crucial role in determining the variability of results obtained through 16S rRNA amplicon sequencing. Particularly, clay-rich samples can impede the efficiency of various standard cultivation-independent techniques. We conducted an inter-laboratory comparison study to thoroughly assess the efficacy of two published DNA extraction methods (kit-based and phenol-chloroform-based) specifically designed for bentonite samples. To this end, we spiked Wyoming MX 80 bentonite with two different mock communities and compared the obtained DNA yield and purity, the presence of contaminants and the community profile. Our findings suggest that both methods are equally viable, with the best choice depending on the specific requirements of the downstream analysis. However, it is crucial to maintain consistency in the chosen method, as comparing results becomes challenging, particularly in the presence of bentonite. In summary, our study emphasizes the significance of standardized DNA extraction methods and underscores the importance of validating these methods using appropriate controls when studying microbial communities with 16S rRNA amplicon sequencing, particularly in environments characterized by low biomass and clay-rich compositions. Additionally, slight modifications to one of the extraction methods can substantially enhance its efficiency.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70047","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142708265","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kristel Mijnendonckx, Carla Smolders, Deepa Bartak, Trung Le Duc, Mar Morales-Hidalgo, Cristina Povedano-Priego, Fadwa Jroundi, Mohamed L. Merroun, Natalie Leys, Katerina Cerna
{"title":"Comparing the effectiveness of different DNA extraction methods in MX-80 bentonite","authors":"Kristel Mijnendonckx, Carla Smolders, Deepa Bartak, Trung Le Duc, Mar Morales-Hidalgo, Cristina Povedano-Priego, Fadwa Jroundi, Mohamed L. Merroun, Natalie Leys, Katerina Cerna","doi":"10.1111/1758-2229.70047","DOIUrl":"https://doi.org/10.1111/1758-2229.70047","url":null,"abstract":"<p>Approaches to DNA extraction play a crucial role in determining the variability of results obtained through 16S rRNA amplicon sequencing. Particularly, clay-rich samples can impede the efficiency of various standard cultivation-independent techniques. We conducted an inter-laboratory comparison study to thoroughly assess the efficacy of two published DNA extraction methods (kit-based and phenol-chloroform-based) specifically designed for bentonite samples. To this end, we spiked Wyoming MX 80 bentonite with two different mock communities and compared the obtained DNA yield and purity, the presence of contaminants and the community profile. Our findings suggest that both methods are equally viable, with the best choice depending on the specific requirements of the downstream analysis. However, it is crucial to maintain consistency in the chosen method, as comparing results becomes challenging, particularly in the presence of bentonite. In summary, our study emphasizes the significance of standardized DNA extraction methods and underscores the importance of validating these methods using appropriate controls when studying microbial communities with 16S rRNA amplicon sequencing, particularly in environments characterized by low biomass and clay-rich compositions. Additionally, slight modifications to one of the extraction methods can substantially enhance its efficiency.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70047","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142708092","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient","authors":"Yihui Ding, Rui-Ao Ma, Ran Zhang, Hongwei Zhang, Jian Zhang, Shaopeng Li, Si-Yu Zhang","doi":"10.1111/1758-2229.70042","DOIUrl":"10.1111/1758-2229.70042","url":null,"abstract":"<p>Antibiotic resistance genes (ARGs) are ancient and widespread in natural habitats, providing survival advantages for microbiomes under challenging conditions. In mountain ecosystems, phyllosphere bacterial communities face multiple stress conditions, and the elevational gradients of mountains represent crucial environmental gradients for studying biodiversity distribution patterns. However, the distribution patterns of ARGs in the phyllosphere along elevational gradients, and their correlation with bacterial community structures, remain poorly understood. Here, we applied metagenomic analyses to investigate the abundance and diversity of ARGs in 88 phyllosphere samples collected from Mount Tianmu, a national natural reserve. Our results showed that the abundance of ARGs in the phyllosphere increased along elevational gradients and was dominated by multidrug resistance and efflux pumps. The composition of bacterial communities, rather than plant traits or abiotic factors, significantly affected ARG abundance. Moreover, increased ARG abundance was correlated with greater phylogenetic overdispersion and a greater proportion of negative associations in the bacterial co-occurrence networks, suggesting that bacterial competition primarily shapes phyllosphere resistomes. These findings constitute a major advance in the biodiversity of phyllosphere resistomes along elevations, emphasizing the significant impact of bacterial community structure and assembly on ARG distribution, and are essential for understanding the emergence of ARGs.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11581953/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142685525","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Laura Matarredona, Basilio Zafrilla, Mónica Camacho, María-José Bonete, Julia Esclapez
{"title":"Understanding the tolerance of halophilic archaea to stress landscapes","authors":"Laura Matarredona, Basilio Zafrilla, Mónica Camacho, María-José Bonete, Julia Esclapez","doi":"10.1111/1758-2229.70039","DOIUrl":"10.1111/1758-2229.70039","url":null,"abstract":"<p>Haloarchaea, known for their resilience to environmental fluctuations, require a minimum salt concentration of 10% (w/v) for growth and can survive up to 35% (w/v) salinity. In biotechnology, these halophiles have diverse industrial applications. This study investigates the tolerance responses of nine haloarchaea: <i>Haloferax mediterranei</i>, <i>Haloferax volcanii</i>, <i>Haloferax gibbonsii</i>, <i>Halorubrum californiense</i>, <i>Halorubrum litoreum, Natrinema pellirubrum</i>, <i>Natrinema altunense</i>, <i>Haloterrigena thermotolerans</i> and <i>Haloarcula sinaiiensis</i>, under various stressful conditions. All these archaea demonstrated the ability to thrive in the presence of toxic metals such as chromium, nickel, cobalt and arsenic, and their tolerance to significantly elevated lithium concentrations in the medium was remarkable. Among the studied haloarchaea, <i>Hfx. mediterranei</i> exhibited superior resilience, particularly against lithium, with an impressive minimum inhibitory concentration (MIC) of up to 4 M LiCl, even replacing NaCl entirely. <i>Haloferax</i> species showed specificity for conditions with maximal growth rates, while <i>Htg. thermotolerans</i> and <i>Nnm. altunense</i> displayed high resilience without losing growth throughout the ranges, although these were generally low. ICP-MS results highlighted the impressive intracellular lithium accumulation in <i>Nnm. pellirubrum</i>, emphasizing its potential significance in bioremediation. This research highlights a new characteristic of haloarchaea, their tolerance to high lithium concentrations and the potential for new applications in extreme industrial processes and bioremediation.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11578932/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142680441","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Metagenomic analysis reveals houseflies as indicators for monitoring environmental antibiotic resistance genes","authors":"Yuhan Yang, Ping Xu, Wei He, Fei Tao","doi":"10.1111/1758-2229.70032","DOIUrl":"10.1111/1758-2229.70032","url":null,"abstract":"<p>Given the threat to public health posed by antibiotic resistance transmission, environmental monitoring is essential for tracking antibiotic resistance genes (ARGs). Houseflies, being ubiquitous organisms capable of carrying and disseminating ARGs, serve as suitable indicators for environmental monitoring. In this study, we employ metagenomic approaches to investigate housefly body surface samples from five typical sites associated with human activities. The investigation reveals microbiome diversity among the samples, along with variations in the occurrence and mobility potential of ARGs. Metagenomic analysis indicates that the composition of ARGs on housefly body surfaces is influenced by environmental ARGs, which may be enriched on the housefly body surface. The resistance genes related to multidrug, <i>β</i>-lactam, bacitracin, and tetracycline were the predominant ARGs detected, with multidrug-related ARGs consistently exhibiting dominance. Furthermore, the abundance of ARGs in the different housefly body surface samples was found to correlate with the population density and mobility of the sampling site. Natural environments exhibited the lowest ARG abundance, while areas with higher population density and limited population mobility displayed higher ARG abundance. This study emphasizes the effectiveness of houseflies as monitors for environmental ARGs and underscores their potential for assessing and controlling antibiotic resistance risks in urban environments.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"16 6","pages":""},"PeriodicalIF":3.6,"publicationDate":"2024-11-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11576324/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142674450","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}