AnaerobePub Date : 2024-04-12DOI: 10.1016/j.anaerobe.2024.102853
Sergio Ruiz-Saavedra , Nuria Salazar , Adolfo Suárez , Ylenia Diaz , Carmen González del Rey , Sonia González , Clara G. de los Reyes-Gavilán
{"title":"Human fecal alpha-glucosidase activity and its relationship with gut microbiota profiles and early stages of intestinal mucosa damage","authors":"Sergio Ruiz-Saavedra , Nuria Salazar , Adolfo Suárez , Ylenia Diaz , Carmen González del Rey , Sonia González , Clara G. de los Reyes-Gavilán","doi":"10.1016/j.anaerobe.2024.102853","DOIUrl":"https://doi.org/10.1016/j.anaerobe.2024.102853","url":null,"abstract":"<div><h3>Objectives</h3><p>We investigated potential relationships among initial lesions of the intestinal mucosa, fecal enzymatic activities and microbiota profiles.</p></div><div><h3>Methods</h3><p>Fecal samples from 54 volunteers were collected after recruitment among individuals participating in a colorectal cancer (CRC) screening program in our region (Northern Spain) or attending for consultation due to clinical symptoms; intestinal mucosa samples were resected during colonoscopy. Enzymatic activities were determined in fecal supernatants by a semi-quantitative method. The fecal microbiota composition was determined by 16S rRNA gene-based sequencing. The results were compared between samples from clinical diagnosis groups (controls and polyps), according with the type of polyp (hyperplastic polyps or conventional adenomas) and considering the grade of dysplasia for conventional adenomas (low and high grade dysplasia).</p></div><div><h3>Results</h3><p>High levels of α-glucosidase activity were more frequent among samples from individuals diagnosed with intestinal polyps, reaching statistical significance for conventional adenomas and for low grade dysplasia adenomas when compared to controls. Regarding the microbiota profiles, higher abundance of <em>Christensenellaceae_R-7</em> group and <em>Oscillospiraceae</em>_<em>UCG-002</em> were found in fecal samples displaying low α-glucosidase activity as compared with those with higher activity as well as in controls with respect to conventional adenomas. A relationship was evidenced among intestinal mucosal lesions, gut glucosidase activities and intestinal microbiota profiles.</p></div><div><h3>Conclusions</h3><p>Our findings suggest a relationship among altered fecal α-glucosidase levels, the presence of intestinal mucosal lesions, which can be precursors of CRC, and shifts in defined microbial groups of the fecal microbiota.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102853"},"PeriodicalIF":2.3,"publicationDate":"2024-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000362/pdfft?md5=47ffa1eaeb36489ae825c3cddf0c8b6a&pid=1-s2.0-S1075996424000362-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140555158","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}
AnaerobePub Date : 2024-04-10DOI: 10.1016/j.anaerobe.2024.102856
Lanxin Ou , Bijin Ye , Mingfei Sun , Nanshan Qi , Juan Li , Minna Lv , Xuhui Lin , Haiming Cai , Junjing Hu , Yongle Song , Xiangjie Chen , Yibin Zhu , Lijun Yin , Jianfei Zhang , Shenquan Liao , Haoji Zhang
{"title":"Mechanisms of intestinal epithelial cell damage by Clostridium perfringens","authors":"Lanxin Ou , Bijin Ye , Mingfei Sun , Nanshan Qi , Juan Li , Minna Lv , Xuhui Lin , Haiming Cai , Junjing Hu , Yongle Song , Xiangjie Chen , Yibin Zhu , Lijun Yin , Jianfei Zhang , Shenquan Liao , Haoji Zhang","doi":"10.1016/j.anaerobe.2024.102856","DOIUrl":"10.1016/j.anaerobe.2024.102856","url":null,"abstract":"<div><p><em>Clostridium perfringens</em>, a Gram-positive bacterium, causes intestinal diseases in humans and livestock through its toxins, related to alpha toxin (CPA), beta toxin (CPB), <em>C. perfringens</em> enterotoxin (CPE), epsilon toxin (ETX), Iota toxin (ITX), and necrotic enteritis B-like toxin (NetB). These toxins disrupt intestinal barrier, leading to various cell death mechanisms such as necrosis, apoptosis, and necroptosis. Additionally, non-toxin factors like adhesins and degradative enzymes contribute to virulence by enhancing colonization and survival of <em>C. perfringens</em>. A vicious cycle of intestinal barrier breach, misregulated cell death, and subsequent inflammation is at the heart of chronic inflammatory and infectious gastrointestinal diseases. Understanding these mechanisms is essential for developing targeted therapies against <em>C. perfringens</em>-associated intestinal diseases.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102856"},"PeriodicalIF":2.3,"publicationDate":"2024-04-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000398/pdfft?md5=72253330a0f355abc010d876a62a219d&pid=1-s2.0-S1075996424000398-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140788105","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}
AnaerobePub Date : 2024-04-06DOI: 10.1016/j.anaerobe.2024.102851
Marion Saunier , Louis-Charles Fortier , Olga Soutourina
{"title":"RNA-based regulation in bacteria-phage interactions","authors":"Marion Saunier , Louis-Charles Fortier , Olga Soutourina","doi":"10.1016/j.anaerobe.2024.102851","DOIUrl":"https://doi.org/10.1016/j.anaerobe.2024.102851","url":null,"abstract":"<div><p>Interactions of bacteria with their viruses named bacteriophages or phages shape the bacterial genome evolution and contribute to the diversity of phages. RNAs have emerged as key components of several anti-phage defense systems in bacteria including CRISPR-Cas, toxin-antitoxin and abortive infection. Frequent association with mobile genetic elements and interplay between different anti-phage defense systems are largely discussed. Newly discovered defense systems such as retrons and CBASS include RNA components. RNAs also perform their well-recognized regulatory roles in crossroad of phage-bacteria regulatory networks. Both regulatory and defensive function can be sometimes attributed to the same RNA molecules including CRISPR RNAs. This review presents the recent advances on the role of RNAs in the bacteria-phage interactions with a particular focus on clostridial species including an important human pathogen, <em>Clostridioides difficile</em>.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102851"},"PeriodicalIF":2.3,"publicationDate":"2024-04-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000349/pdfft?md5=8b178f0cd4f8113a7a2463a6ddc04d55&pid=1-s2.0-S1075996424000349-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140540345","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}
AnaerobePub Date : 2024-04-04DOI: 10.1016/j.anaerobe.2024.102844
Hailee N. Nerber, Joseph A. Sorg
{"title":"The small acid-soluble proteins of spore-forming organisms: Similarities and differences in function","authors":"Hailee N. Nerber, Joseph A. Sorg","doi":"10.1016/j.anaerobe.2024.102844","DOIUrl":"https://doi.org/10.1016/j.anaerobe.2024.102844","url":null,"abstract":"<div><p>The small acid-soluble proteins are found in all endospore-forming organisms and are a major component of spores. Through their DNA binding capabilities, the SASPs shield the DNA from outside insults (e.g., UV and genotoxic chemicals). The absence of the major SASPs results in spores with reduced viability when exposed to UV light and, in at least one case, the inability to complete sporulation. While the SASPs have been characterized for decades, some evidence suggests that using newer technologies to revisit the roles of the SASPs could reveal novel functions in spore regulation.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102844"},"PeriodicalIF":2.3,"publicationDate":"2024-04-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000271/pdfft?md5=43c02569759ce5a7d997c1defcfc5882&pid=1-s2.0-S1075996424000271-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140543038","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}
AnaerobePub Date : 2024-03-28DOI: 10.1016/j.anaerobe.2024.102842
Isaura Rigo, Mary K. Young, Mayuresh M. Abhyankar, Feifan Xu, Girija Ramakrishnan, Farha Naz, Gregory R. Madden , William A. Petri
{"title":"The impact of existing total anti-toxin B IgG immunity in outcomes of recurrent Clostridioides difficile infection","authors":"Isaura Rigo, Mary K. Young, Mayuresh M. Abhyankar, Feifan Xu, Girija Ramakrishnan, Farha Naz, Gregory R. Madden , William A. Petri","doi":"10.1016/j.anaerobe.2024.102842","DOIUrl":"10.1016/j.anaerobe.2024.102842","url":null,"abstract":"<div><p>Late anti-toxin-B humoral immunity acquired after treatment is important for preventing recurrent <em>Clostridioides difficile</em> infection. We prospectively-measured anti-toxin-B IgG and neutralization titers at diagnosis as potential early predictors of recurrence. High anti-toxin-B-IgG/neutralizing antibodies were associated with short-lasting protection within 6-weeks, however, no difference in recurrence risk was observed by 90-days post-infection.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102842"},"PeriodicalIF":2.3,"publicationDate":"2024-03-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000258/pdfft?md5=0f538c143729db31974658bf8b4a2a0a&pid=1-s2.0-S1075996424000258-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140326265","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}
AnaerobePub Date : 2024-03-27DOI: 10.1016/j.anaerobe.2024.102839
Laura M. Cersosimo , Jay N. Worley , Lynn Bry
{"title":"Approaching toxigenic Clostridia from a one health perspective","authors":"Laura M. Cersosimo , Jay N. Worley , Lynn Bry","doi":"10.1016/j.anaerobe.2024.102839","DOIUrl":"10.1016/j.anaerobe.2024.102839","url":null,"abstract":"<div><p>Spore-forming pathogens have a unique capacity to thrive in diverse environments, and with temporal persistence afforded through their ability to sporulate. Their prevalence in diverse ecosystems requires a One Health approach to identify critical reservoirs and outbreak-associated transmission chains, given their capacity to freely move across soils, waterways, foodstuffs and as commensals or infecting pathogens in human and animal populations. Among anaerobic spore-formers, genomic resources for pathogens including <em>C</em>. <em>botulinum</em>, <em>C</em>. <em>difficile</em>, and <em>C</em>. <em>perfringens</em> enable our capacity to identify common and unique factors that support their persistence in diverse reservoirs and capacity to cause disease. Publicly available genomic resources for spore-forming pathogens at NCBI's Pathogen Detection program aid outbreak investigations and longitudinal monitoring in national and international programs in public health and food safety, as well as for local healthcare systems. These tools also enable research to derive new knowledge regarding disease pathogenesis, and to inform strategies in disease prevention and treatment. As global community resources, the continued sharing of strain genomic data and phenotypes further enhances international resources and means to develop impactful applications. We present examples showing use of these resources in surveillance, including capacity to assess linkages among clinical, environmental, and foodborne reservoirs and to further research investigations into factors promoting their persistence and virulence in different settings.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102839"},"PeriodicalIF":2.3,"publicationDate":"2024-03-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140326264","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}
AnaerobePub Date : 2024-03-26DOI: 10.1016/j.anaerobe.2024.102837
Deiziane V.S. Costa , Natalie Pham , Andrea V. Loureiro , Suemin E. Yang , Brian W. Behm , Cirle A. Warren
{"title":"Clostridioides difficile infection promotes gastrointestinal dysfunction in human and mice post-acute phase of the disease","authors":"Deiziane V.S. Costa , Natalie Pham , Andrea V. Loureiro , Suemin E. Yang , Brian W. Behm , Cirle A. Warren","doi":"10.1016/j.anaerobe.2024.102837","DOIUrl":"10.1016/j.anaerobe.2024.102837","url":null,"abstract":"<div><h3>Objectives</h3><p>In the US, <em>Clostridioides difficile</em> (<em>C. difficile</em>) infection (CDI) is the 8th leading cause of hospital readmission and 7th for mortality among all gastrointestinal (GI) disorders. Here, we investigated GI dysfunction post-CDI in humans and mice post-acute infection.</p></div><div><h3>Materials and methods</h3><p>From March 2020 to July 2021, we reviewed the clinical records of 67 patients referred to the UVA Complicated <em>C. difficile c</em>linic for fecal microbiota transplantation (FMT) eligibility. C57BL/6 mice were infected with <em>C. difficile</em> and clinical scores were determined daily. Stool samples from mice were collected to measure the shedding of <em>C. difficile</em> and myeloperoxidase (MPO) levels. On day 21 post-infection, Evans's blue and FITC-70kDa methods were performed to evaluate GI motility in mice.</p></div><div><h3>Results</h3><p>Of the 67 patients evaluated at the <em>C. difficile</em> clinic, 40 patients (59.7%) were confirmed to have CDI, and 22 patients (32.8%) with post-CDI IBS (diarrhea-type, constipation-type, and mixed-type). In infected mice, levels of MPO in stools and clinical score were higher on day 3. On day 21, mice recovered from body weight loss induced by CDI, and fecal MPO was undetectable. The total GI transit time (TGITT) and FITC-70kDa levels on the proximal colon were increased in infected mice (p = 0.002), suggesting a constipation phenotype post-acute phase of CDI. A positive correlation intestinal inflammation on day 3 and TGITT on day 21 was observed.</p></div><div><h3>Conclusion</h3><p>In conclusion, post-infection intestinal dysfunction occurs in humans and mice post-CDI. Importantly, we have validated in the mouse model that CDI causes abnormal GI transit in the recovery phase of the disease, indicating the potential utility of the model in exploring the underlying mechanisms of post-infectious IBS in humans.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102837"},"PeriodicalIF":2.3,"publicationDate":"2024-03-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140288013","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}
AnaerobePub Date : 2024-03-25DOI: 10.1016/j.anaerobe.2024.102843
Jourdan E. Lakes , Jessica L. Ferrell , Mark A. Berhow , Michael D. Flythe
{"title":"Antimicrobial effects of cannabidiol on select agriculturally important Clostridia","authors":"Jourdan E. Lakes , Jessica L. Ferrell , Mark A. Berhow , Michael D. Flythe","doi":"10.1016/j.anaerobe.2024.102843","DOIUrl":"10.1016/j.anaerobe.2024.102843","url":null,"abstract":"<div><p>Amino acid-fermenting Clostridia have undesirable effects in agricultural systems, which can be mitigated by antibiotics, but resistance necessitates alternatives. Here, we demonstrate the efficacy of cannabidiol on growth and ammonia inhibition of five agriculturally relevant Clostridia: <em>Clostridium sporogenes</em>, <em>Peptostreptococcus</em> spp., <em>Clostridioides difficile</em>, <em>Acetoanaerobium sticklandii</em>, and <em>Clostridium aminophilum</em>.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"87 ","pages":"Article 102843"},"PeriodicalIF":2.3,"publicationDate":"2024-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S107599642400026X/pdfft?md5=c4ef856ff01518283ff4498b29dbb0ba&pid=1-s2.0-S107599642400026X-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140304465","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}
AnaerobePub Date : 2024-03-21DOI: 10.1016/j.anaerobe.2024.102841
G. Brett Moreau , Farha Naz , William A. Petri Jr.
{"title":"Fecal microbiota transplantation stimulates type 2 and tolerogenic immune responses in a mouse model","authors":"G. Brett Moreau , Farha Naz , William A. Petri Jr.","doi":"10.1016/j.anaerobe.2024.102841","DOIUrl":"10.1016/j.anaerobe.2024.102841","url":null,"abstract":"<div><h3>Objectives</h3><p><em>Clostridioides difficile</em> infection (CDI) is the leading hospital-acquired infection in North America. While previous work on fecal microbiota transplantation (FMT), a highly effective treatment for CDI, has focused on colonization resistance mounted against <em>C. difficile</em> by FMT-delivered commensals, the effects of FMT on host gene expression are relatively unexplored. This study aims to identify transcriptional changes associated with FMT, particularly changes associated with protective immune responses.</p></div><div><h3>Methods</h3><p>Gene expression was assessed on day 2 and day 7 after FMT in mice after antibiotic-induced dysbiosis. Flow cytometry was also performed on colon and mesenteric lymph nodes at day 7 to investigate changes in immune cell populations.</p></div><div><h3>Results</h3><p>FMT administration after antibiotic-induced dysbiosis successfully restored microbial alpha diversity to levels of donor mice by day 7 post-FMT. Bulk RNA sequencing of cecal tissue at day 2 identified immune genes, including both pro-inflammatory and Type 2 immune pathways as upregulated after FMT. RNA sequencing was repeated on day 7 post-FMT, and expression of these immune genes was decreased along with upregulation of genes associated with restoration of intestinal homeostasis. Immunoprofiling on day 7 identified increased colonic CD45<sup>+</sup> immune cells that exhibited dampened Type 1 and heightened regulatory and Type 2 responses. These include an increased abundance of eosinophils, alternatively activated macrophages, Th2, and T regulatory cell populations.</p></div><div><h3>Conclusion</h3><p>These results highlight the impact of FMT on host gene expression, providing evidence that FMT restores intestinal homeostasis after antibiotic treatment and facilitates tolerogenic and Type 2 immune responses.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"86 ","pages":"Article 102841"},"PeriodicalIF":2.3,"publicationDate":"2024-03-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1075996424000246/pdfft?md5=d265c57f3782405811faf04b4a2cd539&pid=1-s2.0-S1075996424000246-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140193151","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}
AnaerobePub Date : 2024-03-21DOI: 10.1016/j.anaerobe.2024.102838
Elie Bou Sanayeh , Mark Tawfik , Marina Makram , Georges Khattar , Faris Qaqish , Sudeep Acharya , Janet Farag , Michel Chalhoub , Allison Glaser
{"title":"Hungatella hathewayi bacteremia due to acute appendicitis: A case report and a narrative review","authors":"Elie Bou Sanayeh , Mark Tawfik , Marina Makram , Georges Khattar , Faris Qaqish , Sudeep Acharya , Janet Farag , Michel Chalhoub , Allison Glaser","doi":"10.1016/j.anaerobe.2024.102838","DOIUrl":"10.1016/j.anaerobe.2024.102838","url":null,"abstract":"<div><p><em>Hungatella</em> species, including <em>Hungatella hathewayi</em> and <em>Hungatella effluvii</em>, previously identified as part of the <em>Clostridium</em> genus, are anaerobic bacteria primarily residing in the gut microbiome, with infrequent implications in human infections. This article presents the case of an 87-year-old Asian male admitted for a hyperosmolar hyperglycemic state with septic shock secondary to <em>Hungatella hathewayi</em> bacteremia originating from acute appendicitis. Remarkably, the bacterium was detected in the blood 48 hours before the emergence of clinical and radiographic evidence of acute appendicitis. Additionally, we conducted a literature review to identify all documented human infections caused by <em>Hungatella</em> species. Timely microbial identification in such cases is essential for implementing targeted antibiotic therapy and optimizing clinical outcomes.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"86 ","pages":"Article 102838"},"PeriodicalIF":2.3,"publicationDate":"2024-03-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140193152","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}