Chloe A Fouilloux, Eric Neeno-Eckwall, Ipsita Srinivas, Jonathan S Compton, Josh Sampson, Jesse Weber, Cole Wolf, Amanda Hund, John Berini, Heather Alexander, Emma Choi, Daniel I Bolnick, Jessica L Hite
{"title":"Needle in a Haystack: A Droplet Digital Polymerase Chain Reaction Assay to Detect Rare Helminth Parasites Infecting Natural Host Populations.","authors":"Chloe A Fouilloux, Eric Neeno-Eckwall, Ipsita Srinivas, Jonathan S Compton, Josh Sampson, Jesse Weber, Cole Wolf, Amanda Hund, John Berini, Heather Alexander, Emma Choi, Daniel I Bolnick, Jessica L Hite","doi":"10.1111/1755-0998.14131","DOIUrl":"https://doi.org/10.1111/1755-0998.14131","url":null,"abstract":"<p><p>Helminths infect humans, livestock, and wildlife, yet remain understudied despite their significant impact on public health and agriculture. Because many of the most prevalent helminth-borne diseases are zoonotic, understanding helminth transmission among wildlife could improve predictions and management of infection risks across species. A key challenge to understanding helminth transmission dynamics in wildlife is accurately and quantitatively tracking parasite load across hosts and environments. Traditional methods, such as visual parasite identification from environmental samples or infected hosts, are time-consuming, while standard molecular techniques (e.g., PCR and qPCR) often lack the sensitivity to reliably detect lower parasite burdens. These limitations can underestimate the prevalence and severity of infection, hindering efforts to manage infectious diseases. Here, we developed a multiplexed droplet digital PCR (ddPCR) assay to quantify helminth loads in aquatic habitats using 18S rRNA target genes. Using Schistocephalus solidus and their copepod hosts as a case study, we demonstrate ddPCR's sensitivity and precision. The assay is highly reproducible, reliably detecting target genes at concentrations as low as 1 pg of DNA in lab standards and field samples (multi-species and eDNA). Thus, we provide a toolkit for quantifying parasite load in intermediate hosts and monitoring infection dynamics across spatio-temporal scales in multiple helminth systems of concern for public health, agriculture, and conservation biology.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14131"},"PeriodicalIF":5.5,"publicationDate":"2025-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144264957","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Heroen Verbruggen, Kavitha Uthanumallian, Felix Powrie, Tara Jalali, Chiela Cremen, Maren Preuss, Sebastian Duchene, Pilar Diaz-Tapia
{"title":"Scaling Up Species Delimitation From DNA Barcodes to Whole Organelle Genomes: Strong Evidence for Discordance Among Genes and Methods for the Red Alga Dasyclonium.","authors":"Heroen Verbruggen, Kavitha Uthanumallian, Felix Powrie, Tara Jalali, Chiela Cremen, Maren Preuss, Sebastian Duchene, Pilar Diaz-Tapia","doi":"10.1111/1755-0998.14132","DOIUrl":"https://doi.org/10.1111/1755-0998.14132","url":null,"abstract":"<p><p>Molecular sequence data have become a ubiquitous tool for delimiting species and are particularly important in organisms where morphological traits are not informative about species boundaries. A range of statistical methods have been developed to derive species limits from molecular data, for example, by quantifying changes in branching patterns in phylogenetic trees. We aim to investigate how such methods scale up from single genes to whole organelle genomes. We gathered chloroplast genome data from 38 samples of the red algal genus Dascyclonium and analysed them with the popular species delimitation methods Assemble Species by Automatic Partitioning (ASAP), General Mixed Yule Coalescent (GMYC), and Poisson Tree Processes (PTP). We show extensive variation in inferred species boundaries depending on the method and dataset used. Genome-scale analyses differed substantially between methods, with ASAP predicting the fewest species, PTP intermediate, and GMYC inferring many species. Based on a series of simulations, we identify a tendency of GMYC to overestimate species numbers as alignments increase in length, while the other two methods are not sensitive to this scaling. Gene-by-gene analyses show strong differences in predicted species limits, which is unexpected seeing that all genes are on a single uniparentally inherited chromosome, and highlight that choosing a particular gene as a DNA barcode has significant consequences for species diversity estimates. We show extensive cryptic diversity in the genus Dasyclonium and propose a consensus solution for species limits based on our combined results, enriched with biogeographic and morphological interpretations. Finally, we make recommendations for interpreting the results and improving the inferences drawn from species delimitation methods.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14132"},"PeriodicalIF":5.5,"publicationDate":"2025-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144256984","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sophie von der Heyden, Luciano B. Beheregaray, Sarah Fitzpatrick, Catherine E. Grueber, Yibo Hu, Alison G. Nazareno
{"title":"Advancing Species Conservation and Management Through Omics Tools","authors":"Sophie von der Heyden, Luciano B. Beheregaray, Sarah Fitzpatrick, Catherine E. Grueber, Yibo Hu, Alison G. Nazareno","doi":"10.1111/1755-0998.14123","DOIUrl":"https://doi.org/10.1111/1755-0998.14123","url":null,"abstract":"<p>The conservation of biological resources has become a priority worldwide, exacerbated by the negative effects of a growing human population and related impacts on the structure, function and composition of ecosystems. A plethora of species and populations across terrestrial, freshwater and marine environments are experiencing reductions in population sizes, some of which are more susceptible to demographic and genetic stochasticity than others (Exposito-Alonso et al. <span>2022</span>). The era of omics has inspired thought-provoking possibilities in the field of conservation biology. Access to and application of large-scale omics datasets (e.g., genomics, epigenomics, transcriptomics, proteomics, metabolomics, metagenomics) can shed novel insights on and resolve aspects of wildlife species biology and demography relevant to conservation assessments, management actions and monitoring (Allendorf et al. <span>2010</span>; Schweizer et al. <span>2021</span>; Zamudio <span>2023</span>). The compilation and analysis of omics datasets can also inform management strategies for threatened wild and captive populations by, for example, identifying genetically vulnerable populations, adaptive loci, or uncovering interactions between host and symbiotic microbiota. These approaches contribute to a better understanding of local adaptation, introgression, inbreeding depression and genetic mechanisms of disease susceptibility and resistance. To this extent, the use of omics data to maximise effective actions for conservation and management is critical, particularly for species on the verge of extinction.</p><p>Halting climate change and the ongoing anthropogenic pressures that impact biodiversity is mandatory to curb the extinction crisis, but the loss of species and populations requires additional novel approaches for their conservation and management. To this end, the Special Issue ‘Advancing species conservation and management through omics tools’ was launched to bring attention to scientists interested in demonstrating how innovative techniques are useful to safeguard and manage biodiversity. In this editorial, we highlight how omics tools can help preserve biological diversity across space and time and across a wide range of biodiversity, encompassing authors from across the globe (Figure 1). Topics in this Special Issue include conservation surveys using genomics, epigenomics, metagenomics, transcriptomics, the development of computational models, novel pipelines related to best practices for sampling design and wet lab procedures, as well as genomic resources for wildlife species and their applicability to guide conservation and management strategies. Overall, our special issue provides a timely collection of research across broad themes that expand the application of omics tools across the tree of life. In doing so, we not only showcase contemporary development of the field but also provide an opportunity for engagement with stakeholders interested in","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":"25 5","pages":""},"PeriodicalIF":5.5,"publicationDate":"2025-06-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/1755-0998.14123","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144220414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Coralie Rousseau, Nicolas Henry, Sylvie Rousvoal, Gwenn Tanguy, Erwan Legeay, Catherine Leblanc, Simon M Dittami
{"title":"A Practical Comparison of Short- and Long-Read Metabarcoding Sequencing: Challenges and Solutions for Plastid Read Removal and Microbial Community Exploration of Seaweed Samples.","authors":"Coralie Rousseau, Nicolas Henry, Sylvie Rousvoal, Gwenn Tanguy, Erwan Legeay, Catherine Leblanc, Simon M Dittami","doi":"10.1111/1755-0998.14129","DOIUrl":"https://doi.org/10.1111/1755-0998.14129","url":null,"abstract":"<p><p>Short-read metabarcoding analysis is the gold standard for accessing partial 16S and ITS genes with high read quality. With the advent of long-read sequencing, the amplification of full-length target genes is possible, but with low read accuracy. Moreover, 16S rRNA gene amplification in seaweed results in a large proportion of plastid reads, which are directly or indirectly derived from cyanobacteria. Primers designed not to amplify plastid sequences are available for short-read sequencing, while Oxford Nanopore Technology (ONT) offers adaptive sampling, a unique way to remove reads in real time. In this study, we compare three options to address the issue of plastid reads: deleting plastid reads with adaptive sampling, using optimised primers with Illumina MiSeq technology, and sequencing large numbers of reads with Illumina NovaSeq technology with universal primers. We show that adaptive sampling using the default settings of the MinKNOW software was ineffective for plastid depletion. NovaSeq sequencing with universal primers stood out with its deep coverage, low error rate, and ability to include both eukaryotes and bacteria in the same sequencing run, but it had limitations regarding the identification of fungi. The ONT sequencing helped us explore the fungal diversity and allowed for the retrieval of taxonomic information for genera poorly represented in the sequence databases. We also demonstrated with a mock community that the SAMBA workflow provided more accurate taxonomic assignment at the bacterial genus level than the IDTAXA and KRAKEN2 pipelines, but many false positives were generated at the species level.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14129"},"PeriodicalIF":5.5,"publicationDate":"2025-06-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144214415","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ayke Haller, Judith Risse, Bernice Sepers, Kees van Oers
{"title":"Independent Avian Epigenetic Clocks for Ageing and Development.","authors":"Ayke Haller, Judith Risse, Bernice Sepers, Kees van Oers","doi":"10.1111/1755-0998.14128","DOIUrl":"https://doi.org/10.1111/1755-0998.14128","url":null,"abstract":"<p><p>Information on individual age is a fundamental aspect in many ecological and evolutionary studies. However, accurate and non-lethal methods that can be applied to estimate the age of wild animals are often absent. Furthermore, since the process of ageing is accompanied by a physical decline and the deterioration of biological functions, the biological age often deviates from the chronological age. Epigenetic marks are widely suggested to be associated with this age-related physical decline, and especially changes in DNA methylation are suggested to be reliable age-predictive biomarkers. Here, we developed separate epigenetic clocks for ageing and development in a small passerine bird, the great tit (Parus major). The ageing clock was constructed and evaluated using erythrocyte DNA methylation data of 122 post-fledging individuals, and the developmental clock using 67 pre-fledging individuals from a wild population. Using a leave-one-out cross-validation approach, we were able to accurately predict the ages of individuals with median absolute deviations of 0.40 years for the ageing and 1.06 days for the development clock. Moreover, using existing data from a brood-size manipulation, we show that nestlings from reduced broods are estimated to be biologically older compared to control nestlings, while they are expected to have higher fitness. These epigenetic clocks provide further evidence that, as observed in mammals, changes in DNA methylation of certain CpG sites are highly correlated with chronological age in birds and this opens up new avenues for broad applications in behavioural and evolutionary ecology.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14128"},"PeriodicalIF":5.5,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144207288","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mathilde Borg Dahl, Stella Brachmann, Andrea Söllinger, Marina Schnell, Laureen Ahlers, Magdalena Wutkowska, Katharina J Hoff, Neetika Nath, Verena Groß, Haitao Wang, Micha Weil, Marc Piecha, Marc Schaffer, Corinna Jensen, Andreas W Kuss, Christoph Gall, Erika Wimmer, Thomas Pribasnig, Alexander Tøsdal Tveit, Bjarni D Sigurdsson, Christa Schleper, Andreas Richter, Tim Urich
{"title":"Quantifying Soil Microbiome Abundance by Metatranscriptomics and Complementary Molecular Techniques-Cross-Validation and Perspectives.","authors":"Mathilde Borg Dahl, Stella Brachmann, Andrea Söllinger, Marina Schnell, Laureen Ahlers, Magdalena Wutkowska, Katharina J Hoff, Neetika Nath, Verena Groß, Haitao Wang, Micha Weil, Marc Piecha, Marc Schaffer, Corinna Jensen, Andreas W Kuss, Christoph Gall, Erika Wimmer, Thomas Pribasnig, Alexander Tøsdal Tveit, Bjarni D Sigurdsson, Christa Schleper, Andreas Richter, Tim Urich","doi":"10.1111/1755-0998.14130","DOIUrl":"https://doi.org/10.1111/1755-0998.14130","url":null,"abstract":"<p><p>Linking meta-omics and biogeochemistry approaches in soils has remained challenging. This study evaluates the use of an internal RNA extraction standard and its potential for making quantitative estimates of a given microbial community size (biomass) in soil metatranscriptomics. We evaluate commonly used laboratory protocols for RNA processing, metatranscriptomic sequencing and quantitative reverse transcription polymerase chain reaction (qRT-PCR). Metatranscriptomic profiles from soil samples were generated using two library preparation protocols and prepared in triplicates. RNA extracted from pure cultures of Saccharolobus solfataricus was added to the samples as an internal nucleic acid extraction standard (NAE<sub>std</sub>). RNA reads originating from NAE<sub>std</sub> were identified with a 99.9% accuracy. A remarkable replication consistency between triplicates was seen (average Bray-Curtis dissimilarity 0.03 ± 0.02), in addition to a clear library preparation bias. Nevertheless, the between-sample pattern was not affected by library type. Estimates of 16S rRNA transcript abundance derived from qRT-PCR experiments, NAE<sub>std</sub> and a previously published quantification method of metatranscriptomics (hereafter qMeTra) were compared with microbial biomass carbon (MBC) and nitrogen (MBN) extracts. The derived biomass estimates differed by orders of magnitude. While most estimates were significantly correlated with each other, no correlation was observed between NAE<sub>std</sub> and MBC extracts. We discuss how simultaneous changes in community size and the soils nucleic acid retention strength might hamper accurate biomass estimation. Adding NAE<sub>std</sub> has the potential to shed important light on nucleic acid retention in the substance matrix (e.g., soil) during extraction.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14130"},"PeriodicalIF":5.5,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144207218","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Samantha S Fontaine, Stevie R Kennedy-Gold, Kurt J Regester, Jennifer A Sheridan, Kevin D Kohl
{"title":"The Impact of Whole-Animal Fluid Preservation on the Observed Gut Microbiome of Vertebrates: Implications for the Use of Museum Specimens in Microbiome Research.","authors":"Samantha S Fontaine, Stevie R Kennedy-Gold, Kurt J Regester, Jennifer A Sheridan, Kevin D Kohl","doi":"10.1111/1755-0998.14127","DOIUrl":"https://doi.org/10.1111/1755-0998.14127","url":null,"abstract":"<p><p>The vertebrate gut houses diverse microbial communities that provide insights into their host's ecological and evolutionary histories. Nevertheless, microbiome research has not been distributed equally across host taxonomy, geography and timescales. The millions of fluid-preserved specimens stored in natural history museums worldwide represent a potentially untapped resource for microbiome information. However, it is unknown how fluid preservation and long-term storage change the composition and diversity of the original microbial community across a variety of host taxa. Here, we present the largest study to date aimed at addressing this question. Specifically, we identified an optimal method for extracting DNA from preserved samples using commercially available kits. Next, for 11 host species representing four vertebrate classes, we compared the gut microbiomes between animals dissected freshly and those collected simultaneously but subsequently fixed in formalin and stored in 70% ethanol for 1 year, similar to museum conditions. In a secondary analysis in amphibians, we compared our collected samples with those from decades-old historical museum specimens. We found that while fluid preservation altered the community composition and reduced the diversity of the recovered microbiome inventories, host species identity predominated in shaping the gut microbiome, and differences across species and geographic localities were retained after preservation. Historical specimens had microbiomes that were the most different from fresh specimens, suggesting that over time, changes in the microbiome of populations have occurred, or preservation effects have compounded. Considering these findings, we discuss the potential for use of fluid-preserved museum specimens in future microbiome studies.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14127"},"PeriodicalIF":5.5,"publicationDate":"2025-05-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144140953","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Ancient Microbiomes as Mirrored by DNA Extracted From Century-Old Herbarium Plants and Associated Soil.","authors":"Gianluca Grasso, Régis Debruyne, Martino Adamo, Olivier Rué, Franck Lejzerowicz, Lucie Bittner, Valeria Bianciotto, Roland Marmeisse","doi":"10.1111/1755-0998.14122","DOIUrl":"https://doi.org/10.1111/1755-0998.14122","url":null,"abstract":"<p><p>Numerous specimens stored in natural history collections have been involuntarily preserved together with their associated microbiomes. We propose exploiting century-old soils occasionally found on the roots of herbarium plants to assess the diversity of ancient soil microbial communities originally associated with these plants. We extracted total DNA and sequenced libraries produced from rhizospheric soils and roots of four plants preserved in herbaria for more than 120 years in order to characterise the preservation and taxonomic diversity that can be recovered in such contexts. Extracted DNA displayed typical features of ancient DNA, with cytosine deamination at the ends of fragments predominantly shorter than 50 bp. When compared to extant microbiomes, herbarium microbial communities clustered with soil communities and were distinct from communities from other environments. Herbarium communities also displayed biodiversity features and assembly rules typical of soil and plant-associated ones. Soil communities were richer than root-associated ones with which they shared most taxa. Regarding community turnover, we detected collection site, soil versus root and plant species effects. Eukaryotic taxa that displayed a higher abundance in roots were mostly plant pathogens that were not identified among soil-enriched ones. Conservation of these biodiversity features and assembly rules in herbarium-associated microbial communities indicates that herbarium-extracted DNA might reflect the composition of the original plant-associated microbial communities and that preservation in herbaria seemingly did not dramatically alter these characteristics. Using this approach, it should be possible to investigate historical soils and herbarium plant roots to explore the diversity and temporal dynamics of soil microbial communities.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14122"},"PeriodicalIF":5.5,"publicationDate":"2025-05-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144136121","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Martijn Callens, Guillaume Le Berre, Laure Van den Bulcke, Marianne Lolivier, Sofie Derycke
{"title":"An Accessible Metagenomic Strategy Allows for Better Characterisation of Invertebrate Bulk Samples.","authors":"Martijn Callens, Guillaume Le Berre, Laure Van den Bulcke, Marianne Lolivier, Sofie Derycke","doi":"10.1111/1755-0998.14126","DOIUrl":"https://doi.org/10.1111/1755-0998.14126","url":null,"abstract":"<p><p>DNA-based techniques are a popular approach for assessing biodiversity in ecological research, especially for organisms which are difficult to detect or identify morphologically. Metabarcoding, the most established method for determining species composition and relative abundance in bulk samples, can be more sensitive and time- and cost-effective than traditional morphological approaches. However, one drawback of this method is PCR bias caused by between-species variation in the amplification efficiency of a marker gene. Metagenomics, bypassing PCR amplification, has been proposed as an alternative to overcome this bias. Several studies have already shown the promising potential of metagenomics, but they all indicate the unavailability of reference genomes for most species in any ecosystem as one of the primary bottlenecks preventing its wider implementation. In this study, we present a strategy that combines unassembled reads of low-coverage whole genome sequencing and publicly available reference genomes to construct a genomic reference database, thus circumventing high sequencing costs and intensive bioinformatic processing. We show that this approach is superior to metabarcoding for approximating relative biomass of macrobenthos species from bulk samples. Furthermore, these results can be obtained with a sequencing effort comparable to metabarcoding. The strategy presented here can thus accelerate the implementation of metagenomics in biodiversity assessments, as it should be relatively easy to adopt by laboratories familiar with metabarcoding and can be used as an accessible alternative.</p>","PeriodicalId":211,"journal":{"name":"Molecular Ecology Resources","volume":" ","pages":"e14126"},"PeriodicalIF":5.5,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144118474","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}