Karuna Anna Sajeevan , Bibek Acharya , Sakib Ferdous , Dan M. Park , Joseph A. Cotruvo Jr. , Ratul Chowdhury
{"title":"Computationally derived structural insights into Rare Earth selectivity in lanmodulin and its variants","authors":"Karuna Anna Sajeevan , Bibek Acharya , Sakib Ferdous , Dan M. Park , Joseph A. Cotruvo Jr. , Ratul Chowdhury","doi":"10.1016/j.csbj.2025.02.005","DOIUrl":"10.1016/j.csbj.2025.02.005","url":null,"abstract":"<div><div>Understanding rare earth element (REE) binding to proteins enables the engineering of selective protein-based ligands for precise REE recovery. Lanmodulin (LanM), with notable REE selectivity and picomolar binding affinity, is a promising candidate. This study shows that LanM variants employ distinct inter-residue interactions for REE binding. We detail the thermodynamics and structural aspects of binding events in wild-type (WT) <em>Methylorubrum extorquens</em> LanM and five EF-hand residue variants (4P<sub>2</sub>A and 4D<sub>9</sub>X, X = N, A, H, M), using protein variant structure prediction, molecular dynamics simulations and binding motif exploration. We demonstrate strong agreement between experimental binding measurements (apparent <em>K</em><sub><em>d</em></sub>) and <em>in silico</em> binding energy scores of WT, 4 P<sub>2</sub>A, and 4D<sub>9</sub>X LanMs. We systematically investigate the role of solvent dielectric, sample multiple force fields, and initial protein structure bias on metal ion-binding energetics. In addition, we identify amino acids outside the direct metal binding motif crucial for coordinating the binding events which is corroborated with experimental binding characteristics of 4D<sub>9</sub>X variants. Computationally measured binding affinity with contribution from this secondary set of residues show agreement with the experimental <em>K</em><sub>d</sub> values and suggests how some point mutations can induce long-range structural perturbations to regulate metal ion-protein recognition and interactions. Finally, we analyze structural changes arising from alterations in side-chain flexibility of each amino acid on the protein backbone at the instant of metal binding and recognition – which manifests as altered helicity at a specific locus of the protein, a result that is corroborative of the observations from circular dichroism experiments.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 639-648"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143428824","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}
Olivia S. Pratt , Luc G. Elliott , Margaux Haon , Shahram Mesdaghi , Rebecca M. Price , Adam J. Simpkin , Daniel J. Rigden
{"title":"AlphaFold 2, but not AlphaFold 3, predicts confident but unrealistic β-solenoid structures for repeat proteins","authors":"Olivia S. Pratt , Luc G. Elliott , Margaux Haon , Shahram Mesdaghi , Rebecca M. Price , Adam J. Simpkin , Daniel J. Rigden","doi":"10.1016/j.csbj.2025.01.016","DOIUrl":"10.1016/j.csbj.2025.01.016","url":null,"abstract":"<div><div>AlphaFold 2 (AF2) has revolutionised protein structure prediction but, like any new tool, its performance on specific classes of targets, especially those potentially under-represented in its training data, merits attention. Prompted by a highly confident prediction for a biologically meaningless, randomly permuted repeat sequence, we assessed AF2 performance on sequences composed of perfect repeats of random sequences of different lengths. AF2 frequently folds such sequences into β-solenoids which, while ascribed high confidence, contain unusual and implausible features such as internally stacked and uncompensated charged residues. A number of sequences confidently predicted as β-solenoids are predicted by other advanced methods as intrinsically disordered. The instability of some predictions is demonstrated by molecular dynamics. Importantly, other deep learning-based structure prediction tools predict different structures or β-solenoids with much lower confidence suggesting that AF2 alone has an unreasonable tendency to predict confident but unrealistic β-solenoids for perfect repeat sequences. The potential implications for structure prediction of natural (near-)perfect sequence repeat proteins are also explored.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 467-477"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143150061","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}
{"title":"Machine and deep learning to predict viral fusion peptides","authors":"A.M. Sequeira , M. Rocha , Diana Lousa","doi":"10.1016/j.csbj.2025.02.011","DOIUrl":"10.1016/j.csbj.2025.02.011","url":null,"abstract":"<div><div>Viral fusion proteins, located on the surface of enveloped viruses like SARS-CoV-2, Influenza, and HIV, play a vital role in fusing the virus envelope with the host cell membrane. Fusion peptides, conserved segments within these proteins, are crucial for the fusion process and are potential targets for therapy. Experimental identification of fusion peptides is time-consuming and costly, which creates the need for bioinformatics tools that can predict the segment within the fusion protein sequence that corresponds to the FP. Although homology-based methods have been used towards this end, they fail to identify fusion peptides lacking overall sequence similarity to known counterparts. Therefore, alternative methods are needed to discover new putative fusion peptides, namely those based on machine learning. In this study, we explore various ML-based approaches to identify fusion peptides within a fusion protein sequence. We employ token classification methods and sliding window approaches coupled with machine and deep learning models. We evaluate different protein sequence representations, including one-hot encoding, physicochemical features, as well as representations from Natural Language Processing, such as word embeddings and transformers. Through the examination of over 50 combinations of models and features, we achieve promising results, particularly with models based on a state-of-the-art transformer for amino acid token classification. Furthermore, we utilize the best models to predict hypothetical fusion peptides for SARS-CoV-2, and critically analyse annotated peptides from existing research. Overall, our models effectively predict the location of fusion peptides, even in viruses for which limited experimental data is available.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 692-704"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143473603","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}
{"title":"Repurposing thioridazine as a potential CD2068 inhibitor to mitigate antibiotic resistance in Clostridioides difficile infection","authors":"Methinee Pipatthana , Matthew Phanchana , Apiwat Sangphukieo , Sitthivut Charoensutthivarakul , Phurt Harnvoravongchai , Surang Chankhamhaengdecha , Pattaneeya Prangthip , Pattanai Konpetch , Chanakarn Sripong , Sarawut Wongphayak , Tavan Janvilisri","doi":"10.1016/j.csbj.2025.02.036","DOIUrl":"10.1016/j.csbj.2025.02.036","url":null,"abstract":"<div><div><em>Clostridioides difficile</em> infection (CDI) is a major public health issue, driven by antibiotic resistance and frequent recurrence. CD2068, an ABC protein in <em>C. difficile</em>, is associated with drug resistance, making it a potential target for novel therapies. This study explored FDA-approved non-antibiotic drugs for their ability to inhibit CD2068 through drug screening and experimental validation. Thioridazine exhibited moderate binding affinity to CD2068 and inhibited its ATP hydrolysis activity. It also suppressed the growth of multiple <em>C. difficile</em> ribotypes at 64–128 µg/mL, with rapid-killing effects. When combined with sub-MIC levels of standard antibiotics, thioridazine significantly reduced bacterial growth. In a mouse CDI model, thioridazine demonstrated potential in restoring gut microbial balance and improving survival, although it did not show superiority to vancomycin. These findings suggest that thioridazine has potential as a novel therapeutic for CDI, either as an adjunct to existing antibiotics or as part of a combination therapy to combat antibiotic resistance. Further research, including replication studies and dose optimization, is needed to fully evaluate thioridazine’s therapeutic potential.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 887-895"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143548768","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}
Devansh Shah , Kelly McCastlain , Ti-Cheng Chang , Xun Zhu , Gang Wu , Mondira Kundu
{"title":"MitoEdit: A pipeline for optimizing mtDNA base editing and predicting bystander effects","authors":"Devansh Shah , Kelly McCastlain , Ti-Cheng Chang , Xun Zhu , Gang Wu , Mondira Kundu","doi":"10.1016/j.csbj.2025.04.027","DOIUrl":"10.1016/j.csbj.2025.04.027","url":null,"abstract":"<div><div>Human mitochondrial DNA (mtDNA) mutations are causally implicated in maternally inherited mitochondrial respiratory disorders; however, the role of somatic mtDNA mutations in both late-onset chronic diseases and cancer remains less clear. Recent advances in mtDNA base editing technologies offer exciting opportunities to model and study these mutations. However, current approaches are hindered by the challenge of unintended bystander edits, which are often identified only through labor-intensive empirical testing, leading to inefficiencies in construct development. To address this limitation, we developed MitoEdit, an innovative computational tool designed to optimize mtDNA base editing by leveraging empirical base editor patterns. MitoEdit enables users to input DNA sequences in a simple text-based format, specify the target base position and define the desired modification. The tool outputs a list of candidate target windows, predicts the number and functional impact of bystander edits and provides flanking nucleotide sequences tailored for TALE (transcription activator-like effectors) array protein binding. <em>In silico</em> evaluations demonstrate that MitoEdit accurately predicts the majority of bystander edits, reducing the number of constructs that need to be tested empirically. By streamlining the design process, MitoEdit accelerates the development of mitochondrial base editing constructs, thereby facilitating functional studies and enabling faster discovery. Ultimately, MitoEdit has the potential to advance disease modeling and support the development of therapeutic strategies for mitochondrial-related disorders.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 1673-1676"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143870706","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}
Dimitrios Zouraris , Konstantia Graikou , Panagiotis Vasileiou , Vladimir Dimitrov , Zora Dajic Stevanovic , Anna Rita Bilia , Jelena Zivkovic , Alberto Dias , Konstantinos Kasiotis , Konstantinos Gardikis , Paula Dias , Mirko Oluški , Juan Ramón Muñoz Montaño , Hristina Hristova , Hristo Iliev , Giovanna Petrangolini , Antreas Afantitis , Nektarios Aligiannis
{"title":"EthnoHERBS: Harnessing traditional herbal knowledge for biodiversity conservation and innovative health solutions","authors":"Dimitrios Zouraris , Konstantia Graikou , Panagiotis Vasileiou , Vladimir Dimitrov , Zora Dajic Stevanovic , Anna Rita Bilia , Jelena Zivkovic , Alberto Dias , Konstantinos Kasiotis , Konstantinos Gardikis , Paula Dias , Mirko Oluški , Juan Ramón Muñoz Montaño , Hristina Hristova , Hristo Iliev , Giovanna Petrangolini , Antreas Afantitis , Nektarios Aligiannis","doi":"10.1016/j.csbj.2025.03.035","DOIUrl":"10.1016/j.csbj.2025.03.035","url":null,"abstract":"<div><div>EthnoHERBS represents a pioneering multidisciplinary initiative that integrates traditional herbal knowledge with advanced natural product chemistry to promote biodiversity conservation and foster innovative cosmeceutical solutions. The project systematically documents centuries-old ethnobotanical practices across South-Eastern Europe, leading to the identification of a diverse array of medicinal and aromatic plants traditionally used to treat skin disorders. Employing environmentally friendly extraction techniques alongside cutting-edge analytical tools—including UHPLC-HRMS, CPC, and NMR spectroscopy—over 500 bioactive compounds have been characterized, with 30 novel secondary metabolites isolated and structurally elucidated. Advanced <em>in silico</em> methodologies, such as docking, molecular dynamics simulations, and MM-GBSA rescoring, were implemented to evaluate the interaction profiles of these compounds with key skin disorder-related enzymes, including elastase, tyrosinase, hyaluronidase, and xanthine oxidase. Complementary in vitro and in vivo assays confirmed the potent antioxidant, anti-inflammatory, and wound-healing properties of the selected extracts. Furthermore, the project underscores sustainable practices by establishing organic cultivation protocols and pilot-scale production processes, ensuring the eco-friendly exploitation of natural resources. By fostering extensive collaboration between academic institutions and industry partners under the Horizon 2020 framework, EthnoHERBS not only advances scientific research and innovative product development but also serves as a model for preserving traditional knowledge and biodiversity.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"29 ","pages":"Pages 85-94"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143724354","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}
{"title":"Modeling the different conformations of the human mitochondrial ADP/ATP carrier using AlphaFold and molecular dynamics simulations of the protein-ligand complexes","authors":"Virginia Quadrotta , Fabio Polticelli","doi":"10.1016/j.csbj.2025.03.036","DOIUrl":"10.1016/j.csbj.2025.03.036","url":null,"abstract":"<div><div>The ADP/ATP Carrier (AAC), a member of the mitochondrial Solute Carrier Family 25 (SLC25), facilitates the exchange of cytosolic ADP for mitochondrial ATP across the inner mitochondrial membrane (IMM). It serves as a master regulator of the cellular ADP/ATP ratio and is involved in various pathologies, including cancer. Its transport mechanism involves a conformational transition that alternates the accessibility of the binding site between the cytoplasmic (c-state) and mitochondrial (m-state) sides of the IMM. In this study, the human AAC was used as a case study to evaluate the performance of AlphaFold2 (AF2) and AlphaFold3 (AF3) for structural modeling of members of the SLC25 family. The study also compared the AF3 approach for predicting protein-ligand complexes with the standard methodology of modeling followed by molecular docking. Both AF2 and AF3 display a bias toward the c-state conformation. On the other hand, ColabFold implementation of AF2 successfully generated the first <em>ab initio</em> structural model of the human AAC in the m-state conformation. Modeling of the complexes coupled to molecular dynamics (MD) simulations allowed to obtain structural insight into AAC’s substrate binding and stabilization mechanisms, and the possible effects of pathogenic mutations on its conformational dynamics and functionality. These analyses provided a deeper understanding of AAC’s alternating access mechanism and highlighted the potential of AF3 in modeling protein-ligand interactions, though only in the c-state. This work demonstrates the reliability of AlphaFold models when aligned with experimental data and provides further confirmation of their utility for investigating solute carriers and membrane proteins.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 1265-1277"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143715578","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}
Kęstutis Timinskas, Albertas Timinskas, Česlovas Venclovas
{"title":"Common themes in architecture and interactions of prokaryotic PolB2 and Pol V mutasomes inferred from in silico studies","authors":"Kęstutis Timinskas, Albertas Timinskas, Česlovas Venclovas","doi":"10.1016/j.csbj.2025.01.010","DOIUrl":"10.1016/j.csbj.2025.01.010","url":null,"abstract":"<div><div>Translesion DNA synthesis (TLS) is typically performed by inherently error-prone Y-family DNA polymerases. Extensively studied <em>Escherichia coli</em> Pol V mutasome, composed of UmuC, an UmuD′ dimer and RecA is an example of a multimeric Y-family TLS polymerase. Less commonly TLS is performed by DNA polymerases of other families. One of the most intriguing such cases in B-family is represented by archaeal PolB2 and its bacterial homologs. Previously thought to be catalytically inactive, PolB2 was recently shown to be absolutely required for targeted mutagenesis in <em>Sulfolobus islandicus</em>. However, the composition and structure of the PolB2 holoenzyme remain unknown. We used highly accurate AlphaFold structural models, coupled with protein sequence and genome context analysis to comprehensively characterize PolB2 and its associated proteins, PPB2, a small helical protein, and iRadA, a catalytically inactive Rad51 homolog. We showed that these three proteins can form a heteropentameric PolB2 complex featuring high confidence modeling scores. Unexpectedly, we found that PolB2 binds iRadA through a structural motif reminiscent of RadA/Rad51 oligomerization motif. In some mutasomes we identified clamp binding motifs, present in either iRadA or PolB2, but rarely in both. We also used AlphaFold to derive a three-dimensional structure of Pol V, for which the experimental structure remains unsolved thus precluding comprehensive understanding of its molecular mechanism. Our analysis showed that the structural features of Pol V explain many of the puzzling previous experimental results. Even though models of PolB2 and Pol V mutasomes are structurally different, we found striking similarities in their architectural organization and interactions.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 401-410"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143098554","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}
{"title":"Topology entropy: Enhancing graph partitioning for TAD identification and single-cell clustering","authors":"Qiushi Liang , Shengjie Zhao , Lingxi Chen , Shuai Cheng Li","doi":"10.1016/j.csbj.2025.04.037","DOIUrl":"10.1016/j.csbj.2025.04.037","url":null,"abstract":"<div><div>Entropy quantifies the limits of information compression and provides a theoretical foundation for exploring complex structures in large-scale graphs. However, effective metrics are needed to capture the intricate structural details in biological graphs. In this paper, we introduce the <em>topology entropy encoding tree</em> to quantify the complexity of biological graphs and show that minimizing the associated entropy is equivalent to optimal graph partitioning. We develop two methods, TEC-O and TEC-U, for partitioning ordered and unordered biological graphs. TEC-O is applied to identify Topologically Associated Domains (TADs) in Hi-C contact maps, while TEC-U is used for cell clustering in single-cell sequencing data. Results from simulated datasets demonstrate that topology entropy is robust to noise and effectively captures structural information, outperforming existing methods. Experiments on Hi-C data from five cell lines and ten single-cell sequencing datasets show that TEC-O and TEC-U achieve the highest accuracy in TAD detection and cell clustering, respectively, providing biologically meaningful insights.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 1864-1886"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143942063","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}
{"title":"Nanopore sequencing of protozoa: Decoding biological information on a string of biochemical molecules into human-readable signals","authors":"Branden Hunter , Timothy Cromwell , Hyunjin Shim","doi":"10.1016/j.csbj.2025.01.002","DOIUrl":"10.1016/j.csbj.2025.01.002","url":null,"abstract":"<div><div>Biological information is encoded in a sequence of biochemical molecules such as nucleic acids and amino acids, and nanopore sequencing is a long-read sequencing technology capable of directly decoding these molecules into human-readable signals. The long reads from nanopore sequencing offer the advantage of obtaining contiguous information, which is particularly beneficial for decoding complex or repetitive regions in a genome. In this study, we investigated the efficacy of nanopore sequencing in decoding biological information from distinctive genomes in metagenomic samples, which pose significant challenges for traditional short-read sequencing technologies. Specifically, we sequenced blood and fecal samples from mice infected with <em>Trypanosoma brucei</em>, a unicellular protozoan known for its hypervariable and dynamic regions that help it evade host immunity. Such characteristics are also prevalent in other host-dependent parasites, such as bacteriophages. The taxonomic classification results showed a high proportion of nanopore reads identified as <em>T. brucei</em> in the infected blood samples, with no significant identification in the control blood samples and fecal samples. Furthermore, metagenomic de novo assembly of these nanopore reads yielded contigs that mapped to the reference genome of <em>T. brucei</em> in the infected blood samples with over 96 % accuracy. This exploratory work demonstrates the potential of nanopore sequencing for the challenging task of classifying and assembling hypervariable and dynamic genomes from metagenomic samples.</div></div>","PeriodicalId":10715,"journal":{"name":"Computational and structural biotechnology journal","volume":"27 ","pages":"Pages 440-450"},"PeriodicalIF":4.4,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143098821","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}