{"title":"Increased Nutrient Levels Enhance Bacterial Exopolysaccharides Production in the Context of Algae","authors":"Valeria Lipsman, Einat Segev","doi":"10.1111/1758-2229.70071","DOIUrl":"https://doi.org/10.1111/1758-2229.70071","url":null,"abstract":"<p>Microbial aggregation is central in environmental processes, such as marine snow and harmful marine mucilage events. Nutrient enrichment positively correlates with microbial aggregation. This correlation is largely attributed to the overgrowth of microalgae and the overproduction of agglomerating exopolysaccharides. However, recent studies highlight the significant contribution of bacterial exopolysaccharides to algal-bacterial aggregation. Here, using controlled laboratory experiments and environmental metatranscriptomic analysis, we investigate the impact of nutrient enrichment on bacterial exopolysaccharides production, while bacteria are in the context of their algal hosts. Our findings demonstrate a marked increase in bacterial exopolysaccharides production in response to a relative increase of inorganic phosphorus and nitrogen levels, both in the lab and in the environment. These results highlight the interplay between nutrient regimes, bacterial physiology and microbial aggregation in marine ecosystems and emphasise gaps in our understanding regarding the bacterial role in environmental processes that involve microbial aggregation.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-2229.70071","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143248488","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}
Pia Marter, Heike M. Freese, Victoria Ringel, Henner Brinkmann, Silke Pradella, Manfred Rohde, Michal Jarek, Cathrin Spröer, Irene Wagner-Döbler, Jörg Overmann, Boyke Bunk, Jörn Petersen
{"title":"Superior Resolution Profiling of the Coleofasciculus Microbiome by Amplicon Sequencing of the Complete 16S rRNA Gene and ITS Region","authors":"Pia Marter, Heike M. Freese, Victoria Ringel, Henner Brinkmann, Silke Pradella, Manfred Rohde, Michal Jarek, Cathrin Spröer, Irene Wagner-Döbler, Jörg Overmann, Boyke Bunk, Jörn Petersen","doi":"10.1111/1758-2229.70066","DOIUrl":"10.1111/1758-2229.70066","url":null,"abstract":"<p>The filamentous cyanobacterium <i>Coleofasciculus chthonoplastes</i> is the key primary producer of marine microbial mats. We elucidated the microbiomes of 32 non-axenic <i>Coleofasciculus</i> isolates using PacBio-based amplicon sequencing of the complete 16S rRNA gene and the internally transcribed spacer (16S-ITS). The length of authentic amplicon sequence variants (ASVs) ranged from 1827 to 3044 nucleotides (median: 2267 nt). The results, which were complemented by metagenome analyses and cultivation approaches, revealed the presence of more than 70 associated heterotrophs in the culture of <i>Coleofasciculus</i> sp. WW12. The great bacterial diversity in the cyanosphere is dominated by <i>Pseudomonadota</i> (59%) and <i>Bacteroidota</i> (23%). Allelic ribosomal operon variants were detected in 18 <i>Coleofasciculus</i> strains and our analyses proposed the presence of at least four different species. A comparative analysis of cyanobacterial microbiomes documented complementary advantages of amplicon sequencing versus metagenomics with an individual strength of the 16S-ITS approach in terms of (i) ribosomal target sequence quality, (ii) contaminant detection and (iii) identification of rare bacteria. The characterisation of the <i>Coleofasciculus</i> microbiome showed that long-read amplicon sequencing of the 16S-ITS region is the method of choice for rapid profiling of non-axenic cyanobacteria. Its superior resolution allows a reliable differentiation of even very closely related strains.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11785472/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143072955","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}
Naciye Sena Cagatay, Mohammad Akhoundi, Arezki Izri, Sophie Brun, Gregory D. D. Hurst
{"title":"Prevalence of Heritable Symbionts in Parisian Bedbugs (Hemiptera: Cimicidae)","authors":"Naciye Sena Cagatay, Mohammad Akhoundi, Arezki Izri, Sophie Brun, Gregory D. D. Hurst","doi":"10.1111/1758-2229.70054","DOIUrl":"10.1111/1758-2229.70054","url":null,"abstract":"<p>Like many insects, the biology of bedbugs is impacted by a range of partner heritable microbes. Three maternally inherited symbionts are recognised: <i>Wolbachia</i> (an obligate partner), <i>Symbiopectobacterium purcellii</i> strain <i>Sy</i>Clec, and <i>Candidatus</i> Tisiphia sp. (facultative symbionts typically present in some but not all individuals). Past work had examined the presence of these heritable microbes from established laboratory lines, but not from broader field samples. We therefore deployed targeted endpoint PCR assays to determine the symbiont infection status for 50 bedbugs collected from 10 districts of Paris during the 2023 outbreak. All three symbionts were found to be broadly present across <i>Cimex lectularius</i> samples, with the <i>Symbiopectobacterium</i>-<i>Candidatus</i> Tisiphia-<i>Wolbachia</i> triple infection most commonly observed. A minority of individuals lacked either one or both facultative symbionts. Five mtDNA haplotypes were observed across the COI barcode region, and triple infections were found in all mtDNA haplotypes, indicating that symbiont infection is not a recent invasion event. We conclude that the Parisian bedbug outbreak was one in which the host's secondary symbionts were present at high-frequency coinfections, and facultative symbionts are an important but uncharacterised component of bedbug populations.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11779572/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143062174","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":"Temperature Requirements Can Affect the Microbial Composition Causing Sour Rot in Grapes","authors":"Chiara Brischetto, Vittorio Rossi, Irene Salotti, Luca Languasco, Giorgia Fedele","doi":"10.1111/1758-2229.70061","DOIUrl":"10.1111/1758-2229.70061","url":null,"abstract":"<p>Sour rot (SR) is a late-season non-Botrytis rot affecting grapevines, resulting from a complex interplay of microorganisms, including non-<i>Saccharomyces</i> yeasts and acetic acid bacteria. Nonmicrobial factors contributing to disease development encompass vectors (e.g., <i>Drosophila</i> spp.), the presence of wounds or microcracks on grape berry surfaces, and environmental conditions during berry ripening. The microbial complexes within SR-affected grapes exhibit variability among different bioclimates and seasons, with certain microorganisms predominating under specific conditions. This study examined the influence of environmental conditions on the microbiome composition associated with SR-affected grape bunches, utilising data from 41 locations across three distinct Italian bioclimates. We selected nine yeast and two bacterial species frequently isolated from sour-rotted grapes for analysis. The growth responses of these microorganisms to temperature were assessed by categorising them into four ecophysiological clusters. Furthermore, we analysed the distribution of these microorganisms and their respective ecophysiological clusters across the three bioclimates. The results indicate that the microbiomes involved in SR can vary according to the bioclimatic conditions of the grape-growing area. Further research is required to comprehend the ecological requirements of these microorganisms, define their ecological niches to understand their geographical distribution and epidemiology, and enhance SR management strategies.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11772317/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143051154","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":"Sulfate and Dissolved Organic Carbon Concentrations Drive Distinct Microbial Community Patterns in Prairie Wetland Ponds","authors":"Zohra Zahir, Faraz Khan, Britt D. Hall","doi":"10.1111/1758-2229.70069","DOIUrl":"10.1111/1758-2229.70069","url":null,"abstract":"<p>Prairie wetland ponds on the Great Plains of North America offer a diverse array of geochemical scenarios that can be informative about their impact on microbial communities. These ecosystems offer invaluable ecological services while experiencing significant stressors, primarily through drainage and climate change. In this first study systematically combining environmental conditions with microbial community composition to identify various niches in prairie wetland ponds, sediments had higher microbial abundance but lower phylogenetic diversity in ponds with lower concentrations of dissolved organic carbon ([DOC]; 10–18 mg/L) and sulfate ([SO<sub>4</sub><sup>2−</sup>]; 37–58 mg/L) in water. As [DOC] and [SO<sub>4</sub><sup>2−</sup>] increased, there was an initial decline in abundance but not phylogenetic diversity. Maximum values of both abundance and phylogenetic diversity occurred between 56 and 115 mg/L [DOC] and 5,000–6,000 mg/L [SO<sub>4</sub><sup>2−</sup>] and decreased thereafter in ponds with 150–180 mg/L and 8,000–14,000 mg/L [DOC] and [SO<sub>4</sub><sup>2−</sup>], respectively. These findings confirm that environmental variables shape the microbial communities and that key microbial taxa involved in sulfur and carbon cycling dominated these ponds potentially impacting vital biogeochemical processes such as bioavailability of heavy metals, carbon sequestration, and methane emissions.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11772329/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143051152","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}
Angélica Jara-Servin, Luis D. Alcaraz, Sabino I. Juarez-Serrano, Aarón Espinosa-Jaime, Ivan Barajas, Lucia Morales, Alexander DeLuna, Antonio Hernández-López, Eugenio Mancera
{"title":"Microbial Communities in Agave Fermentations Vary by Local Biogeographic Regions","authors":"Angélica Jara-Servin, Luis D. Alcaraz, Sabino I. Juarez-Serrano, Aarón Espinosa-Jaime, Ivan Barajas, Lucia Morales, Alexander DeLuna, Antonio Hernández-López, Eugenio Mancera","doi":"10.1111/1758-2229.70057","DOIUrl":"10.1111/1758-2229.70057","url":null,"abstract":"<p>The production of traditional agave spirits in Mexico, such as mezcal, involves a process that uses environmental microorganisms to ferment the cooked must from agave plants. By analysing these microorganisms, researchers can understand the dynamics of microbial communities at the interface of natural and human-associated environments. This study involved 16S and ITS amplicon sequencing of 99 fermentation tanks from 42 distilleries across Mexico. The Agave species used, production methods, climatic conditions and biogeographic characteristics varied significantly among sites. However, certain taxa were found in most fermentations, indicating a core group of microorganisms common to these communities. The primary variable consistently associated with the composition of both bacterial and fungal communities was the distillery, suggesting that local production practices and site-specific attributes influence the microbiomes. The fermentation stage, climate and producing region also affected community composition but only for prokaryotes. Analysis of multiple tanks within three distilleries showed taxa enriched in specific fermentation stages or agave species. This research provides a detailed analysis of the microbiome of agave fermentations, offering important knowledge for its management and conservation.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11761429/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143045128","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":"Microbial seafood safety assessment following a marine mucilage disaster in the Sea of Marmara","authors":"Didem Üçok, Şehnaz Yasemin Tosun, Nuray Erkan, İdil Can Tunçelli, Hande Doğruyol, Şafak Ulusoy, Sühendan Mol, Özkan Özden, Eda Dagsuyu, Refiye Yanardag","doi":"10.1111/1758-2229.70050","DOIUrl":"10.1111/1758-2229.70050","url":null,"abstract":"<p>Marine mucilage disasters, primarily caused by global warming and marine pollution, threaten food security and the sustainability of marine food resources. This study assessed the microbial risks to public health in common sole, deep-water rose shrimp, European anchovy, Atlantic horse mackerel and Mediterranean mussel following the mucilage disaster in the Sea of Marmara in 2021. The total viable count, total Enterobacteriaceae count and the presence of <i>Escherichia coli</i> O157:H7, <i>Salmonella</i> spp., <i>Listeria monocytogenes</i>, <i>Vibrio parahaemolyticus</i>, <i>Vibrio cholerae</i>, <i>Aeromonas hydrophila</i>, <i>Clostridium perfringens</i> and <i>Bacillus cereus</i> were studied during the 2021–2022 fishing season. In September, the first month of the catching season, pathogens in all seafood were markedly higher compared to the entire season: <i>E. coli</i> O157:H7: 86%, <i>Salmonella</i> spp.: 30%, <i>L. monocytogenes</i>: 21%, <i>V. parahaemolyticus</i>: 53% and <i>A. hydrophila</i>: 100%. The main factors for the high prevalence of pathogens in September are elevated seawater temperature and the fact that it is the first month following the mucilage disaster. Following natural disasters such as mucilage, evisceration of seafood, washing with clean water, depuration of shellfish and ensuring adequate cooking time and temperature are essential for food safety and public health.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11754768/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143021347","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}
Inkeri Vuori, Greta Gaiani, Sıla Arsın, Endrews Delbaje, Julia Järn, Robert Snårbacka, Annaël Couëdelo, Gayathri Murukesan, Matti Wahlsten, Jouni Jokela, Tânia Keiko Shishido, David P. Fewer
{"title":"Direct Evidence of Microbial Sunscreen Production by Scum-Forming Cyanobacteria in the Baltic Sea","authors":"Inkeri Vuori, Greta Gaiani, Sıla Arsın, Endrews Delbaje, Julia Järn, Robert Snårbacka, Annaël Couëdelo, Gayathri Murukesan, Matti Wahlsten, Jouni Jokela, Tânia Keiko Shishido, David P. Fewer","doi":"10.1111/1758-2229.70056","DOIUrl":"10.1111/1758-2229.70056","url":null,"abstract":"<p>Mycosporine-like amino acids are water-soluble secondary metabolites that protect photosynthetic microorganisms from ultraviolet radiation. Here, we present direct evidence for the production of these compounds in surface scums of cyanobacteria along the Baltic Sea coast. We collected 59 environmental samples from the southern coast of Finland during the summers of 2021 and 2022 and analysed them using high-resolution liquid chromatography-mass spectrometry. Our results revealed the presence of microbial sunscreens in nearly all surface scum samples. Mycosporine-like amino acids are synthesised through the coordinated action of four biosynthetic enzymes encoded in a compact biosynthetic pathway. Bioinformatics analysis of the mysB biosynthetic gene from a surface scum indicated that the cyanobacteria responsible for production belonged to the <i>Anabaena</i>/<i>Dolichospermum</i>/<i>Aphanizomenon</i> species complex. We mapped the distribution of biosynthetic enzymes onto a phylogenomic tree, utilising 120 bacterial single-copy conserved genes from 101 draft or complete genomes within the species complex. This analysis showed that 48% of identified species possess the ability to produce these compounds, with biosynthetic pathways being most common in <i>Dolichospermum</i> and <i>Aphanizomenon</i> strains. We detected the production of porphyra-334 and shinorine, two widely reported family members, in <i>Dolichospermum</i> strains isolated from the Gulf of Finland's surface layer. The estimated content of porphyra-334 in <i>Dolichospermum</i> sp. UHCC 0684 was 7.4 mg per gram dry weight. Our results suggest that bloom-forming cyanobacteria could be a potential source of these compounds for cosmetic and biotechnological applications and may play a significant role in cyanobacterial bloom formation.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11738650/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142996972","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}
Wojciech Pijanowski, Sebastian Chmielewski, Wojciech Wysoczański, Polina Havrysh, Katarzyna Turnau, Marlena Lembicz
{"title":"Beauveria felina Accelerates Growth When Competing With Other Potential Endophytes","authors":"Wojciech Pijanowski, Sebastian Chmielewski, Wojciech Wysoczański, Polina Havrysh, Katarzyna Turnau, Marlena Lembicz","doi":"10.1111/1758-2229.70067","DOIUrl":"10.1111/1758-2229.70067","url":null,"abstract":"<p>The fungus <i>Beauveria felina</i> is often classified as one of the so-called good biocontrol agents. However, no information is available about the growth of this entomopathogenic fungus in the presence of other endophytic fungi, which are usually found in plant tissues. Effects of fungal interactions vary from inhibiting the activity of a biocontrol agent to stimulating its effect on the targeted pathogen. This study compared the growth rate of <i>Beauveria felina</i> alone and in interaction with other endophytic fungi. In the presence of each competitor (<i>Gliomastix polychroma</i> or <i>Rhodotorula mucilaginosa</i>), <i>B. felina</i> grew faster than in the control. In the interaction between <i>Beauveria felina</i> and <i>Gliomastix polychroma</i>, an inhibition zone was formed between their mycelia. This is the first report showing the response of its mycelium to biotic stress caused by the presence of other fungi.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736628/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142996933","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}
Ronnie Mooney, Kiri Rodgers, Sandro Carnicelli, Matías E. Carnevale, Maria Eugenia Farias, Fiona L. Henriquez
{"title":"Isolation of Acanthamoeba Species and Bacterial Symbiont Variability in Puna Salt Plains, Argentina","authors":"Ronnie Mooney, Kiri Rodgers, Sandro Carnicelli, Matías E. Carnevale, Maria Eugenia Farias, Fiona L. Henriquez","doi":"10.1111/1758-2229.70059","DOIUrl":"10.1111/1758-2229.70059","url":null,"abstract":"<p><i>Acanthamoeba</i> spp. are widespread protists that feed on bacteria via phagocytosis. This predation pressure has led many bacteria to evolve strategies to resist and survive inside these protists. The impact of this is not well understood, but it may limit detection and allow survival in extreme environments. Three sites in the Puna salt plains, Catamarca province, Argentina, were sampled for <i>Acanthamoeba</i> spp., verified using PCR and Sanger sequencing. The intracellular microbiome was analysed with 16S rRNA gene sequencing and compared to the overall site microbiome. <i>Acanthamoeba</i> were found at all locations, and their intracellular microbiome was similar across samples but differed from the overall site microbiome. <i>Pseudomonas</i> spp., a clinically relevant genus, was most abundant in all isolates. This study suggests <i>Acanthamoeba</i> can protect bacteria, aiding their detection avoidance and survival in harsh conditions.</p>","PeriodicalId":163,"journal":{"name":"Environmental Microbiology Reports","volume":"17 1","pages":""},"PeriodicalIF":3.6,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11733093/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142982042","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}