Linnea F M Kop, Hanna Koch, Paula Dalcin Martins, Carolina Suarez, Sabina Karačić, Frank Persson, Britt-Marie Wilén, Per Hagelia, Mike S M Jetten, Sebastian Lücker
{"title":"High diversity of nitrifying bacteria and archaea in biofilms from a subsea tunnel.","authors":"Linnea F M Kop, Hanna Koch, Paula Dalcin Martins, Carolina Suarez, Sabina Karačić, Frank Persson, Britt-Marie Wilén, Per Hagelia, Mike S M Jetten, Sebastian Lücker","doi":"10.1093/femsec/fiaf032","DOIUrl":"10.1093/femsec/fiaf032","url":null,"abstract":"<p><p>Microbial biofilm formation can contribute to the accelerated deterioration of steel-reinforced concrete structures and significantly impact their service life, making it critical to understand the diversity of the biofilm community and prevailing processes in these habitats. Here, we analyzed 16S rRNA gene amplicon and metagenomics sequencing data to study the abundance and diversity of nitrifiers within biofilms on the concrete surface of the Oslofjord subsea road tunnel in Norway. We showed that the abundance of nitrifiers varied greatly in time and space, with a mean abundance of 24.7 ± 15% but a wide range between 1.2% and 61.4%. We hypothesize that niche differentiation allows the coexistence of several nitrifier groups and that their high diversity increases the resilience to fluctuating environmental conditions. Strong correlations were observed between the nitrifying families Nitrosomonadaceae and Nitrospinaceae, and the iron-oxidizing family Mariprofundaceae. Metagenome-assembled genome analyses suggested that early Mariprofundaceae colonizers may provide a protected environment for nitrifiers in exchange for nitrogen compounds and vitamin B12, but further studies are needed to elucidate the spatial organization of the biofilms and the cooperative and competitive interactions in this environment. Together, this research provides novel insights into the diverse communities of nitrifiers living within biofilms on concrete surfaces and establishes a foundation for future experimental studies of concrete biofilms.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11995701/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143742714","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Assessing the methanogenic activity of microbial communities enriched from a depleted reservoir.","authors":"Arianna Vizzarro, Annalisa Abdel Azim, Ilaria Bassani, Ruggero Bellini, Nicolò Santi Vasile, Candido Fabrizio Pirri, Francesca Verga, Barbara Menin","doi":"10.1093/femsec/fiaf040","DOIUrl":"https://doi.org/10.1093/femsec/fiaf040","url":null,"abstract":"<p><p>Using a depleted gas reservoir as a natural reactor is a novel approach for microbial methanation of hydrogen (H2) and carbon dioxide (CO2) into methane (CH4). This approach, known as underground biomethanation reactor (UMR), could enable the simultaneous valorization of geologically sequestered CO2 and the excess renewable energy, stored in the form of H2 in the same formation as the CO2. In this study, we explore the possibility to trigger biomethanation from formation water sample by testing various carbon sources (CO2, trypticase peptone, glucose, and acetate) in batch test with a defined mineral medium. Obtained results show that trypticase peptone supplementation greatly increased methane production and the enrichment of methanogenic archaea, outperforming alternative carbon sources. 16S rRNA amplicon sequencing of the enriched consortia revealed that supplementation of trypticase peptone and a mixture of H2:CO2 (80:20), resulted in the selection of a mixed culture dominated by microorganisms assigned to the Methanothermobacterium, Garciella, and Caminicella genera. Furthermore, KEGG (Kyoto Encyclopedia of Genes and Genomes) and COG (Clusters of Orthologous Genes) predictive functional analyses underline a possible syntrophic relationship, enhancing the conversion of H2 and CO2 into CH4. This work lays the groundwork for biologically exploiting a depleted gas reservoir by implementing the UMR technology.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":"101 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12054477/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143960683","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ulises E Rodriguez-Cruz, Manuel Ochoa-Sánchez, Luis E Eguiarte, Valeria Souza
{"title":"Running against the clock: exploring microbial diversity in an extremely endangered microbial oasis in the Chihuahuan Desert.","authors":"Ulises E Rodriguez-Cruz, Manuel Ochoa-Sánchez, Luis E Eguiarte, Valeria Souza","doi":"10.1093/femsec/fiaf033","DOIUrl":"https://doi.org/10.1093/femsec/fiaf033","url":null,"abstract":"<p><p>The Cuatro Ciénegas Basin is a biodiversity hotspot known for its unique biodiversity. However, this ecosystem is facing severe anthropogenic threats that are drying its aquatic systems. We investigated microbial communities at three sites with different physicochemical and environmental characteristics (Pozas Rojas, Archean Domes, and the Churince system) within the basin to explore potential connections to deep aquifers and determine if the sites shared microorganisms. Utilizing 16S rRNA gene data, we identified a core microbiota between Pozas Rojas (PR) and Archean Domes (AD). Sulfur reduction appears to shape the microbial connectivity among sites, since sulfur-reducing bacteria has the highest prevalence between samples from PR and AD: Halanaerobium sp. (88.46%) and Desulfovermiculus halophilus (65%); and between the Churince system and AD: Halanaerobium sp. (63%) and D. halophilus (60%). Furthermore, metagenome-assembled genomes from Ectothiorhodospira genus were found in both AD and Churince, suggesting microbial dispersal. An important finding is that microbial diversity in the AD system declined, from 2016 to 2023 the ecosystem lost 29 microbial phyla. If this trend continues, the basin will lose most of its water, resulting in the loss of various prokaryotic lineages and potential biotechnological solutions, such as enzymes or novel antibiotics. Our findings highlighting the need for water extraction regulations to preserve the basin's biodiversity.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":"101 5","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11995699/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143976772","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Halo-tolerant plant growth-promoting bacteria-mediated plant salt resistance and microbiome-based solutions for sustainable agriculture in saline soils.","authors":"Hui-Ping Li, Hong-Bin Ma, Jin-Lin Zhang","doi":"10.1093/femsec/fiaf037","DOIUrl":"10.1093/femsec/fiaf037","url":null,"abstract":"<p><p>Soil salinization has been the major form of soil degradation under the dual influence of climate change and high-intensity human activities, threatening global agricultural sustainability and food security. High salt concentrations induce osmotic imbalance, ion stress, oxidative damage, and other hazards to plants, resulting in retarded growth, reduced biomass, and even total crop failure. Halo-tolerant plant growth promoting rhizobacteria (HT-PGPR), as a widely distributed group of beneficial soil microorganisms, are emerging as a valuable biological tool for mitigating the toxic effects of high salt concentrations and improve plant growth while remediating degraded saline soil. Here, the current status, harm, and treatment measures of global soil salinization are summarized. The mechanism of salt tolerance and growth promotion induced by HT-PGPR are reviewed. We highlight that advances in multiomics technologies are helpful for exploring the genetic and molecular mechanisms of microbiota centered on HT-PGPR to address the issue of plant losses in saline soil. Future research is urgently needed to comprehensively and robustly determine the interaction mechanism between the root microbiome centered on HT-PGPR and salt-stressed plants via advanced means to maximize the efficacy of HT-PGPR as a microbial agent.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12051855/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143803027","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Andreas Härer, Joshua Dominguez, Jonathan B Shurin, Diana J Rennison
{"title":"Contrasting alpha, beta, and gamma diversity in the littoral zones of mountain lakes: effects of habitat size and within-lake community structuring on bacterial biogeography.","authors":"Andreas Härer, Joshua Dominguez, Jonathan B Shurin, Diana J Rennison","doi":"10.1093/femsec/fiaf026","DOIUrl":"10.1093/femsec/fiaf026","url":null,"abstract":"<p><p>Research on microbial biogeography has revealed key patterns like the diversity-area relationship and distance-decay of similarity. However, how habitat size affects bacterial diversity in freshwater environments remains largely unclear. Here, we characterize bacterial communities in the littoral zones of 10 mountain lakes in the Sierra Nevada, CA, ranging in surface area from 0.92 to 71.72 ha. Despite significant habitat size effects on community composition, dominant bacterial phyla were shared across lakes. We found no evidence for diversity-area relationships, either in single samples (alpha diversity) or cumulative lake-level samples (within-lake gamma diversity), when accounting for environmental variation. Moreover, within-lake beta diversity showed little spatial structuring, with similar bacterial community composition across samples regardless of geographic distance. Gamma diversity did not reach saturation with our sample size, and lake size had no effect on the predicted sample size necessary to reach gamma diversity saturation. Our findings offer new insights into diversity-area dynamics and spatial structuring by investigating alpha, beta, and gamma diversity in freshwater environments. Notably, individual water samples captured much of the bacterial community, with strong correlations between alpha and gamma diversity. These results advance our understanding of microbial biogeography and inform sampling designs for characterizing bacterial diversity in freshwater ecosystems.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11963758/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143647862","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Verena Nikeleit, Markus Maisch, Daniel Straub, Sümeyya Eroglu, Jimena C Lopez-Rivoldi, Harald Strauss, Fin Ring-Hrubesh, James M Byrne, Andreas Kappler, Casey Bryce
{"title":"Cryptic iron cycling influenced by organic carbon availability in a seasonally stratified lake.","authors":"Verena Nikeleit, Markus Maisch, Daniel Straub, Sümeyya Eroglu, Jimena C Lopez-Rivoldi, Harald Strauss, Fin Ring-Hrubesh, James M Byrne, Andreas Kappler, Casey Bryce","doi":"10.1093/femsec/fiaf029","DOIUrl":"10.1093/femsec/fiaf029","url":null,"abstract":"<p><p>Iron cycling including phototrophic Fe(II) oxidation has been observed in multiple permanently stratified meromictic lakes, yet less focus has been on dimictic lakes, which seasonally overturn and are vastly more common. Here, we investigated iron cycling in a dimictic lake, Großes Heiliges Meer in northwest Germany, using 16S rRNA amplicon sequencing, as well as in-situ and lab-based experiments. Bacterial community composition in the lake follows geochemical gradients and differs markedly between oxic and anoxic conditions. Potential iron-metabolizing bacteria were found mostly in anoxic conditions at 7 and 8 m depth and were comprised of taxa from the genera Chlorobium, Thiodictyon, Sideroxydans, Geobacter, and Rhodoferrax. We were able to recreate active iron cycling (1) with an ex-situ microbial community from 8 m depth and (2) with a successful microbial enrichment culture from 7 m depth. Varying the light and organic carbon availability in lab-based experiments showed that Fe(III) reduction overshadows Fe(II) oxidation leading to a cryptic iron cycle. Overall, we could demonstrate that microbial iron cycling can be a key biogeochemical process in dimictic lakes despite regular disturbance, and that complex environmental factors such as organic substrates control the balance between Fe(II) oxidation and Fe(III) reduction.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11974394/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143669188","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Stefanie Becker, Thu Trang Dang, Ran Wei, Andreas Kappler
{"title":"Evaluation of Thiobacillus denitrificans' sustainability in nitrate-reducing Fe(II) oxidation and the potential significance of Fe(II) as a growth-supporting reductant.","authors":"Stefanie Becker, Thu Trang Dang, Ran Wei, Andreas Kappler","doi":"10.1093/femsec/fiaf024","DOIUrl":"10.1093/femsec/fiaf024","url":null,"abstract":"<p><p>The betaproteobacterium Thiobacillus denitrificans (ATCC 25259) oxidizes Fe(II) while reducing nitrate, yet its capacity for autotrophic growth as a nitrate-reducing Fe(II)-oxidizer remains uncertain. This study explored this capacity through cultivation experiments across multiple transfers, using growth medium with Fe(II) and nitrate as sole electron donor and acceptor, respectively. This setup necessitated nitrate reduction coupled to Fe(II) oxidation as the primary energy-yielding mechanism and Fe(II) as the exclusive electron donor for CO2 fixation and biomass production. Thiosulfate/nitrate pregrown T. denitrificans oxidized 42% of 10 mM Fe(II), reduced 54% of 3.5 mM nitrate, and accumulated 1.6 mM nitrite, but showed no cell growth. Subsequent transfers from this Fe(II)/nitrate culture to fresh medium with Fe(II) and nitrate showed no nitrate-reducing Fe(II) oxidation or population growth. While bacterial activity [Fe(II) oxidation, nitrate reduction] occurred in the first transfer from thiosulfate/nitrate to Fe(II)/nitrate, nitrite was produced, further reacting with Fe(II) abiotically (chemodenitrification). A kinetic model assessed enzymatic versus abiotic Fe(II) oxidation, revealing enzymatic oxidation accounted for twice as much (ca. 70%) as abiotic denitrification (ca. 30%) within 22 days. These findings suggest T. denitrificans performs the first step of denitrification with Fe(II) as an electron donor but does not achieve autotrophic growth under these conditions.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11963766/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143647863","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Elisabeth Williamson, Kelly Hill, Katja Hogendoorn, Raphael Eisenhofer
{"title":"The bacterial community associated with the solitary resin bee Megachile tosticauda throughout its life cycle.","authors":"Elisabeth Williamson, Kelly Hill, Katja Hogendoorn, Raphael Eisenhofer","doi":"10.1093/femsec/fiaf023","DOIUrl":"10.1093/femsec/fiaf023","url":null,"abstract":"<p><p>Unlike in eusocial bees where the identity, acquisition, and function of symbiotic microbes are well understood, little is known about the relationships formed between solitary bees and bacteria. Assessing the potential role of microbes in solitary bee health is important, especially in the face of global bee declines. Early evidence suggests solitary bee microbiomes differ between bee species and development stages, but the reported bacteria are often indistinguishable from environmental taxa. Here, we use metabarcoding of the 16S rRNA gene to characterize the bacterial communities associated with solitary resin bee Megachile tosticauda. We describe the microbiome at different life cycle stages, and within pollen provisions, and investigate indirect inheritance from nesting substrate upon eclosion. The microbiome of adult M. tosticauda was consistent between samples, and the bacterial composition of larval pollen supplies changed with progressing larval development. In wild adults and pollen provisions, the genus Acinetobacter-a common nectar associate-dominated the communities. In prepupae and frass, Tyzzerella dominated, a genus that has been found in a number of other immature bee systems. Intriguingly, while wild adults did not harbour Tyzzerella, all bees that had newly emerged from the nest did. The combined observations show that M. tosticauda acquire their bacterial community from the environment, and Tyzzerella may represent a beneficial symbiont for mature brood.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11916890/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143556166","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"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, Daniel Padfield, Rai Lewis, Angus Buckling
{"title":"Microbial community structure is affected by phage-resistance associated increases in host density.","authors":"Meaghan Castledine, Daniel Padfield, Rai Lewis, Angus Buckling","doi":"10.1093/femsec/fiaf027","DOIUrl":"10.1093/femsec/fiaf027","url":null,"abstract":"<p><p>Lytic bacteriophages ('phages') can limit bacterial densities and shape community structure, either directly through lysis or indirectly through costs to resistance. However, phages have also been reported to have no, and in some cases even positive, effects on host densities. Here, we investigate the mechanisms behind an increase in host density in Variovorax sp. populations following a fixation of resistance that was maintained after phage extinction. Our results demonstrate that the density increase was a genetic trait coinciding with resistance emergence. Growth curves showed that phage resistance shifted population growth curves such that density was higher in the death phase. This density-increasing effect of resistance had important implications for community structure with phage-resistant Variovorax decreasing the density of a conspecific. That resistance to lytic phage can increase host densities has implications for wider ecology and phage therapy, where lytic phages are presumed to have negative effects on their hosts.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11953036/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143656603","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jingyi Xiao, Sijia Hao, Li-Juan Xiao, Yang Yang, Qinglong L Wu, Dan He, Lijun Zhou, Ren Hu, Lijuan Ren
{"title":"Particle-attached bacterial communities are more susceptible to seasonal environmental fluctuations in mesotrophic than eutrophic tropical reservoirs.","authors":"Jingyi Xiao, Sijia Hao, Li-Juan Xiao, Yang Yang, Qinglong L Wu, Dan He, Lijun Zhou, Ren Hu, Lijuan Ren","doi":"10.1093/femsec/fiae154","DOIUrl":"10.1093/femsec/fiae154","url":null,"abstract":"<p><p>Particle-attached bacterial (PAB) communities play pivotal roles in water organic matter decomposition, nutrient cycling, and the natural self-purification processes. However, we know little about their responses to seasonal environmental fluctuations, under eutrophication in reservoir ecosystems. In this study, we studied the shifts of PAB communities to seasonal environmental fluctuations in tropical China. Trophic state index (TSI) indicated that the studied reservoirs ranged from mesotrophic to eutrophic state with a gradual increase in TSI from 31 to 58. In eutrophic reservoirs, Cyanobacteria, especially Raphidiopsis raciborskii, significantly increased in its relative abundance from the wet to dry season, but Synechococcales and Microcystaceae decreased. In contrast, the relative abundance of Clostridia, Bacilli, Coriobacteriia, Enterobacteriales, and Vibrionales were more susceptible to seasonal environmental fluctuations in mesotrophic than eutrophic reservoirs. PAB co-occurrence relationships in mesotrophic reservoirs varied more greatly in response to seasonal environmental fluctuations, compared with eutrophic reservoirs, in terms of topological properties of connectedness, average degree, robustness, and vulnerability. Our results further demonstrated that the seasonal stability of PAB co-occurrence relationships was strongly correlative with TSI through mediating key bacterial taxa and community biodiversity. We proposed that eutrophication dramatically reduced the seasonal variation of PAB community compositions and co-occurring relationships in reservoir ecosystems.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-03-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11925149/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142603871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}