Daniele Corsaro , Martin Mrva , Philippe Colson , Julia Walochnik
{"title":"Validation and redescription of Acanthamoeba terricola Pussard, 1964 (Amoebozoa: Acanthamoebidae)","authors":"Daniele Corsaro , Martin Mrva , Philippe Colson , Julia Walochnik","doi":"10.1016/j.ejop.2024.126091","DOIUrl":"10.1016/j.ejop.2024.126091","url":null,"abstract":"<div><p><em>Acanthamoeba castellanii</em> (Douglas, 1930) Page, 1967 is the type species of a widespread genus of free-living amoebae, potentially pathogenic for humans and animals. The Neff strain is one of the most widely used in biological research, serving as a model for both <em>A. castellanii</em> and the whole genus in general. The Neff strain, isolated in California, closely resembles another strain found in France and originally described as a separate species, <em>Acanthamoeba terricola</em> Pussard, 1964, but both were successively synonymized with <em>A. castellanii</em>. Molecular sequence analysis has largely replaced morphological diagnosis for species identification in <em>Acanthamoeba</em>, and rDNA phylogenies show that the Neff strain forms a distinct lineage from that of the type strain of <em>A. castellanii</em>. In this study, we compared the type strain of <em>A. terricola</em> with the Neff strain and <em>A. castellanii</em>, and analysed the available molecular data including new sequences obtained from <em>A. terricola</em>. Here we provide molecular evidence to validate the species <em>A. terricola</em>. The Neff strain is therefore transferred to <em>A. terricola</em> and should no longer be considered as belonging to <em>A. castellanii</em>.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126091"},"PeriodicalIF":2.9,"publicationDate":"2024-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141031470","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alejandro Berlinches de Gea , Stefan Geisen , Franka Grootjans , Rutger A. Wilschut , Arne Schwelm
{"title":"Species-specific predation determines the feeding impacts of six soil protist species on bacterial and eukaryotic prey","authors":"Alejandro Berlinches de Gea , Stefan Geisen , Franka Grootjans , Rutger A. Wilschut , Arne Schwelm","doi":"10.1016/j.ejop.2024.126090","DOIUrl":"10.1016/j.ejop.2024.126090","url":null,"abstract":"<div><p>Predatory protists play a central role in nutrient cycling and are involved in other ecosystem functions by predating the microbiome. While most soil predatory protist species arguably are bacterivorous, some protist species can prey on eukaryotes. However, studies about soil protist feeding mainly focused on bacteria as prey and rarely tested both bacteria and eukaryotes as potential prey. In this study, we aimed to decipher soil predator–prey interactions of three amoebozoan and three heterolobosean soil protists and potential bacterial (<em>Escherichia coli</em>; 0.5–1.5 µm), fungal (<em>Saccharomyces cerevisiae</em>; 5–7 µm) and protist (<em>Plasmodiophora brassicae</em>; 3–5 µm) prey, either as individual prey or in all their combinations. We related protist performance (relative abundance) and prey consumption (qPCR) to the protist phylogenetic group and volume. We showed that for the six soil protist predators, the most suitable prey was <em>E. coli</em>, but some species also grew on <em>P. brassicae</em> or <em>S. cerevisiae</em>. While protist relative abundances and growth rates depended on prey type in a protist species-specific manner, phylogenetic groups and volume affected prey consumption. Yet we conclude that protist feeding patterns are mainly species-specific and that some known bacterivores might be more generalist than expected, even preying on eukaryotic plant pathogens such as <em>P. brassicae</em>.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126090"},"PeriodicalIF":2.9,"publicationDate":"2024-05-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0932473924000403/pdfft?md5=5230387304ec9b0524af064607d4f01f&pid=1-s2.0-S0932473924000403-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141040172","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Huilin Guo , Qiping Zhao , Haixia Wang, Shunhai Zhu, Hui Dong, Xinrui Xie, Lihui Wang, Lang Chen, Hongyu Han
{"title":"Molecular characterization and functional analysis of Eimeria tenella ankyrin repeat-containing protein","authors":"Huilin Guo , Qiping Zhao , Haixia Wang, Shunhai Zhu, Hui Dong, Xinrui Xie, Lihui Wang, Lang Chen, Hongyu Han","doi":"10.1016/j.ejop.2024.126089","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126089","url":null,"abstract":"<div><p>Chicken coccidiosis causes disastrous losses to the poultry industry all over the world. <em>Eimeria tenella</em> is the most prevalent of these disease-causing species. Our former RNA-seq indicated that <em>E. tenella</em> ankyrin repeat-containing protein (<em>Et</em>ANK) was expressed differently between drug-sensitive (DS) and drug-resistant strains. In this study, we cloned <em>Et</em>ANK and analyzed its translational and transcriptional levels using quantitative real-time PCR (qPCR) and western blotting. The data showed that <em>Et</em>ANK was significantly upregulated in diclazuril-resistant (DZR) strain and maduramicin-resistant (MRR) strain compared with the drug-sensitive (DS) strain. In addition, the transcription levels in the DZR strains isolated from the field were higher than in the DS strain. The translation levels of <em>Et</em>ANK were higher in unsporulated oocysts (UO) than in sporozoites (SZ), sporulated oocysts (SO), or second-generation merozoites (SM), and the protein levels in SM were significantly higher than in UO, SO, and SZ. The results of the indirect immunofluorescence localization showed that the protein was distributed mainly at the anterior region of SZ and on the surface and in the cytoplasm of SM. The fluorescence intensity increased further with its development in vitro. An anti-r<em>Et</em>ANK polyclonal antibody inhibited the invasive ability of <em>E. tenella</em> in DF-1 cells. These results showed that <em>Et</em>ANK may be related to host cell invasion, required for the parasite’s growth in the host, and may be involved in the development of <em>E. tenella</em> resistance to some drugs.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126089"},"PeriodicalIF":2.9,"publicationDate":"2024-05-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140917837","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ran Li , Wenbao Zhuang , Xiaochen Feng , Xiaoxuan Zhu , Xiaozhong Hu
{"title":"Morphology and molecular phylogeny of three Parasonderia species including a new species (Ciliophora, Plagiopylea)","authors":"Ran Li , Wenbao Zhuang , Xiaochen Feng , Xiaoxuan Zhu , Xiaozhong Hu","doi":"10.1016/j.ejop.2024.126087","DOIUrl":"10.1016/j.ejop.2024.126087","url":null,"abstract":"<div><p>Ciliates of the class Plagiopylea play a vital role in various anaerobic environments as consumers of prokaryotes. Yet, the diversity and phylogeny of this group of ciliates, especially marine representatives, remain poorly known. In this study, three <em>Parasonderia</em> species, viz., <em>Parasonderia elongata</em> spec. nov., and the already known <em>P. cyclostoma</em> and <em>P. vestita</em>, discovered in anaerobic sediments from various intertidal zones in China, were investigated based on their living morphology, infraciliature, and small subunit ribosomal rRNA gene sequences. <em>Parasonderia elongata</em> can be recognized by its larger body size, elongated body shape, oval oral opening, number of oral kineties, and significantly shortened leftmost postbuccal polykineties on the cell surface. Improved diagnosis and redescription of <em>P. cyclostoma</em> is provided for the first time, including data on infraciliature and molecular sequence. Phylogenetic analyses revealed that the three species cluster together and with the sequence of a Chinese population of <em>P. vestita</em> already present in the GenBank database, forming a robust clade.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126087"},"PeriodicalIF":2.9,"publicationDate":"2024-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140956949","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Morphology, morphogenesis and molecular phylogeny of a new soil ciliate, Lamtostyla paravitiphila nov. spec. (Ciliophora, Hypotrichia)","authors":"Tengteng Zhang , Furui Lu , Xiaoqing Yang, Yurui Wang, Chen Shao","doi":"10.1016/j.ejop.2024.126088","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126088","url":null,"abstract":"<div><p>The morphology and morphogenesis of <em>Lamtostyla paravitiphila</em> nov. spec<em>.</em>, a novel soil hypotrichous ciliate collected from eastern China, were investigated based on live observations and protargol-stained specimens. The new species is morphologically characterized as follows: seven to twelve macronuclear nodules, cortical granules absent, 19–26 adoral membranelles, three or four frontoventral cirri, the amphisiellid median cirral row extends to about mid-body and composed of 12–18 cirri, two or three transverse cirri, 27–39 left and 30–41 right marginal cirri, three almost bipolar dorsal kineties. Morphogenetically, it is characterized by the initial formation of six frontal-ventral-transverse cirral anlagen as primary primordia. Notably, the amphisiellid median cirral row and the posterior frontoventral cirrus (or cirri) contribute to the development of the frontal-ventral-transverse cirral anlagen, while the buccal cirrus may not participate in this process. Phylogenetic analyses based on small subunit ribosomal DNA sequence data indicate that the <em>Lamtostyla</em> species with available molecular data do not form a monophyletic group.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126088"},"PeriodicalIF":2.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140913997","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yeliz Dündar Orhan , Ayça Fulya Üstüntanır Dede , Şeyma Duran , Muhittin Arslanyolu
{"title":"Use of E-64 cysteine protease inhibitor for the recombinant protein production in Tetrahymena thermophila","authors":"Yeliz Dündar Orhan , Ayça Fulya Üstüntanır Dede , Şeyma Duran , Muhittin Arslanyolu","doi":"10.1016/j.ejop.2024.126085","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126085","url":null,"abstract":"<div><p><em>Tetrahymena thermophila</em> is an alternative organism for recombinant protein production. However, the production efficiency in <em>T. thermophila</em> is quite low mainly due to the rich cysteine proteases. In this study, we studied whether supplementation of the E-64 inhibitor to <em>T. thermophila</em> cultures increases the recombinant protein production efficiency without any toxic side effects. Our study showed that supplementation of E-64 had no lethal effects on <em>T. thermophila</em> cells in flask culture at 30 °C and 38 °C. <em>In vitro</em> protease activity analysis using secretome as protease enzyme source from E-64-supplemented cell cultures showed a reduced protein substrate degradation using bovine serum albumin, rituximab, and milk lactoglobulin proteins. E-64 also prevented proteolysis of the recombinantly produced and secreted TtmCherry2-sfGFP fusion protein at some level. This reduced inhibitory effect of E-64 could be due to genetic compensation of the inhibited proteases. As a result, the 5 µM concentration of E-64 was found to be a non-toxic protease inhibitory supplement to improve extracellular recombinant protein production efficiency in <em>T. thermophila</em>. This study suggests that the use of E-64 may increase the efficiency of extracellular recombinant protein production by continuously reducing extracellular cysteine protease activity during cultivation<em>.</em></p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126085"},"PeriodicalIF":2.9,"publicationDate":"2024-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140820078","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eduarda de Souza-Maciel, Luiz Fernando Carvalho-Kelly, Anita Leocadio Freitas-Mesquita, José Roberto Meyer-Fernandes
{"title":"The ecto-3′-nucleotidase activity of Acanthamoeba castellanii trophozoites increases their adhesion to host cells through the generation of extracellular adenosine","authors":"Eduarda de Souza-Maciel, Luiz Fernando Carvalho-Kelly, Anita Leocadio Freitas-Mesquita, José Roberto Meyer-Fernandes","doi":"10.1016/j.ejop.2024.126086","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126086","url":null,"abstract":"<div><p><em>Acanthamoeba castellanii</em>, a free-living amoeba, can be pathogenic to humans causing a corneal infection named <em>Acanthamoeba</em> keratitis (AK). The mannose-binding protein (MBP) is well established as the major factor related to <em>Acanthamoeba</em> pathogenesis. However, additional factors that participate in the adhesion process and protect trophozoites from cytolytic effects caused by host immune responses remain unknown. Ectonucleotidases, including 3′-nucleotidase/nuclease (3′-NT/NU), a bifunctional enzyme that was recently reported in <em>A. castellanii</em>, are frequently related to the establishment of parasitic infections. We verified that trophozoites can hydrolyze 3′-AMP, and this activity is similar to that observed in other protists. The addition of 3′-AMP increases the adhesion of trophozoites to LLC-MK2 epithelial cells, and this stimulation is completely reversed by DTT, an inhibitor of ecto-3′-nucleotidase activity. Lesions in corneal cells caused by AK infection may elevate the extracellular level of 3′-AMP. We believe that ecto-3′-nucleotidase activity can modulate the host immune response, thus facilitating the establishment of parasitic infection. This activity results from the generation of extracellular adenosine, which can bind to purinergic receptors present in host immune cells. Positive feedback may occur in this cascade of events once the ecto-3′-nucleotidase activity of trophozoites is increased by the adhesion of trophozoites to LLC-MK2 cells.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126086"},"PeriodicalIF":2.9,"publicationDate":"2024-04-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140813171","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kevin McKinley , Anastasios D. Tsaousis , Sonja Rückert
{"title":"Description and prevalence of gregarines infecting the amphipod Gammarus pulex, in the Water of Leith, Scotland, UK","authors":"Kevin McKinley , Anastasios D. Tsaousis , Sonja Rückert","doi":"10.1016/j.ejop.2024.126084","DOIUrl":"10.1016/j.ejop.2024.126084","url":null,"abstract":"<div><p>Gregarines are symbiotic protists that are found in a broad spectrum of invertebrates, including insects, crustaceans, and annelids. Among these the globally distributed amphipod <em>Gammarus pulex</em> is one of the earliest recognized hosts for aquatic gregarines and is prevalent among macroinvertebrates in freshwater environments. In this study, samples of <em>G. pulex</em> were collected in the Water of Leith river, Scotland, UK. Gregarines were identified using light and scanning electron microscopy as well as standard molecular techniques. We identified three septate eugregarine symbionts—<em>Heliospora longissima</em>, <em>Cephaloidophora gammari</em>, and the here newly characterized <em>Cephaloidophora conus</em> n. sp. (formerly <em>Cephaloidophora</em> sp.) associated with <em>Gammarus pulex</em> in the Water of Leith. Prevalences for identified gregarine species were calculated and seasonal dynamics of gregarine infections/colonization were analyzed. Prevalences were highest in autumn and spring reaching almost 50 %. While the two <em>Cephaloidophora</em> species showed similar colonization patterns, the prevalence of <em>Heliospora</em> showed an opposite trend. Identifying gregarine infection/colonization patterns is one step towards better understanding the gregarine–host relationship, as well as possible impacts of the gregarines on their hosts.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126084"},"PeriodicalIF":2.9,"publicationDate":"2024-04-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0932473924000348/pdfft?md5=7e5f9f7d71af9f1c7707d225f798a1c4&pid=1-s2.0-S0932473924000348-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140765910","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nicholas W. Fry , Robert E. Jones , Quentin Blandenier , Alexander K. Tice , Alfredo L. Porfirio-Sousa , Felicity Kleitz-Singleton , Tristan C. Henderson , Matthew W. Brown
{"title":"Molecular phylogenetic analyses support the validity of Ceratiomyxa porioides (Amoebozoa, Eumycetozoa) at species level","authors":"Nicholas W. Fry , Robert E. Jones , Quentin Blandenier , Alexander K. Tice , Alfredo L. Porfirio-Sousa , Felicity Kleitz-Singleton , Tristan C. Henderson , Matthew W. Brown","doi":"10.1016/j.ejop.2024.126083","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126083","url":null,"abstract":"<div><p>The frequently encountered macroscopic slime molds of the genus <em>Ceratiomyxa</em> have long been recognized by mycologists and protistologists for hundreds of years. These organisms are amoebozoan amoebae that live and grow inside and on the surface of decaying wood. When conditions are favorable, they form subaerial sporulating structures called fruiting bodies which take on a variety of forms. These forms are typically some arrangement of column and/or branches, but one is uniquely poroid, forming folds instead. Originally, this poroid morphology was designated as its own species. However, it was not always clear what significance fruiting body morphology held in determining species. Currently, <em>Ceratiomyxa fruticulosa</em> var. <em>porioides</em>, the poroid form, is considered a taxonomic variety of <em>Ceratiomyxa fruticulosa</em> based on morphological designation alone. Despite its long history of observation and study, the genus <em>Ceratiomyxa</em> has been paid little molecular attention to alleviate these morphological issues. We have obtained the first transcriptomes of the taxon <em>C. fruticulosa</em> var. <em>porioides</em> and found single gene phylogenetic and multigene phylogenomic support to separate it from <em>C. fruticulosa.</em> This provides molecular evidence that fruiting body morphology does correspond to species level diversity. Therefore, we formally raise <em>Ceratiomyxa porioides</em> to species level.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126083"},"PeriodicalIF":2.9,"publicationDate":"2024-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140618005","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tristan C. Henderson, Lucia Garcia-Gimeno, Charles E. Beasley Jr., Nicholas W. Fry, Jayden Bess, Matthew W. Brown
{"title":"High above the rest: standing behaviors in the amoebae of Sappinia and Thecamoeba","authors":"Tristan C. Henderson, Lucia Garcia-Gimeno, Charles E. Beasley Jr., Nicholas W. Fry, Jayden Bess, Matthew W. Brown","doi":"10.1016/j.ejop.2024.126082","DOIUrl":"https://doi.org/10.1016/j.ejop.2024.126082","url":null,"abstract":"<div><p>Many terrestrial microbes have evolved cell behaviors that help them rise above their substrate, often to facilitate dispersal. One example of these behaviors is found in the amoebae of <em>Sappinia pedata</em>, which actively lift most of their cell mass above the substrate, known as standing. This standing behavior was first described in <em>S. pedata</em> in the 1890s from horse dung isolates but never molecularly characterized from dung. Our study expands this understanding, revealing the first molecularly confirmed <em>S. pedata</em> from herbivore dung in Mississippi, USA, and describing a new species, <em>Sappinia dangeardi</em> n. sp., with larger trophozoite cells. Additionally, we isolated another standing amoeba, <em>Thecamoeba homeri</em> n. sp., from soil, exhibiting a previously unreported “doughnut shape” transient behavior. In <em>S. dangeardi</em> n. sp., we discovered that standing is likely triggered by substrate drying, and that actin filaments actively localize in the “stalk” to support the standing cells, as observed through confocal microscopy. While the purpose of standing behaviors has not been investigated, we hypothesize it is energetically expensive and therefore a significant evolutionary strategy in these organisms. Overall, this study emphasizes behavioral adaptations to terrestrial environments within Amoebozoa, stressing the importance of diverse laboratory conditions that replicate natural habitats.</p></div>","PeriodicalId":12042,"journal":{"name":"European journal of protistology","volume":"94 ","pages":"Article 126082"},"PeriodicalIF":2.9,"publicationDate":"2024-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140824663","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}