{"title":"Genome-wide differentiation corresponds to climatic niches in two species of lichen-forming fungi","authors":"Edgar L. Y. Wong, Henrique F. Valim, Imke Schmitt","doi":"10.1111/1462-2920.16703","DOIUrl":"10.1111/1462-2920.16703","url":null,"abstract":"<p>Lichens can withstand fluctuating environmental conditions such as hydration-desiccation cycles. Many species distribute across climate zones, suggesting population-level adaptations to conditions such as freezing and drought. Here, we aim to understand how climate affects population genomic patterns in lichenized fungi. We analysed population structure along elevational gradients in closely related <i>Umbilicaria phaea</i> (North American; two gradients) and <i>Umbilicaria pustulata</i> (European; three gradients). All gradients showed clear genomic breaks splitting populations into low-elevation (Mediterranean zone) and high-elevation (cold temperate zone). A total of 3301 SNPs in <i>U. phaea</i> and 138 SNPs in <i>U. pustulata</i> were driven to fixation between the two ends of the gradients. The difference between the species is likely due to differences in recombination rate: the sexually reproducing <i>U. phaea</i> has a higher recombination rate than the primarily asexually reproducing <i>U. pustulata</i>. Cline analysis revealed allele frequency transitions along all gradients at approximately 0°C, coinciding with the transition between the Mediterranean and cold temperate zones, suggesting freezing is a strong driver of population differentiation. Genomic scans further confirmed temperature-related selection targets. Both species showed similar differentiation patterns overall, but different selected alleles indicate convergent adaptation to freezing. Our results enrich our knowledge of fungal genomic functions related to temperature and climate, fungal population genomics, and species responses to environmental heterogeneity.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16703","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142398506","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}
Dan Zheng, Britt-Marie Wilén, Ola Öberg, Torsten Wik, Oskar Modin
{"title":"Metagenomics reveal the potential for geosmin and 2-methylisoborneol production across multiple bacterial phyla in recirculating aquaculture systems","authors":"Dan Zheng, Britt-Marie Wilén, Ola Öberg, Torsten Wik, Oskar Modin","doi":"10.1111/1462-2920.16696","DOIUrl":"10.1111/1462-2920.16696","url":null,"abstract":"<p>Geosmin and 2-methylisoborneol (MIB) are known to cause taste-and-odour problems in recirculating aquaculture systems (RAS). Both geosmin and MIB are microbial metabolites belonging to terpenoids. Precursors for terpenoids are biosynthesized via the methylerythritol phosphate (MEP) and the mevalonate (MVA) pathways. We carried out a metagenomic analysis of 50 samples from five RAS to investigate terpenoid biosynthesis and metabolic potential for geosmin and MIB production in RAS microbiomes. A total of 1008 metagenome-assembled genomes (MAGs) representing 26 bacterial and three archaeal phyla were recovered. Although most archaea are thought to use the MVA pathway for terpenoid precursor biosynthesis, an <i>Iainarchaeota</i> archaeal MAG is shown to harbour a complete set of genes encoding the MEP pathway but lacking genes associated with the MVA pathway. In this study, a total of 16 MAGs affiliated with five bacterial phyla (<i>Acidobacteriota</i>, <i>Actinobacteriota</i>, <i>Bacteroidota</i>, <i>Chloroflexota</i>, and <i>Myxococcota</i>) were identified as possessing potential geosmin or MIB synthases. These putative taste and odour producers were diverse, many were taxonomically unidentified at the genus or species level, and their relative abundance differed between the investigated RAS farms. The metagenomic study of the RAS microbiomes revealed a previously unknown phylogenetic diversity of the potential to produce geosmin and MIB.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16696","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142385436","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}
Adeline Loyau, Rayan Bouchali, Hugo Sentenac, Dirk S. Schmeller
{"title":"The commensal skin microbiome of amphibian mountain populations and its association with the pathogen Batrachochytrium dendrobatidis","authors":"Adeline Loyau, Rayan Bouchali, Hugo Sentenac, Dirk S. Schmeller","doi":"10.1111/1462-2920.16699","DOIUrl":"10.1111/1462-2920.16699","url":null,"abstract":"<p>Microbial assemblages naturally living on the skin are an integral part of immunity. In amphibians, this skin microbiota may hold a mitigation solution against the fungal pathogen <i>Batrachochytrium dendrobatidis</i> (Bd), which causes the panzootic disease chytridiomycosis. We used 16S rRNA gene metabarcoding to test the adaptive microbiome hypothesis. We compared the community composition, richness, and putative Bd-inhibitory function of the skin microbiome of three amphibian host species in the Pyrenees, as well as three species in Taiwan, in both Bd-positive and negative mountain populations. In both geographical regions, the amphibian host species played a decisive role in shaping the microbial assemblage and putative anti-Bd properties. In the Pyrenees, the species most susceptible to chytridiomycosis, <i>Alytes obstetricans</i>, had the lowest relative abundances of putative protective bacteria. In Bd-positive and negative sites, individuals had different skin microbiomes, with all anuran species showing increased relative abundances of potential anti-Bd bacteria, while the Taiwanese caudata <i>Hynobius sonani</i> showed the opposite pattern. Our results suggest that, in response to exposure to the pathogen, the skin microbiota shifted to a defensive state with increased anti-Bd function, which may contribute to promoting disease resistance, as proposed by the adaptive microbiome hypothesis.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16699","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384368","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}
Yanhui Kong, Rui Zhang, Stéphane Blain, Ingrid Obernosterer
{"title":"Seasonal dynamics in microbial trace metals transporters during phytoplankton blooms in the Southern Ocean","authors":"Yanhui Kong, Rui Zhang, Stéphane Blain, Ingrid Obernosterer","doi":"10.1111/1462-2920.16695","DOIUrl":"10.1111/1462-2920.16695","url":null,"abstract":"<p>Trace metals are required as cofactors in metalloproteins that are essential in microbial metabolism and growth. The microbial requirements of diverse metals and the capabilities of prokaryotic taxa to acquire these metals remain poorly understood. We present here results from metagenomic observations over an entire productive season in the region off Kerguelen Island (Indian Sector of the Southern Ocean). We observed seasonal patterns in the abundance of prokaryotic transporters of seven trace elements (zinc [Zn], manganese [Mn], nickel [Ni], molybdenum [Mo], tungsten [W], copper [Cu] and cobalt [Co]) and the consecutive spring and summer phytoplankton blooms were strong drivers of these temporal trends. Taxonomic affiliation of the functional genes revealed that <i>Rhodobacteraceae</i> had a broad repertoire of trace metal transporters (Mn, Zn, Ni, W and Mo) and a more restricted set was observed for other prokaryotic groups, such as <i>Flavobacteriaceae</i> (Zn), <i>Nitrincolaceae</i> (Ni and W) and <i>Thioglobaceae</i> (Mo). The prevalence of trace metal transporters within a prokaryotic group, as determined on the family level, was overall confirmed in representative metagenome-assembled genomes. We discuss the potential involvement of prokaryotic groups in processes related to organic matter utilisation that require these metals and the consequences on carbon and trace metal cycling in surface waters of the Southern Ocean.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16695","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142375299","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}
Xinyue Gu, Perran A. Ross, Qiong Yang, Alex Gill, Paul A. Umina, Ary A. Hoffmann
{"title":"Influence of genetic and environmental factors on the success of endosymbiont transfers in pest aphids","authors":"Xinyue Gu, Perran A. Ross, Qiong Yang, Alex Gill, Paul A. Umina, Ary A. Hoffmann","doi":"10.1111/1462-2920.16704","DOIUrl":"10.1111/1462-2920.16704","url":null,"abstract":"<p>There is increasing interest in exploring how endosymbionts could be useful in pest control, including in aphids, which can carry a diversity of endosymbionts. Endosymbionts often have a large impact on host traits, and their presence can be self-sustaining. Identifying useful host-endosymbiont combinations for pest control is facilitated by the transfer of specific endosymbionts into target species, particularly if the species lacks the endosymbiont. Here, we complete a comprehensive literature review, which included 56 relevant papers on endosymbiont transfer experiments in aphids, to uncover factors that might influence transfer success. We then report on our own microinjection attempts of diverse facultative endosymbionts from a range of donor species into three agriculturally important aphid species as recipients: the green peach aphid (<i>Myzus persicae</i>), bird cherry-oat aphid (<i>Rhopalosiphum padi</i>), and Russian wheat aphid (<i>Diuraphis noxia</i>). Combining this information, we consider reasons that impact the successful establishment of lines carrying transferred endosymbionts. These include a lack of stability in donors, deleterious effects on host fitness, the absence of plant-based (versus vertical) transmission, high genetic variation in the endosymbiont, and susceptibility of an infection to environmental factors. Taking these factors into account should help in increasing success rates in future introductions.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-10-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16704","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142364919","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}
Chao Zhong, Anhuai Lu, Hailiang Dong, Shan Huang, Liang Shi, Yanan Shen, Yangjian Cheng, Yiran Dong, Xiangzhen Li, Jie Xu, Jinren Ni, Michael F. Hochella Jr, Juan Liu
{"title":"Photoelectron-promoted metabolism of sulphate-reducing microorganisms in substrate-depleted environments","authors":"Chao Zhong, Anhuai Lu, Hailiang Dong, Shan Huang, Liang Shi, Yanan Shen, Yangjian Cheng, Yiran Dong, Xiangzhen Li, Jie Xu, Jinren Ni, Michael F. Hochella Jr, Juan Liu","doi":"10.1111/1462-2920.16683","DOIUrl":"10.1111/1462-2920.16683","url":null,"abstract":"<p>Sulphate-reducing microorganisms, or SRMs, are crucial to organic decomposition, the sulphur cycle, and the formation of pyrite. Despite their low energy-yielding metabolism and intense competition with other microorganisms, their ability to thrive in natural habitats often lacking sufficient substrates remains an enigma. This study delves into how <i>Desulfovibrio desulfuricans</i> G20, a representative SRM, utilizes photoelectrons from extracellular sphalerite (ZnS), a semiconducting mineral that often coexists with SRMs, for its metabolism and energy production. Batch experiments with sphalerite reveal that the initial rate and extent of sulphate reduction by G20 increased by 3.6 and 3.2 times respectively under light conditions compared to darkness, when lactate was not added. Analyses of microbial photoelectrochemical, transcriptomic, and metabolomic data suggest that in the absence of lactate, G20 extracts photoelectrons from extracellular sphalerite through cytochromes, nanowires, and electron shuttles. Genes encoding movement and biofilm formation are upregulated, suggesting that G20 might sense redox potential gradients and migrate towards sphalerite to acquire photoelectrons. This process enhances the intracellular electron transfer activity, sulphur metabolism, and ATP production of G20, which becomes dominant under conditions of carbon starvation and extends cell viability in such environments. This mechanism could be a vital strategy for SRMs to survive in energy-limited environments and contribute to sulphur cycling.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142344046","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}
Hee-Jeong Cha, Dominic J. Glover, Douglas S. Clark
{"title":"The filamentous γ-prefoldin chaperone is not essential for growth and thermal adaptation in Methanocaldococcus jannaschii","authors":"Hee-Jeong Cha, Dominic J. Glover, Douglas S. Clark","doi":"10.1111/1462-2920.16705","DOIUrl":"10.1111/1462-2920.16705","url":null,"abstract":"<p>Elucidating the role of molecular chaperones in extremely thermophilic archaea, including the gamma prefoldin (γPFD) in the deep-sea methanogen <i>Methanocaldococcus jannaschii</i>, is integral to understanding microbial adaptation to hot environments. This study focuses on genetically engineered knock-out and overexpression strains to evaluate the importance of γPFD in the growth and thermal tolerance of <i>M. jannaschii</i>. An in-depth analysis of cell growth, morphology and transcriptional responses to heat stress revealed that although the gene encoding γPFD is substantially upregulated in response to heat shock, the γPFD is not indispensable for high-temperature survival. Instead, its absence in the knock-out strain is compensated for by the upregulation of several proteolytic proteins in the absence of heat shock, nearly matching the corresponding transcription profile of selected transcripts for proteins involved in protein synthesis and folding in the wild-type strain following heat shock, using quantitative reverse-transcription PCR (RT-qPCR). These findings bridge environmental adaptation with molecular biology, underscoring the versatility of extremophiles and providing a deeper mechanistic understanding of how they cope with stress.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16705","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142344047","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}
Xinming Xu, Adele Pioppi, Heiko T. Kiesewalter, Mikael Lenz Strube, Ákos T. Kovács
{"title":"Disentangling the factors defining Bacillus subtilis group species abundance in natural soils","authors":"Xinming Xu, Adele Pioppi, Heiko T. Kiesewalter, Mikael Lenz Strube, Ákos T. Kovács","doi":"10.1111/1462-2920.16693","DOIUrl":"10.1111/1462-2920.16693","url":null,"abstract":"<p><i>Bacillus subtilis</i> is ubiquitously and broadly distributed in various environments but is mostly isolated from soil. Given that <i>B. subtilis</i> is known as a plant growth-promoting rhizobacterium in agriculture, we aimed to describe the natural distribution of this species and uncover how biotic and abiotic factors affect its distribution. When comparing different soils, we discovered that <i>B. subtilis</i> group species are most abundant in grasslands but can rarely be isolated from forest soil, even if the soil sample sites are situated in proximity. Differential analysis revealed that spore-forming bacteria exhibited enrichments in the grassland, suggesting niche overlap or synergistic interactions leading to the proliferation of certain <i>Bacillus</i> species in grassland environments. Network analysis further revealed that <i>Bacillus</i> and other <i>Bacillota</i> established a densely interconnected hub module in the grassland, characterised by positive associations indicating co-occurrence, a pattern not observed in the forest soil. Speculating that this difference was driven by abiotic factors, we combined amplicon sequencing with physico-chemical analysis of soil samples and found multiple chemical variables, mainly pH, to affect microbial composition. Our study pinpoints the factors that influence <i>B. subtilis</i> abundance in natural soils and, therefore, offers insights for designing <i>B. subtilis</i>-based biocontrol products in agricultural settings.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16693","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142321865","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}
Jason D. Selwyn, Brecia A. Despard, Miles V. Vollmer, Emily C. Trytten, Steven V. Vollmer
{"title":"Identification of putative coral pathogens in endangered Caribbean staghorn coral using machine learning","authors":"Jason D. Selwyn, Brecia A. Despard, Miles V. Vollmer, Emily C. Trytten, Steven V. Vollmer","doi":"10.1111/1462-2920.16700","DOIUrl":"10.1111/1462-2920.16700","url":null,"abstract":"<p>Coral diseases contribute to the rapid decline in coral reefs worldwide, and yet coral bacterial pathogens have proved difficult to identify because 16S rRNA gene surveys typically identify tens to hundreds of disease-associate bacteria as putative pathogens. An example is white band disease (WBD), which has killed up to 95% of the now-endangered Caribbean <i>Acropora</i> corals since 1979, yet the pathogen is still unknown. The 16S rRNA gene surveys have identified hundreds of WBD-associated bacterial amplicon sequencing variants (ASVs) from at least nine bacterial families with little consensus across studies. We conducted a multi-year, multi-site 16S rRNA gene sequencing comparison of 269 healthy and 143 WBD-infected <i>Acropora cervicornis</i> and used machine learning modelling to accurately predict disease outcomes and identify the top ASVs contributing to disease. Our ensemble ML models accurately predicted disease with greater than 97% accuracy and identified 19 disease-associated ASVs and five healthy-associated ASVs that were consistently differentially abundant across sampling periods. Using a tank-based transmission experiment, we tested whether the 19 disease-associated ASVs met the assumption of a pathogen and identified two pathogenic candidate ASVs—ASV25 <i>Cysteiniphilum litorale</i> and ASV8 <i>Vibrio</i> sp. to target for future isolation, cultivation, and confirmation of Henle-Koch's postulate via transmission assays.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1462-2920.16700","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142237019","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}
Jordyn D. Proctor, Virginija Mackevicius-Dubickaja, Yuval Gottlieb, Jennifer A. White
{"title":"Warm temperature inhibits cytoplasmic incompatibility induced by endosymbiotic Rickettsiella in spider hosts","authors":"Jordyn D. Proctor, Virginija Mackevicius-Dubickaja, Yuval Gottlieb, Jennifer A. White","doi":"10.1111/1462-2920.16697","DOIUrl":"10.1111/1462-2920.16697","url":null,"abstract":"<p>Bacterial endosymbionts manipulate reproduction in arthropods to increase their prevalence in the host population. One such manipulation is cytoplasmic incompatibility (CI), wherein the bacteria sabotage sperm in infected males to reduce the hatch rate when mated with uninfected females, but zygotes are ‘rescued’ when that male mates with an infected female. In the spider <i>Mermessus fradeorum</i> (Linyphiidae), <i>Rickettsiella</i> symbionts cause variable levels of CI. We hypothesised that temperature affects the strength of CI and its rescue in <i>M. fradeorum</i>, potentially mediated by bacterial titre. We reared <i>Rickettsiella</i>-infected spiders in two temperature conditions (26°C vs. 20°C) and tested CI induction in males and rescue in females. In incompatible crosses between infected males and uninfected females, the hatch rate from warm males was doubled (mean ± standard error = 0.687 ± 0.052) relative to cool males (0.348 ± 0.046), indicating that CI induction is weaker in warm males. In rescue crosses between infected females and infected males, female rearing temperature had a marginal effect on CI rescue, but the hatch rate remained high for both warm (0.960 ± 0.023) and cool females (0.994 ± 0.004). Bacterial titre, as measured by quantitative polymerase chain reaction, was lower in warm than cool spiders, particularly in females, suggesting that bacterial titre may play a role in causing the temperature-mediated changes in CI.</p>","PeriodicalId":11898,"journal":{"name":"Environmental microbiology","volume":null,"pages":null},"PeriodicalIF":4.3,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142160998","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}