Julien Amoros, Noor Fattar, Marie Buysse, Meriem Louni, Joanne Bertaux, Didier Bouchon, Olivier Duron
{"title":"Reassessment of the genetic basis of natural rifampin resistance in the genus Rickettsia","authors":"Julien Amoros, Noor Fattar, Marie Buysse, Meriem Louni, Joanne Bertaux, Didier Bouchon, Olivier Duron","doi":"10.1002/mbo3.1431","DOIUrl":"10.1002/mbo3.1431","url":null,"abstract":"<p><i>Rickettsia</i>, a genus of obligate intracellular bacteria, includes species that cause significant human diseases. This study challenges previous claims that the Leucine-973 residue in the RNA polymerase beta subunit is the primary determinant of rifampin resistance in <i>Rickettsia</i>. We investigated a previously untested <i>Rickettsia</i> species, <i>R. lusitaniae</i>, from the Transitional group and found it susceptible to rifampin, despite possessing the Leu-973 residue. Interestingly, we observed the conservation of this residue in several rifampin-susceptible species across most <i>Rickettsia</i> phylogenetic groups. Comparative genomics revealed potential alternative resistance mechanisms, including additional amino acid variants that could hinder rifampin binding and genes that could facilitate rifampin detoxification through efflux pumps. Importantly, the evolutionary history of <i>Rickettsia</i> genomes indicates that the emergence of natural rifampin resistance is phylogenetically constrained within the genus, originating from ancient genetic features shared among a unique set of closely related <i>Rickettsia</i> species. Phylogenetic patterns appear to be the most reliable predictors of natural rifampin resistance, which is confined to a distinct monophyletic subclade known as Massiliae. The distinctive features of the RNA polymerase beta subunit in certain untested <i>Rickettsia</i> species suggest that <i>R. raoultii</i>, <i>R. amblyommatis</i>, <i>R. gravesii</i>, and <i>R. kotlanii</i> may also be naturally rifampin-resistant species.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.9,"publicationDate":"2024-07-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11289727/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141855996","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}
Shannon E. Pipes, Charles R. Lovell, Katie L. Kathrein
{"title":"In vivo examination of pathogenicity and virulence in environmentally isolated Vibrio vulnificus","authors":"Shannon E. Pipes, Charles R. Lovell, Katie L. Kathrein","doi":"10.1002/mbo3.1427","DOIUrl":"10.1002/mbo3.1427","url":null,"abstract":"<p>Human exposure to <i>Vibrio vulnificus</i>, a gram-negative, halophilic environmental pathogen, is increasing. Despite this, the mechanisms of its pathogenicity and virulence remain largely unknown. Each year, hundreds of infections related to <i>V. vulnificus</i> occur, leading to hospitalization in 92% of cases and a mortality rate of 35%. The infection is severe, typically contracted through the consumption of contaminated food or exposure of an open wound to contaminated water. This can result in necrotizing fasciitis and the need for amputation of the infected tissue. Although several genes (<i>rtxA1, vvpE</i>, and <i>vvhA</i>) have been implicated in the pathogenicity of this organism, a defined mechanism has not been discovered. In this study, we examine environmentally isolated <i>V. vulnificus</i> strains using a zebrafish model (<i>Danio rerio</i>) to investigate their virulence capabilities. We found significant variation in virulence between individual strains. The commonly used marker gene of disease-causing strains, <i>vcgC</i>, did not accurately predict the more virulent strains. Notably, the least virulent strain in the study, <i>V. vulnificus</i> Sept WR1-BW6, which tested positive for <i>vcgC, vvhA</i>, and <i>rtxA1</i>, did not cause severe disease in the fish and was the only strain that did not result in any mortality. Our study demonstrates that virulence varies greatly among different environmental strains and cannot be accurately predicted based solely on genotype.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.9,"publicationDate":"2024-07-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11264103/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748591","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}
Miranda Herschel Seixas, Jeffrey S. Munroe, Erin M. Eggleston
{"title":"Bacterial diversity and geomicrobiology of Winter Wonderland ice cave, Utah, USA","authors":"Miranda Herschel Seixas, Jeffrey S. Munroe, Erin M. Eggleston","doi":"10.1002/mbo3.1426","DOIUrl":"10.1002/mbo3.1426","url":null,"abstract":"<p>The Winter Wonderland ice cave, located at an elevation of 3140 m above sea level in the Uinta Mountains of northern Utah, USA, maintains a constant sub-zero temperature. Seasonal snowmelt and rain enter the cave, freeze on the surface of the existing ice, and contribute to a 3-m-thick layered ice mass. This ice mass contains organic matter and cryogenic cave carbonates (CCCs) that date back centuries. In this study, samples of ice, liquid water, and exposed CCCs were collected to examine the bacterial communities within the cave and to determine if these communities vary spatially and between sample types. Flow cytometry showed that cell counts are an order of magnitude higher in liquid water samples than in ice. Epifluorescence microscopy and scanning electron microscopy imaging revealed potential coccoid and bacillus microbial morphologies in water samples and putative cells or calcite spherules in the CCCs. The diversity of bacteria associated with soil, identified through sequence-based analysis, supports the hypothesis that water enters the cave by filtering through soil and bedrock. A differential abundance of bacterial taxa was observed between sample types, with the greatest diversity found in CCCs. This supports a geomicrobiological framework where microbes aggregate in the water, sink into a concentrated layer, and precipitate out of the ice with the CCCs, thereby reducing the cell counts in the ice. These CCCs may provide essential nutrients for the bacteria or could themselves be products of biomineralization.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.9,"publicationDate":"2024-07-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11241547/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141590740","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}
Benjamin R. Dietz, Tyler J. Nelson, Neil E. Olszewski, Brett M. Barney
{"title":"A deoxyviolacein-based transposon insertion vector for pigmented tracer studies","authors":"Benjamin R. Dietz, Tyler J. Nelson, Neil E. Olszewski, Brett M. Barney","doi":"10.1002/mbo3.1425","DOIUrl":"10.1002/mbo3.1425","url":null,"abstract":"<p>Pigments provide a simple means to rapidly visually ascertain the quantities or presence of specific microbes in a complex community. The selection of pigment-producing colonies that are simple to differentiate from common colony phenotypes provides a high degree of certainty for the identity of pigment-tagged strains. Successful employment of pigment production is dependent on various intrinsic factors related to proper levels of gene expression and pigment production that are not always easy to predict and vary within each microbe. We have constructed a simple transposon system that incorporates the genes for the production of deoxyviolacein, a pigment produced from intracellular reserves of the amino acid tryptophan, to randomly insert these genes throughout the genome. This tool allows the user to select from many thousands of potential sites throughout a bacterial genome for an ideal location to generate the desired amount of pigment. We have applied this system to a small selection of endophytes and other model bacteria to differentiate these strains from complex communities and confirm their presence after several weeks in natural environments. We provide two examples of applications using the pigments to trace strains following introduction into plant tissues or to produce a reporter strain for extracellular nitrogen compound sensing. We recognize that this tool could have far broader utility in other applications and microbes, and describe the methodology for use by the greater scientific community.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.9,"publicationDate":"2024-07-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1425","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141580220","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}
Huayu Zheng, Kathleen D. Triplett, Eric R. Prossnitz, Pamela R. Hall, Seth M. Daly
{"title":"G protein-coupled estrogen receptor agonist G-1 decreases ADAM10 levels and NLRP3-inflammasome component activation in response to Staphylococcus aureus alpha-hemolysin","authors":"Huayu Zheng, Kathleen D. Triplett, Eric R. Prossnitz, Pamela R. Hall, Seth M. Daly","doi":"10.1002/mbo3.1423","DOIUrl":"10.1002/mbo3.1423","url":null,"abstract":"<p>The G protein-coupled estrogen receptor, also known as GPER1 or originally GPR30, is found in various tissues, indicating its diverse functions. It is typically present in immune cells, suggesting its role in regulating immune responses to infectious diseases. Our previous studies have shown that G-1, a selective GPER agonist, can limit the pathogenesis mediated by <i>Staphylococcus aureus</i> alpha-hemolysin (Hla). It aids in clearing bacteria in a mouse skin infection model and restricts the surface display of the Hla receptor, ADAM10 (a disintegrin and metalloprotease 10) in HaCaT keratinocytes. In this report, we delve into the modulation of GPER in human immune cells in relation to the NLRP3 inflammasome. We used macrophage-like differentiated THP-1 cells for our study. We found that treating these cells with G-1 reduces ATP release, decreases the activity of the caspase-1 enzyme, and lessens cell death following Hla intoxication. This is likely due to the reduced levels of ADAM10 and NLRP3 proteins, as well as the decreased display of the ADAM10 receptor in the G-1-treated THP-1 cells. Our studies, along with our previous work, suggest the potential therapeutic use of G-1 in reducing Hla susceptibility in humans. This highlights the importance of GPER in immune regulation and its potential as a therapeutic target.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-06-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1423","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141311105","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}
Robyn Dove, Emily R. Wolfe, Nathan U. Stewart, Abigail Coleman, Sara Herrejon Chavez, Daniel J. Ballhorn
{"title":"Root nodules of red alder (Alnus rubra) and sitka alder (Alnus viridis ssp. sinuata) are inhabited by taxonomically diverse cultivable microbial endophytes","authors":"Robyn Dove, Emily R. Wolfe, Nathan U. Stewart, Abigail Coleman, Sara Herrejon Chavez, Daniel J. Ballhorn","doi":"10.1002/mbo3.1422","DOIUrl":"10.1002/mbo3.1422","url":null,"abstract":"<p>The root nodules of actinorhizal plants are home to nitrogen-fixing bacterial symbionts, known as <i>Frankia</i>, along with a small percentage of other microorganisms. These include fungal endophytes and non-<i>Frankia</i> bacteria. The taxonomic and functional diversity of the microbial consortia within these root nodules is not well understood. In this study, we surveyed and analyzed the cultivable, non-<i>Frankia</i> fungal and bacterial endophytes of root nodules from red and Sitka alder trees that grow together. We examined their taxonomic diversity, co-occurrence, differences between hosts, and potential functional roles. For the first time, we are reporting numerous fungal endophytes of alder root nodules. These include <i>Sporothrix guttuliformis</i>, <i>Fontanospora</i> sp., <i>Cadophora melinii</i>, an unclassified <i>Cadophora</i>, <i>Ilyonectria destructans</i>, an unclassified <i>Gibberella</i>, <i>Nectria ramulariae</i>, an unclassified <i>Trichoderma</i>, <i>Mycosphaerella tassiana</i>, an unclassified <i>Talaromyces</i>, <i>Coniochaeta</i> sp., and <i>Sistotrema brinkmanii</i>. We are also reporting several bacterial genera for the first time: <i>Collimonas</i>, <i>Psychrobacillus</i>, and <i>Phyllobacterium</i>. Additionally, we are reporting the genus <i>Serratia</i> for the second time, with the first report having been recently published in 2023. <i>Pseudomonas</i> was the most frequently isolated bacterial genus and was found to co-inhabit individual nodules with both fungi and bacteria. We found that the communities of fungal endophytes differed by host species, while the communities of bacterial endophytes did not.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-06-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1422","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141284230","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}
Daniel P. R. Herlemann, Helen Tammert, Carmen Kivistik, Kairi Käiro, Veljo Kisand
{"title":"Distinct biogeographical patterns in snail gastrointestinal tract bacterial communities compared with sediment and water","authors":"Daniel P. R. Herlemann, Helen Tammert, Carmen Kivistik, Kairi Käiro, Veljo Kisand","doi":"10.1002/mbo3.1413","DOIUrl":"10.1002/mbo3.1413","url":null,"abstract":"<p>The factors that influence the distribution of bacterial community composition are not well understood. The role of geographical patterns, which suggest limited dispersal, is still a topic of debate. Bacteria associated with hosts face unique dispersal challenges as they often rely on their hosts, which provide specific environments for their symbionts. In this study, we examined the effect of biogeographic distances on the bacterial diversity and composition of bacterial communities in the gastrointestinal tract of <i>Ampullaceana balthica</i>. We compared the effects on the host-associated bacterial community to those on bacterial communities in water and sediment. This comparison was made using 16S ribosomal RNA gene sequencing. We found that the bacterial communities we sampled in Estonia, Denmark, and Northern Germany varied between water, sediment, and the gastrointestinal tract. They also varied between countries within each substrate. This indicates that the type of substrate is a dominant factor in determining bacterial community composition. We separately analyzed the turnover rates of water, sediment, and gastrointestinal bacterial communities over increasing geographic distances. We observed that the turnover rate was lower for gastrointestinal bacterial communities compared to water bacterial communities. This implies that the composition of gastrointestinal bacteria remains relatively stable over distances, while water bacterial communities exhibit greater variability. However, the gastrointestinal tract had the lowest percentage of country-specific amplicon sequence variants, suggesting bacterial colonization from local bacterial communities. Since the overlap between the water and gastrointestinal tract was highest, it appears that the gastrointestinal bacterial community is colonized by the water bacterial community. Our study confirmed that biogeographical patterns in host-associated communities differ from those in water and sediment bacterial communities. These host-associated communities consist of numerous facultative symbionts derived from the water bacterial community.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-06-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1413","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141200308","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":"Exploring solute binding proteins in Pseudomonas aeruginosa that bind to γ-aminobutyrate and 5-aminovalerate and their role in activating sensor kinases","authors":"Jean Paul Cerna-Vargas, Tino Krell","doi":"10.1002/mbo3.1415","DOIUrl":"10.1002/mbo3.1415","url":null,"abstract":"<p>The standard method of receptor activation involves the binding of signals or signal-loaded solute binding proteins (SBPs) to sensor domains. Many sensor histidine kinases (SHKs), which are activated by SBP binding, are encoded adjacent to their corresponding sbp gene. We examined three SBPs of <i>Pseudomonas aeruginosa</i> PAO1, encoded near the genes for the AgtS (PA0600) and AruS (PA4982) SHKs, to determine how common this arrangement is. Ligand screening and microcalorimetric studies revealed that the SBPs PA0602 and PA4985 preferentially bind to GABA (KD = 2.3 and 0.58 μM, respectively), followed by 5-aminovalerate (KD = 30 and 1.6 μM, respectively) and ethanoldiamine (KD = 2.3 and 0.58 μM, respectively). In contrast, AgtB (PA0604) exclusively recognizes 5-aminovaleric acid (KD = 2.9 μM). However, microcalorimetric titrations did not show any binding between the AgtS sensor domain and AgtB or PA0602, regardless of the presence of ligands. Similarly, bacterial two-hybrid assays did not demonstrate an interaction between PA4985 and the AruS sensor domain. Therefore, sbp and shk genes located nearby are not always functionally linked. We previously identified PA0222 as a GABA-specific SBP. The presence of three SBPs for GABA may be linked to GABA's role as a trigger for <i>P. aeruginosa</i> virulence.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-05-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1415","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141081786","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":"Correction to “Staphylococcus argenteus from rabbits in Thailand”","authors":"","doi":"10.1002/mbo3.1414","DOIUrl":"10.1002/mbo3.1414","url":null,"abstract":"<p>Indrawattana N., Pumipuntu N., Suriyakhun N., Jangsangthong A., Kulpeanprasit S., Chantratita N., Sookrung N., Chaicumpa W., & <b>Buranasinsup S</b>. <i>Staphylococcus argenteus</i> from rabbits in Thailand. <i>MicrobiologyOpen</i>. 2018;e665.</p><p>In “abstract” section, line 4, the text “the presence of <i>S. argenteus</i> in isolated <i>S. aureus</i> was investigated in 67 rabbits with abscess lesions during 2014–2016.” should read as “the presence of <i>S. argenteus</i> in isolated <i>S. aureus</i> was investigated in 67 rabbits with abscess lesions during 2014–2015.”</p><p>In “material and method section, 2.1 | Specimen collection and bacterial isolation, line 3, the text “Sixty-seven pus samples were collected from rabbits with clinical abscesses by a veterinarian at Prasu-Arthorn Animal Hospital, Thailand during 2014–2016.” should read as “Sixty-seven pus samples were collected from rabbits with clinical abscesses by a veterinarian at Prasu-Arthorn Animal Hospital, Thailand, during 2014–2015.”</p><p>We apologize for this error.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1414","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140922647","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}
Judith Stiefelmaier, Joshua Keller, Wiebke Neupert, Roland Ulber
{"title":"Towards bioprocess engineering of cable bacteria: Establishment of a synthetic sediment","authors":"Judith Stiefelmaier, Joshua Keller, Wiebke Neupert, Roland Ulber","doi":"10.1002/mbo3.1412","DOIUrl":"https://doi.org/10.1002/mbo3.1412","url":null,"abstract":"<p>Cable bacteria, characterized by their multicellular filamentous growth, are prevalent in both freshwater and marine sediments. They possess the unique ability to transport electrons over distances of centimeters. Coupled with their capacity to fix CO<sub>2</sub> and their record-breaking conductivity for biological materials, these bacteria present promising prospects for bioprocess engineering, including potential electrochemical applications. However, the cultivation of cable bacteria has been limited to their natural sediment, constraining their utility in production processes. To address this, our study designs synthetic sediment, drawing on ion exchange chromatography data from natural sediments and existing literature on the requirements of cable bacteria. We examined the effects of varying bentonite concentrations on water retention and the impacts of different sands. For the first time, we cultivated cable bacteria on synthetic sediment, specifically the freshwater strain <i>Electronema aureum</i> GS. This cultivation was conducted over 10 weeks in a specially developed sediment bioreactor, resulting in an increased density of cable bacteria in the sediment and growth up to a depth of 5 cm. The creation of this synthetic sediment paves the way for the reproducible cultivation of cable bacteria. It also opens up possibilities for future process scale-up using readily available components. This advancement holds significant implications for the broader field of bioprocess engineering.</p>","PeriodicalId":18573,"journal":{"name":"MicrobiologyOpen","volume":null,"pages":null},"PeriodicalIF":3.4,"publicationDate":"2024-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mbo3.1412","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140844664","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}