Maryse D Berkhout, Athanasia Ioannou, Yuvashankar Kavanal Jayaprakash, Caroline M Plugge, Clara Belzer
{"title":"Milk and mucin glycans orchestrate a synthetic infant gut microbiota structure.","authors":"Maryse D Berkhout, Athanasia Ioannou, Yuvashankar Kavanal Jayaprakash, Caroline M Plugge, Clara Belzer","doi":"10.1093/femsec/fiaf069","DOIUrl":"10.1093/femsec/fiaf069","url":null,"abstract":"<p><p>Glycans are crucial for infant gut microbiota development. Human milk contains prebiotic human milk oligosaccharides (HMOs) that stimulate gut microbes. Simultaneously, the glycan-rich mucus layer develops and attracts mucin glycan-degrading bacteria. As HMOs and mucin are degraded by homologous enzymes, bacterial glycan-degrading abilities overlap. However, less is known about how infant gut microbial communities form when both types of glycans are available. To study this, we created a synthetic community with specialist glycan degraders and cross-feeders from the infant gut (BabyBac). We evaluated it in different in vitro conditions including combinations of diet-derived [HMOs, galactooligosaccharides (GOS), and fructooligosaccharides (FOS)] and mucus glycans. Glycan combinations significantly affected the community composition and metabolic output. The glycan type affected the overall community, with mucin and HMOs being the top drivers of variation. HMOs favoured glycan degraders and cross-feeders, whereas mucin glycan degrader Akkermansia muciniphila was outcompeted. Conversely, when mucin was present, A. muciniphila thrived. Addition of mucin monomers and 2'-FL to GOS/FOS did not reinstate A. muciniphila abundance. This suggests that A. muciniphila cannot compete with infant-related bacteria without the complete mucin structure. Overall, our findings suggest that the interplay between dietary and mucus glycans creates niche differentiation in the infant gut microbiota.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12268331/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144483746","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}
Nichole M Giani, Shen Jean Lim, Laurie C Anderson, Audrey T Paterson, Annette Summers Engel, Barbara J Campbell
{"title":"Variation in accessory and horizontal gene transfer-associated genes drives lucinid endosymbiont diversity.","authors":"Nichole M Giani, Shen Jean Lim, Laurie C Anderson, Audrey T Paterson, Annette Summers Engel, Barbara J Campbell","doi":"10.1093/femsec/fiaf074","DOIUrl":"10.1093/femsec/fiaf074","url":null,"abstract":"<p><p>Lucinid bivalves harbor environmentally acquired endosymbionts within the class Gammaproteobacteria and genus Candidatus Thiodiazotropha. Despite recent studies focused on lucinid endosymbiont genomic and functional diversity, processes influencing species diversity have been understudied. From the analysis of 333 metagenome-assembled genomes (MAGs) from 40 host species across 8 waterbodies and 77 distinct locations, 272 were high quality MAGs of Ca. Thiodiazotropha endosymbionts that represented 11 genomospecies. Of those, two new genomospecies from lucinids collected from The Bahamas and Florida (USA) were identified, Ca. Thiodiazotropha fisheri and Ca. Thiodiazotropha grosi. Metabolic specialization was evident, such as potential adaptations to diverse carbon sources based on detection of one-carbon (C1) metabolic genes in eight genomospecies. Genes associated with defense, symbiosis/pathogenesis, and horizontal gene transfer (HGT) were also distinct across genomospecies. For instance, Ca. T. taylori exhibited lower abundances of HGT-associated genes compared to other genomospecies, particularly Ca. T. endolucinida, Ca. T. lotti, and Ca. T. weberae. HGT-associated genes were linked to previously unreported retron-type reverse transcriptases, dsDNA phages, and phage resistance. Collectively, the pangenome highlights how lucinid endosymbiont diversity has been shaped by geographic and host-specific interactions linked to gene loss and HGT through time.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12278820/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144599871","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}
Rachel L Vannette, Neal M Williams, Stephen S Peterson, Alexia N Martin
{"title":"Pollen diet, more than geographic distance, shapes provision microbiome composition in two species of cavity-nesting bees.","authors":"Rachel L Vannette, Neal M Williams, Stephen S Peterson, Alexia N Martin","doi":"10.1093/femsec/fiaf067","DOIUrl":"10.1093/femsec/fiaf067","url":null,"abstract":"<p><p>The microbial composition of stored food can influence its stability and the microbial species consumed by the organism feeding on it. Many bee species store nectar and pollen in provisions constructed to feed developing offspring. Yet, whether microbial composition is determined by the pollen types within provisions, variation between bee species at the same nesting sites, or geographic distance was unclear. Here, we sampled two species of cooccurring cavity nesting bees in the genus Osmia at 13 sites in California and examined the composition of pollen, fungi, and bacteria in provisions. Pollen composition explained 15% of variation in bacterial composition and ∼30% of variation in fungal composition, whereas spatial distance among sites explained minimal additional variation. Symbiotic microbe genera Ascosphaera, Sodalis, and Wolbachia showed contrasting patterns of association with pollen composition, suggesting distinct acquisition and transmission routes for each. Comparing provisions from both bee species comprised of the same pollens points to environmental acquisition rather than bee species as a key factor shaping the early stages of the bee microbiome in Osmia. The patterns we observed also contrast with Apilactobacillus-dominated provision microbiome in other solitary bee species, suggesting variable mechanisms of microbial assembly in stored food among bee species.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12320775/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144741738","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":"Emerging probiotics: future therapeutics for human gut health.","authors":"Sylvia H Duncan, Carlos Sabater","doi":"10.1093/femsec/fiaf077","DOIUrl":"10.1093/femsec/fiaf077","url":null,"abstract":"<p><p>The microbial communities that colonize the human large intestine can influence many aspects of health and Bacillota strains, in particular, have been proposed as next-generation probiotics. Of note are strains including fibre-degraders, butyrate producers, lactate producers and utilizers, and other beneficial metabolic activities that are important for health. To illustrate the potential applications of colonic bacteria to design novel prebiotic formulations, a comparative genomics analysis of 16 bacterial strains isolated from the human gut was performed. This analysis revealed a high number of carbohydrate-active enzymes (CAZymes) in the genome sequences of understudied Lachnospiraceae and Oscillospiraceae members including Roseburia intestinalis L1-82, Roseburia faecis M72/1, Butyrivibrio fibrisolvens 16-4, and Ruminococcus bicirculans 80/3, ranging from 32 to 56 CAZymes across different strains. These strains showed complementary enzymatic profiles covering a wide range of different activities required to degrade prebiotic substrates derived from vegetable sources such as arabino- and xylo-oligosaccharides and pectic-oligosaccharides. These metabolic differences highlight the potential of these strains to cross feed and to allow the design novel probiotic consortia for microbiota-oriented interventions that could target specific disease conditions. These bacterial strains are, however, strict anaerobes and therefore special measures may need to be put in place to overcome these limitations.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12342623/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144706932","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":"Sulfidic toluene mineralization by aquifer microbial communities at different temperatures.","authors":"Mohammad Sufian Bin Hudari, Carsten Vogt","doi":"10.1093/femsec/fiaf079","DOIUrl":"10.1093/femsec/fiaf079","url":null,"abstract":"<p><p>High-temperature aquifer thermal energy storage (HT-ATES) is a carbon-neutral technology in the heating and cooling sector particularly suitable for urban areas, where aquifers are often contaminated with hydrocarbons. How HT-ATES could influence the natural degradation of contaminants such as hydrocarbons has hardly been investigated. Here, we determined the effects of temperature and temperature shifts on the capability of aquifer microbial communities to mineralize the model hydrocarbon toluene at sulfate-reducing conditions. Distinct toluene-mineralizing, sulfate-reducing consortia were enriched from material of two hydrocarbon-contaminated field sites at 12°C, 20°C, 25°C, 38°C, and 45°. Lowest toluene mineralization rates were observed at 38°C, and highest rates were observed at 45°C. Consortia adapted to 12°C or 25°C were generally negatively impacted by temporary or permanent temperature shifts to temperatures ≥ 38°C. Desulfosporosinus phylotypes dominated enrichments at 12°C, indicating a major role for toluene mineralization at in situ temperatures. At 20°C-25°C, typical sulfate-reducing genera such as Desulfoprunum, Desulfallas or Pelotomaculum were abundant, indicating synergistic relationships of various toluene degraders belonging to different taxa. The communities grown at 45°C were dominated by putative thermophilic phylotypes affiliated to the phyla Bacillota or Caldiserica. Overall, our data indicate that 45°C is the upper limit for anaerobic toluene mineralization of the investigated communities.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12342453/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144741739","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":"Genomic survey reveals no detectable bacteriophage activity in Mycobacterium bovis across a large population.","authors":"Daniela Pinto, Inês Mendes, Mónica V Cunha","doi":"10.1093/femsec/fiaf072","DOIUrl":"10.1093/femsec/fiaf072","url":null,"abstract":"<p><p>Phages are major drivers of bacterial evolution, yet their ecological and evolutionary interactions with Mycobacterium bovis, a key member of the Mycobacterium tuberculosis complex (MTBC), remain understudied. In this work, we investigate the elusive phage-bacterium interface in M. bovis by integrating comparative genomics of 200 isolates from infected animals with molecular analyses of M. bovis-positive environmental samples. Despite employing diverse and complementary approaches, we found no evidence of active or recent phage infections: no novel prophages beyond the conserved phiRv1, no expansion of CRISPR arrays, and no cooccurrence of M. bovis and mycobacteriophages in host tissues or environmental matrices. Intriguingly, we identified multiple independent excision events of phiRv1 across closely related lineages, suggesting recent prophage mobilization driven by unidentified ecological or genomic triggers. These findings echo previous observations in M. tuberculosis and point toward a stable, phage-scarce landscape across MTBC members. Our results raise compelling questions about the barriers to phage predation in M. bovis, the functionality of its CRISPR-Cas system, and the selective pressures underlying prophage retention and loss. By shedding light on these underexplored dynamics, our study reveals critical gaps in the ecological understanding of M. bovis and highlights opportunities for phage-based innovation in TB control.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12268328/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144559614","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}
Aoife M Duff, Madeline Giles, Syaliny Ganasamurthy, Antonia Santos, Sergio E Morales, Fiona Brennan
{"title":"Counting soil microbial communities: the impact of qPCR platform and mastermix on accuracy and precision.","authors":"Aoife M Duff, Madeline Giles, Syaliny Ganasamurthy, Antonia Santos, Sergio E Morales, Fiona Brennan","doi":"10.1093/femsec/fiaf073","DOIUrl":"10.1093/femsec/fiaf073","url":null,"abstract":"<p><p>Quantitative polymerase chain reaction (qPCR) is widely used in soil microbial ecology to quantify microbial communities, but its accuracy can be compromised by coextracted inhibitors. Furthermore, large-scale international studies involving multiple laboratories or meta-analyses studies can introduce variation in qPCR results when data generated from different sources are compared. This study evaluated the performance of four commercial mastermixes across different soil types, a mock community, and a positive template control against three targets on three widely used platforms. Sensitivity to inhibitors was tested, with one mastermix affected, although this was mitigated by adding 1 mg/ml bovine serum albumin. Amplification success varied by mastermix, platform, gene, and sample matrix. Most mastermix-platform combinations showed low accuracy emphasizing the need for careful pairing. Precision was primarily influenced by gene target, followed by platform, sample matrix, and mastermix, and was reduced at lower template concentrations. Only 64.67% of intraassay (within an assay) measurements meet accepted thresholds. Interassay (between platforms) quantification was unreliable due to significant variability, which increased the risk of inaccurate data interpretation. The study highlights the necessity of considering inter- and intraassay variation, assay accuracy, and inhibitors that may impact sample amplification when utilizing qPCR for quantification of microbial communities in environmental samples.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144698008","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Anna J Wallenius, Jessica Venetz, Olga M Zygadlowska, Wytze K Lenstra, Niels A G M van Helmond, Paula Dalcin Martins, Caroline P Slomp, Mike S M Jetten
{"title":"A ubiquitous and diverse methanogenic community drives microbial methane cycling in eutrophic coastal sediments.","authors":"Anna J Wallenius, Jessica Venetz, Olga M Zygadlowska, Wytze K Lenstra, Niels A G M van Helmond, Paula Dalcin Martins, Caroline P Slomp, Mike S M Jetten","doi":"10.1093/femsec/fiaf075","DOIUrl":"10.1093/femsec/fiaf075","url":null,"abstract":"<p><p>Coastal areas contribute over 75% of global marine methane emissions, a proportion predicted to increase with anthropogenic eutrophication and deoxygenation. Prolonged low oxygen and high organic matter input can disrupt the methane cycle, favoring methane production over oxidation. However, factors influencing this imbalance remain unclear. Here, we show that methanogenesis dominates microbial methane cycling in the anoxic sediments of eutrophic coastal marine Lake Grevelingen (The Netherlands) after summer stratification. A shallow sulfate-methane transition zone (SMTZ; 5-15 cm depth) was observed, with high methane concentrations below. Methane was produced in all investigated layers, while methane oxidation was restricted to the narrow SMTZ. Amplicon sequencing, metagenomics, and incubations revealed a metabolically and phylogenetically diverse methanogenic community with niche separation, and methylotrophic methanogenesis prevalent in all layers. Two clades of ANME archaea, ANME-2a/b and ANME-3, were restricted to a narrow zone together with their putative syntrophic sulfate-reducing bacteria, coinciding with the observed methane oxidation activity. Our results suggest that eutrophication and deoxygenation will further contribute to rising methane emissions, tilting the microbial methane cycle toward increased methanogenesis, and decreasing the efficiency of the microbial methane filter.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12287602/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144616859","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}
Carol de Ram, Maryse D Berkhout, Carolina O Pandeirada, Jean-Paul Vincken, Guido J E J Hooiveld, Clara Belzer, Henk A Schols
{"title":"Distinct in vitro utilization and degradation of porcine gastric mucin glycans by human intestinal bacteria.","authors":"Carol de Ram, Maryse D Berkhout, Carolina O Pandeirada, Jean-Paul Vincken, Guido J E J Hooiveld, Clara Belzer, Henk A Schols","doi":"10.1093/femsec/fiaf066","DOIUrl":"10.1093/femsec/fiaf066","url":null,"abstract":"<p><p>Mucin glycan degradation and utilization by microbes colonizing the human intestine is an essential host-microbe interaction. In this study, degradation and utilization of porcine gastric mucin glycans by Akkermansia muciniphila, Ruminococcus torques, Bacteroides thetaiotaomicron, co-cultures, and a synthetic bacterial community were investigated over time. Liquid chromatography-tandem mass spectrometry O-glycan patterns revealed that all three monocultures removed sialic acid residues. Furthermore, R. torques first targeted fucosylated O-glycans, while A. muciniphila and B. thetaiotaomicron equally favoured fucosylated and non-fucosylated O-glycans. A. muciniphila, R. torques, and B. thetaiotaomicron favoured degradation of first core 2 O-glycan structures relative to core 1 O-glycan structures. Co-cultures, compared to monocultures, demonstrated different O-glycan degradation patterns suggesting distinct ecological interactions between the bacteria. Although extensive O-glycan degradation was observed by the monocultures and co-cultures, only the synthetic community completely degraded all O-glycans within 24 h. Regarding degradation of the constituent N-glycans, matrix-assisted laser desorption ionization-time-of-flight mass spectrometry showed that A. muciniphila and R. torques can partly degrade N-glycans, B. thetaiotaomicron can completely degrade high-mannose N-glycans, and the synthetic community can degrade all N-glycans. The utilization of mucin glycans was observed by production of different metabolites among the bacteria. These results indicate that degradation of mucin glycans depends on microbial interactions and ecological networks.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.5,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12258148/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144527112","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}
Silke Van den Wyngaert, Ali Nawaz, Elisabet Alacid, Steffaney M Wood-Rocca, Albert Reñé, Esther Garcés, Anke Kremp, Christian Wurzbacher
{"title":"Dynamics of zoosporic parasites in summer phytoplankton communities of the Baltic Sea.","authors":"Silke Van den Wyngaert, Ali Nawaz, Elisabet Alacid, Steffaney M Wood-Rocca, Albert Reñé, Esther Garcés, Anke Kremp, Christian Wurzbacher","doi":"10.1093/femsec/fiaf081","DOIUrl":"10.1093/femsec/fiaf081","url":null,"abstract":"<p><p>Zoosporic parasites significantly influence aquatic ecosystems by infecting various phytoplankton taxa, but their interactions in brackish ecosystems remain largely unexplored. This study explores microbial communities and parasitic interactions with summer phytoplankton communities at six brackish coastal sites in the northern Baltic Sea. We hypothesized that small-scale spatial heterogeneity in environmental conditions would lead to distinct assemblages of microbial communities and phytoplankton-parasite interactions. By combining DNA metabarcoding, single-cell sequencing, and microscopy, we provide the first community-level qualitative and quantitative assessment of zoosporic parasites infecting summer phytoplankton in the Baltic Sea. Microbial communities varied significantly across sites, with salinity as primary driver of eukaryotic diversity. Chytrid fungi were the dominant parasites, infecting green algae, diatoms, and filamentous cyanobacteria, with infection rates up to 5.8% of phytoplankton biomass. Sequences from brackish chytrids clustered with those from freshwater environments, reflecting polyphyletic patterns linked to host taxa. Phytoplankton-parasite interactions were influenced by host abundance and site-specific conditions with correlation analysis suggesting broader host ranges and potential generalist behavior in some chytrid species. Additionally, an unidentified oomycete infected up to 85% of the toxic bloom-forming cyanobacterium Nodularia spp. This study highlights the ecological relevance of zoosporic parasites in the Baltic Sea and emphasizes the need for further research into their role in phytoplankton bloom dynamics.</p>","PeriodicalId":12312,"journal":{"name":"FEMS microbiology ecology","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12345203/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144834678","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}