{"title":"Understanding the clinical and environmental drivers of antifungal resistance in the One Health context.","authors":"Catrin C Williams, Jack B Gregory, Jane Usher","doi":"10.1099/mic.0.001512","DOIUrl":"10.1099/mic.0.001512","url":null,"abstract":"<p><p>Antifungal drugs have had a tremendous impact on human health and the yields of crops. However, in recent years, due to usage both in a health setting and in agriculture, there has been a rapid emergence of antifungal drug resistance that has outpaced novel compound discovery. It is now globally recognized that new strategies to tackle fungal infection are urgently needed, with such approaches requiring the cooperation of both sectors and the development of robust antifungal stewardship rationales. In this review, we examine the current antifungal regimes in clinical and agricultural settings, focusing on two pathogens of importance, <i>Candida auris</i> and <i>Aspergillus fumigatus,</i> examining their drivers of antifungal resistance, the impact of dual-use azoles and the impact agricultural practices have on driving the emergence of resistance. Finally, we postulate that a One Health approach could offer a viable alternative to prolonging the efficacy of current antifungal agents.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 10","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11524418/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142548604","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}
Hannah E Johnston, Sarah M Batt, Alistair K Brown, Christos G Savva, Gurdyal S Besra, Klaus Fütterer
{"title":"Cryo-electron microscopy structure of the di-domain core of <i>Mycobacterium tuberculosis</i> polyketide synthase 13, essential for mycobacterial mycolic acid synthesis.","authors":"Hannah E Johnston, Sarah M Batt, Alistair K Brown, Christos G Savva, Gurdyal S Besra, Klaus Fütterer","doi":"10.1099/mic.0.001505","DOIUrl":"10.1099/mic.0.001505","url":null,"abstract":"<p><p>Mycobacteria are known for their complex cell wall, which comprises layers of peptidoglycan, polysaccharides and unusual fatty acids known as mycolic acids that form their unique outer membrane. Polyketide synthase 13 (Pks13) of <i>Mycobacterium tuberculosis</i>, the bacterial organism causing tuberculosis, catalyses the last step of mycolic acid synthesis prior to export to and assembly in the cell wall. Due to its essentiality, Pks13 is a target for several novel anti-tubercular inhibitors, but its 3D structure and catalytic reaction mechanism remain to be fully elucidated. Here, we report the molecular structure of the catalytic core domains of <i>M. tuberculosis</i> Pks13 (Mt-Pks13), determined by transmission cryo-electron microscopy (cryoEM) to a resolution of 3.4 Å. We observed a homodimeric assembly comprising the ketoacyl synthase (KS) domain at the centre, mediating dimerization, and the acyltransferase (AT) domains protruding in opposite directions from the central KS domain dimer. In addition to the KS-AT di-domains, the cryoEM map includes features not covered by the di-domain structural model that we predicted to contain a dimeric domain similar to dehydratases, yet likely lacking catalytic function. Analytical ultracentrifugation data indicate a pH-dependent equilibrium between monomeric and dimeric assembly states, while comparison with the previously determined structures of <i>M. smegmatis</i> Pks13 indicates architectural flexibility. Combining the experimentally determined structure with modelling in AlphaFold2 suggests a structural scaffold with a relatively stable dimeric core, which combines with considerable conformational flexibility to facilitate the successive steps of the Claisen-type condensation reaction catalysed by Pks13.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 10","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11649247/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142479165","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}
Aya S Hassan, Ethan S Heflen, Khoa D Nguyen, Gabriel A Parrett, Douglas D Risser
{"title":"EbsA is essential for both motility and biofilm formation in the filamentous cyanobacterium <i>Nostoc punctiforme</i>.","authors":"Aya S Hassan, Ethan S Heflen, Khoa D Nguyen, Gabriel A Parrett, Douglas D Risser","doi":"10.1099/mic.0.001498","DOIUrl":"10.1099/mic.0.001498","url":null,"abstract":"<p><p>Many cyanobacteria, both unicellular and filamentous, exhibit surface motility driven by type IV pili (T4P). While the component parts of the T4P machinery described in other prokaryotes are largely conserved in cyanobacteria, there are also several T4P proteins that appear to be unique to this phylum. One recently discovered component is EbsA, which has been characterized in two unicellular cyanobacteria. EbsA was found to form a complex with other T4P proteins and is essential for motility. Additionally, deletion of <i>ebsA</i> in one of these strains promoted the formation of biofilms. To expand the understanding of <i>ebsA</i> in cyanobacteria, its role in motility and biofilm formation were investigated in the model filamentous cyanobacterium <i>Nostoc punctiforme</i>. Expression of <i>ebsA</i> was strictly limited to hormogonia, the motile filaments of <i>N. punctiforme</i>. Deletion of <i>ebsA</i> did not affect hormogonium development but resulted in the loss of motility and the failure to accumulate surface pili or produce hormogonium polysaccharide (HPS), consistent with pervious observations in unicellular cyanobacteria. Protein-protein interaction studies indicated that EbsA directly interacts with PilB, and the localization of EbsA-GFP resembled that previously shown for both PilB and Hfq. Collectively, these results support the hypothesis that EbsA forms a complex along with PilB and Hfq that is essential for T4P extension. In contrast, rather than enhancing biofilm formation, deletion of both <i>ebsA</i> and <i>pilB</i> abolish biofilm formation in <i>N. punctiforme</i>, implying that distinct modalities for the relationship between motility, T4P function and biofilm formation may exist in different cyanobacteria.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11407516/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142299611","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}
Meaghan Castledine, Joseph Pennycook, Arthur Newbury, Luke Lear, Zoltan Erdos, Rai Lewis, Suzanne Kay, Dirk Sanders, David Sünderhauf, Angus Buckling, Elze Hesse, Daniel Padfield
{"title":"Characterizing a stable five-species microbial community for use in experimental evolution and ecology.","authors":"Meaghan Castledine, Joseph Pennycook, Arthur Newbury, Luke Lear, Zoltan Erdos, Rai Lewis, Suzanne Kay, Dirk Sanders, David Sünderhauf, Angus Buckling, Elze Hesse, Daniel Padfield","doi":"10.1099/mic.0.001489","DOIUrl":"10.1099/mic.0.001489","url":null,"abstract":"<p><p>Model microbial communities are regularly used to test ecological and evolutionary theory as they are easy to manipulate and have fast generation times, allowing for large-scale, high-throughput experiments. A key assumption for most model microbial communities is that they stably coexist, but this is rarely tested experimentally. Here we report the (dis)assembly of a five-species microbial community from a metacommunity of soil microbes that can be used for future experiments. Using reciprocal invasion-from-rare experiments we show that all species can coexist and we demonstrate that the community is stable for a long time (~600 generations). Crucially for future work, we show that each species can be identified by their plate morphologies, even after >1 year in co-culture. We characterise pairwise species interactions and produce high-quality reference genomes for each species. This stable five-species community can be used to test key questions in microbial ecology and evolution.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11412253/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142299610","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}
Wen Chyin Yew, Stacey Adlard, Michael James Dunn, Siti Aisyah Alias, David Anthony Pearce, Azizan Abu Samah, Peter Convey
{"title":"Seasonal variation in the stomach microbiota of two sympatrically breeding <i>Pygoscelis</i> penguin species at Signy Island, South Orkney Islands.","authors":"Wen Chyin Yew, Stacey Adlard, Michael James Dunn, Siti Aisyah Alias, David Anthony Pearce, Azizan Abu Samah, Peter Convey","doi":"10.1099/mic.0.001503","DOIUrl":"10.1099/mic.0.001503","url":null,"abstract":"<p><p>The gut microbiomes of Antarctic penguins are important for the fitness of the host birds and their chicks. The compositions of microbial communities in Antarctic penguin guts are strongly associated with the birds' diet, physiological adaptation and phylogeny. Whilst seasonal changes in food resources, distribution and population parameters of Antarctic penguins have been well addressed, little research is available on the stability or variability of penguin stomach microbiomes over time. Here, we focused on two <i>Pygoscelis</i> penguin species breeding sympatrically in the maritime Antarctic and analysed their stomach contents to assess whether penguin gut microbiota differed over three austral summer breeding seasons. We used a high-throughput DNA sequencing approach to study bacterial diversity in stomach regurgitates of Adélie (<i>Pygoscelis adeliae</i>) and chinstrap (<i>Pygoscelis antarctica</i>) penguins that have a similar foraging regime on Signy Island (South Orkney Islands). Our data revealed significant differences in bacterial alpha and beta diversity between the study seasons. We also identified bacterial genera that were significantly associated with specific breeding seasons, diet compositions, chick-rearing stages and sampling events. This study provides a baseline for establishing future monitoring of penguin gut microbiomes in a rapidly changing environment.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11541225/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142331122","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 Primer: Phase variation - survival and adaptability by generation of a diverse population.","authors":"Ashley J Fraser, Finn E McMahon, John M Atack","doi":"10.1099/mic.0.001492","DOIUrl":"10.1099/mic.0.001492","url":null,"abstract":"<p><p>Phase variation is defined as the rapid and reversible switching of gene expression, and typically occurs in genes encoding surface features in small genome bacterial pathogens. Phase variation has evolved to provide an extra survival mechanism in bacteria that lack multiple 'sense-and-respond' gene regulation systems. Many bacterial pathogens also encode DNA methyltransferases that are phase-variable, controlling systems called 'phasevarions' (phase-variable regulons). This primer will summarize the current understanding of phase variation, describing the role of major phase-variable factors, and phasevarions, in bacterial pathobiology.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11475388/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142114053","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":"A comparative genomic and phenotypic study of <i>Vibrio cholerae</i> model strains using hybrid sequencing.","authors":"Øyvind M Lorentzen, Christina Bleis, Sören Abel","doi":"10.1099/mic.0.001502","DOIUrl":"10.1099/mic.0.001502","url":null,"abstract":"<p><p>Next-generation sequencing methods have become essential for studying bacterial biology and pathogenesis, often depending on high-quality, closed genomes. In this study, we utilized a hybrid sequencing approach to assemble the genome of C6706, a widely used <i>Vibrio cholerae</i> model strain. We present a manually curated annotation of the genome, enhancing user accessibility by linking each coding sequence to its counterpart in N16961, the first sequenced <i>V. cholerae</i> isolate and a commonly used reference genome. Comparative genomic analysis between <i>V. cholerae</i> C6706 and N16961 uncovered multiple genetic differences in genes associated with key biological functions. To determine whether these genetic variations result in phenotypic differences, we compared several phenotypes relevant to <i>V. cholerae</i> pathogenicity like genetic stability, acid sensitivity, biofilm formation and motility. Notably, <i>V. cholerae</i> N16961 exhibited greater motility and reduced biofilm formation compared to <i>V. cholerae</i> C6706. These phenotypic differences appear to be mediated by variations in quorum sensing and cyclic di-GMP signalling pathways between the strains. This study provides valuable insights into the regulation of biofilm formation and motility in <i>V. cholerae</i>.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11420891/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142299500","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}
Eliza Rayner, Amelie Lavenir, Gemma G R Murray, Marta Matusewska, Alexander W Tucker, John J Welch, Lucy A Weinert
{"title":"Variation in bacterial pathotype is consistent with the sit-and-wait hypothesis.","authors":"Eliza Rayner, Amelie Lavenir, Gemma G R Murray, Marta Matusewska, Alexander W Tucker, John J Welch, Lucy A Weinert","doi":"10.1099/mic.0.001500","DOIUrl":"10.1099/mic.0.001500","url":null,"abstract":"<p><p>The sit-and-wait hypothesis predicts that bacteria can become more virulent when they survive and transmit outside of their hosts due to circumventing the costs of host mortality. While this hypothesis is largely supported theoretically and through comparative analysis, experimental validation is limited. Here we test this hypothesis in <i>Streptococcus suis</i>, an opportunistic zoonotic pig pathogen, where a pathogenic ecotype proliferated during the change to intensive pig farming that amplifies opportunities for fomite transmission. We show in an <i>in vitro</i> environmental survival experiment that pathogenic ecotypes survive for longer than commensal ecotypes, despite similar rates of decline. The presence of a polysaccharide capsule has no consistent effect on survival. Our findings suggest that extended survival in the food chain may augment the zoonotic capability of <i>S. suis</i>. Moreover, eliminating the long-term environmental survival of bacteria could be a strategy that will both enhance infection control and curtail the evolution of virulence.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11407517/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142299615","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}
Catherine J Dawson, Amelia Bartczak, Karl A Hassan
{"title":"Mutations in the efflux regulator gene <i>oqxR</i> provide a simple genetic switch for antimicrobial resistance in <i>Klebsiella pneumoniae</i>.","authors":"Catherine J Dawson, Amelia Bartczak, Karl A Hassan","doi":"10.1099/mic.0.001499","DOIUrl":"10.1099/mic.0.001499","url":null,"abstract":"<p><p><i>Klebsiella pneumoniae</i> is a pathogen of major concern in the global rise of antimicrobial resistance and has been implicated as a reservoir for the transfer of resistance genes between species. The upregulation of efflux pumps is a particularly concerning mechanism of resistance acquisition as, in many instances, a single point mutation can simultaneously provide resistance to a range of antimicrobials and biocides. The current study investigated mutations in <i>oqxR</i>, which encodes a negative regulator of the RND-family efflux pump genes, <i>oqxAB</i>, natively found in the chromosome of <i>K. pneumoniae</i>. Resistant mutants in four <i>K. pneumoniae</i> strains (KP6870155, NTUH-K2044, SGH10, and ATCC43816) were selected from single exposures to 30 µg/mL chloramphenicol and 12 mutants were selected for whole genome sequencing to identify mutations associated with resistance. Resistant mutants generated by single exposures to chloramphenicol, tetracycline, or ciprofloxacin at ≥4 X MIC were replica plated onto all three antibiotics to observe simultaneous cross-resistance to all compounds, indicative of a multidrug resistance phenotype. A variety of novel mutations, including single point mutations, deletions, and insertions, were found to disrupt <i>oqxR</i> leading to significant and simultaneous increases in resistance to chloramphenicol, tetracycline, and ciprofloxacin. The <i>oqxAB</i>-<i>oqxR</i> locus has been mobilized and dispersed on plasmids in many Enterobacteriaceae species and the diversity of these loci was examined to evaluate the evolutionary pressures acting on these genes. Comparison of the promoter regions of <i>oqxR</i> in plasmid-borne copies of the <i>oqxR-oqxAB</i> operon indicated that some constructs may produce truncated versions of the <i>oqxR</i> transcript, which may impact on <i>oqxAB</i> regulation and expression. In some instances, co-carriage of chromosomal and plasmid encoded <i>oqxAB-oqxR</i> was found in <i>K. pneumoniae</i>, implying that there is selective pressure to maintain and expand the efflux pump. Given that OqxR is a repressor of <i>oqxAB</i>, any mutation affecting its expression or function can lead to multidrug resistance. This is in contrast to antibiotic target site mutations that must occur in limited sequence space to be effective and not impact the fitness of the cell. Therefore, <i>oqxR</i> may act as a simple genetic switch to facilitate resistance via OqxAB mediated efflux.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11373524/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142127169","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}
Samia Quaiyum, Yifeng Yuan, Guangxin Sun, R M Madhushi N Ratnayake, Geoffrey Hutinet, Peter C Dedon, Michael F Minnick, Valérie de Crécy-Lagard
{"title":"Queuosine salvage in <i>Bartonella henselae</i> Houston 1: a unique evolutionary path.","authors":"Samia Quaiyum, Yifeng Yuan, Guangxin Sun, R M Madhushi N Ratnayake, Geoffrey Hutinet, Peter C Dedon, Michael F Minnick, Valérie de Crécy-Lagard","doi":"10.1099/mic.0.001490","DOIUrl":"10.1099/mic.0.001490","url":null,"abstract":"<p><p>Queuosine (Q) stands out as the sole tRNA modification that can be synthesized via salvage pathways. Comparative genomic analyses identified specific bacteria that showed a discrepancy between the projected Q salvage route and the predicted substrate specificities of the two identified salvage proteins: (1) the distinctive enzyme tRNA guanine-34 transglycosylase (bacterial TGT, or bTGT), responsible for inserting precursor bases into target tRNAs; and (2) queuosine precursor transporter (QPTR), a transporter protein that imports Q precursors. Organisms such as the facultative intracellular pathogen <i>Bartonella henselae</i>, which possess only bTGT and QPTR but lack predicted enzymes for converting preQ<sub>1</sub> to Q, would be expected to salvage the queuine (q) base, mirroring the scenario for the obligate intracellular pathogen <i>Chlamydia trachomatis</i>. However, sequence analyses indicate that the substrate-specificity residues of their bTGTs resemble those of enzymes inserting preQ<sub>1</sub> rather than q. Intriguingly, MS analyses of tRNA modification profiles in <i>B. henselae</i> reveal trace amounts of preQ<sub>1</sub>, previously not observed in a natural context. Complementation analysis demonstrates that <i>B. henselae</i> bTGT and QPTR not only utilize preQ<sub>1</sub>, akin to their <i>Escherichia coli</i> counterparts, but can also process q when provided at elevated concentrations. The experimental and phylogenomic analyses suggest that the Q pathway in <i>B. henselae</i> could represent an evolutionary transition among intracellular pathogens - from ancestors that synthesized Q <i>de novo</i> to a state prioritizing the salvage of q. Another possibility that will require further investigations is that the insertion of preQ<sub>1</sub> confers fitness advantages when <i>B. henselae</i> is growing outside a mammalian host.</p>","PeriodicalId":49819,"journal":{"name":"Microbiology-Sgm","volume":"170 9","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11570991/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142134281","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}