Pub Date : 2024-05-12DOI: 10.1016/j.syapm.2024.126516
Undine Behrendt , Valentin Burghard , Sonja Wende , Kristina Ulrich , Jacqueline Wolf , Meina Neumann-Schaal , Andreas Ulrich
The tolerance of ash trees against the pathogen Hymenoscyphus fraxineus seems to be associated with the occurrence of specific microbial taxa on leaves. A group of bacterial isolates, primarily identified on tolerant trees, was investigated with regard to their taxonomic classification and their potential to suppress the ash dieback pathogen. Examination of OGRI values revealed a separate species position. A phylogenomic analysis, based on orthologous and marker genes, indicated a separate genus position along with the species Achromobacter aestuarii. Furthermore, analysis of the ratio of average nucleotide identities and genome alignment fractions demonstrated genomic dissimilarities typically observed for inter-genera comparisons within this family. As a result of these investigations, the strains are considered to represent a separate species within a new genus, for which the name Schauerella fraxinea gen. nov., sp. nov. is proposed, with the type strain B3P038T (=LMG 33092 T = DSM 115926 T). Additionally, a reclassification of the species Achromobacter aestuarii as Schauerella aestuarii comb. nov. is proposed.
In a co-cultivation assay, the strains were able to inhibit the growth of a H. fraxineus strain. Accordingly, a functional analysis of the genome of S. fraxinea B3P038T revealed genes mediating the production of antifungal substances. This potential, combined with the prevalent presence in the phyllosphere of tolerant ash trees, makes this group interesting for an inoculation experiment with the aim of controlling the pathogen in an integrative approach. For future field trials, a strain-specific qPCR system was developed to establish an efficient method for monitoring the inoculation success.
{"title":"Schauerella fraxinea gen. nov., sp. nov., a bacterial species that colonises ash trees tolerant to dieback caused by Hymenoscyphus fraxineus","authors":"Undine Behrendt , Valentin Burghard , Sonja Wende , Kristina Ulrich , Jacqueline Wolf , Meina Neumann-Schaal , Andreas Ulrich","doi":"10.1016/j.syapm.2024.126516","DOIUrl":"10.1016/j.syapm.2024.126516","url":null,"abstract":"<div><p>The tolerance of ash trees against the pathogen <em>Hymenoscyphus fraxineus</em> seems to be associated with the occurrence of specific microbial taxa on leaves. A group of bacterial isolates, primarily identified on tolerant trees, was investigated with regard to their taxonomic classification and their potential to suppress the ash dieback pathogen. Examination of OGRI values revealed a separate species position. A phylogenomic analysis, based on orthologous and marker genes, indicated a separate genus position along with the species <em>Achromobacter aestuarii</em>. Furthermore, analysis of the ratio of average nucleotide identities and genome alignment fractions demonstrated genomic dissimilarities typically observed for inter-genera comparisons within this family. As a result of these investigations, the strains are considered to represent a separate species within a new genus, for which the name <em>Schauerella fraxinea</em> gen. nov., sp. nov. is proposed, with the type strain B3P038<sup>T</sup> (=LMG 33092 <sup>T</sup> = DSM 115926 <sup>T</sup>). Additionally, a reclassification of the species <em>Achromobacter aestuarii</em> as <em>Schauerella aestuarii</em> comb. nov. is proposed.</p><p>In a co-cultivation assay, the strains were able to inhibit the growth of a <em>H. fraxineus</em> strain. Accordingly, a functional analysis of the genome of <em>S. fraxinea</em> B3P038<sup>T</sup> revealed genes mediating the production of antifungal substances. This potential, combined with the prevalent presence in the phyllosphere of tolerant ash trees, makes this group interesting for an inoculation experiment with the aim of controlling the pathogen in an integrative approach. For future field trials, a strain-specific qPCR system was developed to establish an efficient method for monitoring the inoculation success.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 4","pages":"Article 126516"},"PeriodicalIF":3.4,"publicationDate":"2024-05-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0723202024000304/pdfft?md5=863b75ac7145c8f11e191c95b97b3c66&pid=1-s2.0-S0723202024000304-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141037842","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}
Pub Date : 2024-05-11DOI: 10.1016/j.syapm.2024.126517
José David Flores-Félix , Fernando Sánchez-Juanes , Laura Pulido-Suárez , Encarna Velázquez , Milagros León-Barrios
The symbiovar mediterranense of Sinorhizobium meliloti was initially found in Phaseolus vulgaris nodules in Tunisia and in an eastern location of Lanzarote (Canary Islands). Here we show that the symbiovar mediterranense of S. meliloti also nodulates P. vulgaris in two western locations of this Island. The analyses of the symbiotic nodA and nodC genes reveal the complexity of the symbiovar mediterranense which encompasses strains belonging to several phylogenetic lineages and clusters. The comparison of the nodA and nodC phylogenies showed that the nodC was the most resolutive phylogenetic marker for the delineation of Sinorhizobium symbiovars. Considering that the similarity of this gene within several symbiovars, particularly mediterranense, is around 95 %, the cut-off value for their differentiation should be lower. Considering that a nodC gene cut-off similarity value of around 92 % is accepted for the genus Bradyrhizobium and that the symbiovar concept is identical in all rhizobial genera, we propose to apply this value for symbiovars delineation within all these genera. Therefore, using this cut-off value for the nodC gene analysis of Sinorhizobium symbiovars, we propose to merge the symbiovars aegeanense and fredii into the single symbiovar fredii and to define four novel symbiovars with the names asiaense, culleni, sudanense and tunisiaense.
{"title":"The symbiovar mediterranense of Sinorhizobium meliloti nodulates Phaseolus vulgaris across Lanzarote (Canary Islands): A revision of this symbiovar supports a proposal to delimit symbiovars boundaries in Sinorhizobium and to define four new symbiovars","authors":"José David Flores-Félix , Fernando Sánchez-Juanes , Laura Pulido-Suárez , Encarna Velázquez , Milagros León-Barrios","doi":"10.1016/j.syapm.2024.126517","DOIUrl":"10.1016/j.syapm.2024.126517","url":null,"abstract":"<div><p>The symbiovar mediterranense of <em>Sinorhizobium meliloti</em> was initially found in <em>Phaseolus vulgaris</em> nodules in Tunisia and in an eastern location of Lanzarote (Canary Islands). Here we show that the symbiovar mediterranense of <em>S. meliloti</em> also nodulates <em>P. vulgaris</em> in two western locations of this Island. The analyses of the symbiotic <em>nodA</em> and <em>nodC</em> genes reveal the complexity of the symbiovar mediterranense which encompasses strains belonging to several phylogenetic lineages and clusters. The comparison of the <em>nodA</em> and <em>nodC</em> phylogenies showed that the <em>nodC</em> was the most resolutive phylogenetic marker for the delineation of <em>Sinorhizobium</em> symbiovars. Considering that the similarity of this gene within several symbiovars, particularly mediterranense, is around 95 %, the cut-off value for their differentiation should be lower. Considering that a <em>nodC</em> gene cut-off similarity value of around 92 % is accepted for the genus <em>Bradyrhizobium</em> and that the symbiovar concept is identical in all rhizobial genera, we propose to apply this value for symbiovars delineation within all these genera. Therefore, using this cut-off value for the <em>nodC</em> gene analysis of <em>Sinorhizobium</em> symbiovars, we propose to merge the symbiovars aegeanense and fredii into the single symbiovar fredii and to define four novel symbiovars with the names asiaense, culleni, sudanense and tunisiaense.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 4","pages":"Article 126517"},"PeriodicalIF":3.4,"publicationDate":"2024-05-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141044758","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}
A novel anaerobic, thermophilic bacterium of the class Atribacteria, strain M15T, was isolated from a high-temperature gas reservoir, Japan. Cells of strain M15T were gram-negative, short oval-shaped, and lacked flagella. Growth occurred at 45–75 °C (optimum 70–75 °C) and pH 6.5–8.5 (optimum pH 7.5–8.0) and was fast under optimal conditions (doubling time 11.4 h). Yeast extract was required for growth. Fermentative growth with glucose, arabinose, xylose, and cellobiose was observed. The major fermentative end products of glucose were acetate and hydrogen. The major cellular fatty acids were C16:0, iso-C15:0, and C18:0. The genomic G + C content was 46.0 mol%. Fluorescence and electron microscopy observations revealed the intracellular localization of genomic DNA surrounded by a membrane in the cells of strain M15T as reported in a sole validly described species of the class Atribacteria in the phylum Atribacterota, Atribacter laminatus strain RT761T, suggesting that the unique morphological traits are widely shared in this class. Phylogenetic analyses indicated that strain M15T belongs to a distinct family-level lineage in the class Atribacteria and shows low similarities to Atribacter laminatus strain RT761T (16S rRNA gene sequence identity of 90.1 %, average nucleotide identity [ANI] of 66.1 %, average amino acid identity [AAI] of 55.8 %). Phenotypic traits of strain M15T (thermophilic, fast-growing, relatively high G + C content, etc.) were clearly distinct from A. laminatus. Based on these phenotypic and genomic properties, we propose a novel genus and species, Atrimonas thermophila gen. nov., sp. nov. for strain M15T (=JCM39389T, =KCTC25731T) representing a novel family Atrimonadaceae fam., nov. in the class Atribacteria.
从日本的一个高温储气库中分离出了一种新型厌氧、嗜热的阿特里伯氏细菌--菌株 M15T。菌株 M15T 的细胞为革兰氏阴性,短椭圆形,无鞭毛。生长温度为 45-75℃(最适温度为 70-75℃),pH 值为 6.5-8.5(最适 pH 值为 7.5-8.0),在最适条件下生长速度很快(倍增时间为 11.4 小时)。生长需要酵母提取物。可观察到葡萄糖、阿拉伯糖、木糖和纤维生物糖的发酵生长。葡萄糖的主要发酵终产物是醋酸和氢。细胞中的主要脂肪酸为 C16:0、异 C15:0 和 C18:0。基因组 G + C 含量为 46.0 摩尔%。荧光和电子显微镜观察显示,在菌株 M15T 的细胞内,基因组 DNA 被一层膜所包围,这在阿特里杆菌门阿特里杆菌属唯一有效描述的物种--层状阿特里杆菌菌株 RT761T 中也有报道,表明其独特的形态特征在该门类中被广泛共享。系统进化分析表明,菌株 M15T 属于阿特里杆菌门中一个独特的科级菌系,与层状阿特里杆菌菌株 RT761T 的相似性较低(16S rRNA 基因序列同一性为 90.1%,平均核苷酸同一性[ANI]为 66.1%,平均氨基酸同一性[AAI]为 55.8%)。菌株 M15T 的表型特征(嗜热、快速生长、相对较高的 G + C 含量等)明显有别于 A. laminatus。基于这些表型和基因组特性,我们为菌株 M15T(=JCM39389T,=KCTC25731T)提出了一个新属和新种 Atrimonas thermophila gen.
{"title":"Atrimonas thermophila gen. nov., sp. nov., a novel anaerobic thermophilic bacterium of the phylum Atribacterota isolated from deep subsurface gas field and proposal of Atrimonadaceae fam. nov. within the class Atribacteria in the phylum Atribacterota","authors":"Hiroki Kawamoto , Miho Watanabe , Hanako Mochimaru , Nozomi Nakahara , Xiang-Ying Meng , Sachiko Sakamoto , Kana Morinaga , Taiki Katayama , Hideyoshi Yoshioka , Nobuhiko Nomura , Hideyuki Tamaki","doi":"10.1016/j.syapm.2024.126515","DOIUrl":"10.1016/j.syapm.2024.126515","url":null,"abstract":"<div><p>A novel anaerobic, thermophilic bacterium of the class <em>Atribacteria</em>, strain M15<sup>T</sup>, was isolated from a high-temperature gas reservoir, Japan. Cells of strain M15<sup>T</sup> were gram-negative, short oval-shaped, and lacked flagella. Growth occurred at 45–75 °C (optimum 70–75 °C) and pH 6.5–8.5 (optimum pH 7.5–8.0) and was fast under optimal conditions (doubling time 11.4 h). Yeast extract was required for growth. Fermentative growth with glucose, arabinose, xylose, and cellobiose was observed. The major fermentative end products of glucose were acetate and hydrogen. The major cellular fatty acids were C<sub>16:0</sub>, <em>iso</em>-C<sub>15:0</sub>, and C<sub>18:0</sub>. The genomic G + C content was 46.0 mol%. Fluorescence and electron microscopy observations revealed the intracellular localization of genomic DNA surrounded by a membrane in the cells of strain M15<sup>T</sup> as reported in a sole validly described species of the class <em>Atribacteria</em> in the phylum <em>Atribacterota</em>, <em>Atribacter laminatus</em> strain RT761<sup>T</sup>, suggesting that the unique morphological traits are widely shared in this class. Phylogenetic analyses indicated that strain M15<sup>T</sup> belongs to a distinct family-level lineage in the class <em>Atribacteria</em> and shows low similarities to <em>Atribacter laminatus</em> strain RT761<sup>T</sup> (16S rRNA gene sequence identity of 90.1 %, average nucleotide identity [ANI] of 66.1 %, average amino acid identity [AAI] of 55.8 %). Phenotypic traits of strain M15<sup>T</sup> (thermophilic, fast-growing, relatively high G + C content, etc.) were clearly distinct from <em>A. laminatus.</em> Based on these phenotypic and genomic properties, we propose a novel genus and species, <em>Atrimonas thermophila</em> gen. nov., sp. nov. for strain M15<sup>T</sup> (=JCM39389<sup>T</sup>, =KCTC25731<sup>T</sup>) representing a novel family <em>Atrimonadaceae</em> fam., nov. in the class <em>Atribacteria</em>.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 4","pages":"Article 126515"},"PeriodicalIF":3.4,"publicationDate":"2024-05-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0723202024000298/pdfft?md5=b9c8c8f687794ac5baf697b6a8ac5b64&pid=1-s2.0-S0723202024000298-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141039484","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}
Pub Date : 2024-05-01DOI: 10.1016/j.syapm.2024.126507
Emily St. John, Anna-Louise Reysenbach
Deep-sea hydrothermal vents host archaeal and bacterial thermophilic communities, including taxonomically and functionally diverse Thermoproteota. Despite their prevalence in high-temperature submarine communities, Thermoproteota are chronically under-represented in genomic databases and issues have emerged regarding their nomenclature, particularly within the Aeropyrum–Thermodiscus–Caldisphaera. To resolve some of these problems, we identified 47 metagenome-assembled genomes (MAGs) within this clade, from 20 previously published deep-sea hydrothermal vent and submarine volcano metagenomes, and 24 MAGs from public databases. Using phylogenomic analysis, Genome Taxonomy Database Toolkit (GTDB-Tk) taxonomic assessment, 16S rRNA gene phylogeny, average amino acid identity (AAI) and functional gene patterns, we re-evaluated of the taxonomy of the Aeropyrum–Thermodiscus–Caldisphaera. At least nine genus-level clades were identified with two or more MAGs. In accordance with SeqCode requirements and recommendations, we propose names for three novel genera, viz. Tiamatella incendiivivens, Hestiella acidicharens and Calypsonella navitae. A fourth genus was also identified related to Thermodiscus maritimus, for which no available sequenced genome exists. We propose the novel species Thermodiscus eudorianus to describe our high-quality Thermodiscus MAG, which represents the type genome for the genus. All three novel genera and T. eudorianus are likely anaerobic heterotrophs, capable of fermenting protein-rich carbon sources, while some Tiamatella, Calypsonella and T. eudorianus may also reduce polysulfides, thiosulfate, sulfur and/or selenite, and the likely acidophile, Hestiella, may reduce nitrate and/or perchlorate. Based on phylogenomic evidence, we also propose the family Acidilobaceae be amended to include Caldisphaera, Aeropyrum, Thermodiscus and Stetteria and the novel genera described here.
{"title":"Genomic comparison of deep-sea hydrothermal genera related to Aeropyrum, Thermodiscus and Caldisphaera, and proposed emended description of the family Acidilobaceae","authors":"Emily St. John, Anna-Louise Reysenbach","doi":"10.1016/j.syapm.2024.126507","DOIUrl":"https://doi.org/10.1016/j.syapm.2024.126507","url":null,"abstract":"<div><p>Deep-sea hydrothermal vents host archaeal and bacterial thermophilic communities, including taxonomically and functionally diverse <em>Thermoproteota.</em> Despite their prevalence in high-temperature submarine communities, <em>Thermoproteota</em> are chronically under-represented in genomic databases and issues have emerged regarding their nomenclature, particularly within the <em>Aeropyrum–Thermodiscus–Caldisphaera</em>. To resolve some of these problems, we identified 47 metagenome-assembled genomes (MAGs) within this clade, from 20 previously published deep-sea hydrothermal vent and submarine volcano metagenomes, and 24 MAGs from public databases. Using phylogenomic analysis, Genome Taxonomy Database Toolkit (GTDB-Tk) taxonomic assessment, 16S rRNA gene phylogeny, average amino acid identity (AAI) and functional gene patterns, we re-evaluated of the taxonomy of the <em>Aeropyrum–Thermodiscus–Caldisphaera.</em> At least nine genus-level clades were identified with two or more MAGs. In accordance with SeqCode requirements and recommendations, we propose names for three novel genera, viz. <em>Tiamatella incendiivivens, Hestiella acidicharens</em> and <em>Calypsonella navitae.</em> A fourth genus was also identified related to <em>Thermodiscus maritimus,</em> for which no available sequenced genome exists. We propose the novel species <em>Thermodiscus eudorianus</em> to describe our high-quality <em>Thermodiscus</em> MAG<em>,</em> which represents the type genome for the genus. All three novel genera and <em>T. eudorianus</em> are likely anaerobic heterotrophs, capable of fermenting protein-rich carbon sources, while some <em>Tiamatella, Calypsonella</em> and <em>T. eudorianus</em> may also reduce polysulfides, thiosulfate, sulfur and/or selenite, and the likely acidophile, <em>Hestiella,</em> may reduce nitrate and/or perchlorate. Based on phylogenomic evidence, we also propose the family <em>Acidilobaceae</em> be amended to include <em>Caldisphaera, Aeropyrum, Thermodiscus</em> and <em>Stetteria</em> and the novel genera described here.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126507"},"PeriodicalIF":3.4,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140822835","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}
Pub Date : 2024-05-01DOI: 10.1016/j.syapm.2024.126514
Dimitry Y. Sorokin , Alexander G. Elcheninov , Nicole J. Bale , Jaap Sininghe Damsté , Ilya V. Kublanov
Use of curldlan, an insoluble β-1,3-glucan, as an enrichment substrate under aerobic conditions resulted in the selection from hypersaline soda lakes of a single natronarchaeon, strain AArc-curdl1. This organism is an obligately aerobic saccharolytic, possessing a poorly explored (in Archaea) potential to utilize beta-1–3 glucans, being only a second example of a haloarchaeon with this ability known in pure culture. The main phenotypic property of the isolate is the ability to grow with insoluble β-1,3-backboned glucans, i.e. curdlan and pachyman. Furthermore, the strain utilized starch family α-glucans, beta-fructan inulin and a limited spectrum of sugars. The major ether-bound membrane polar phospholipids included PGP-Me and PG. The glyco- and sulfolipids were absent. The major respiratory menaquinone is MK-8:8. According to phylogenomic analysis, AArc-curdl1 represents a separate species in the recently described genus Natronosalvus within the family Natrialbaceae. The closest related species is Natronosalvus amylolyticus (ANI, AAI and DDH values of 90.2, 91.6 and 44 %, respectively). On the basis of its unique physiological properties and phylogenomic distance, strain AArc-curdl1T is classified as a novel species Natronosalvus hydrolyticus sp. nov. (=JCM 34865 = UQM 41566).
{"title":"Natronosalvus hydrolyticus sp. nov., a beta-1,3-glucan utilizing natronoarchaeon from hypersaline soda lakes","authors":"Dimitry Y. Sorokin , Alexander G. Elcheninov , Nicole J. Bale , Jaap Sininghe Damsté , Ilya V. Kublanov","doi":"10.1016/j.syapm.2024.126514","DOIUrl":"https://doi.org/10.1016/j.syapm.2024.126514","url":null,"abstract":"<div><p>Use of curldlan, an insoluble β-1,3-glucan, as an enrichment substrate under aerobic conditions resulted in the selection from hypersaline soda lakes of a single natronarchaeon, strain AArc-curdl1. This organism is an obligately aerobic saccharolytic, possessing a poorly explored (in Archaea) potential to utilize beta-1–3 glucans, being only a second example of a haloarchaeon with this ability known in pure culture. The main phenotypic property of the isolate is the ability to grow with insoluble β-1,3-backboned glucans, i.e. curdlan and pachyman. Furthermore, the strain utilized starch family α-glucans, beta-fructan inulin and a limited spectrum of sugars. The major ether-bound membrane polar phospholipids included PGP-Me and PG. The glyco- and sulfolipids were absent. The major respiratory menaquinone is MK-8:8. According to phylogenomic analysis, AArc-curdl1 represents a separate species in the recently described genus <em>Natronosalvus</em> within the family <em>Natrialbaceae.</em> The closest related species is <em>Natronosalvus amylolyticus</em> (ANI, AAI and DDH values of 90.2, 91.6 and 44 %, respectively). On the basis of its unique physiological properties and phylogenomic distance, strain AArc-curdl1<sup>T</sup> is classified as a novel species <em>Natronosalvus hydrolyticus</em> sp. nov. (=JCM 34865 = UQM 41566).</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126514"},"PeriodicalIF":3.4,"publicationDate":"2024-05-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140905657","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}
Pub Date : 2024-04-09DOI: 10.1016/j.syapm.2024.126506
Juan F. Gago , Tomeu Viver , Mercedes Urdiain , Elaine Ferreira , Pedro Robledo , Ramon Rossello-Mora
Groundwater offers an intriguing blend of distinctive physical and chemical conditions, constituting a challenge for microbial life. In Mallorca, the largest island of Balearic archipelago, harbours a variety of thermal anomalies (i.e., geothermal manifestation where surface aquifers exhibiting temperatures exceeding the regional average). The metagenomes of two aquifers in the centre and southern of the island showed Pseudomonadota to be the most represented phylum when using extracted 16S rRNA gene sequences. However, the microbial structures within and between aquifers were remarkably diverse but similar in their metabolic profiles as revealed by the metagenome-assembled genomes (MAGs) pointing to a prevalence of aerobic chemolithoautotrophic and heterotrophic metabolisms, especially in the Llucmajor aquifer. Also, some evidences of anaerobic lifestyles were detected, which would indicate that these environments either could suffer episodes of oxygen depletion or the anaerobes had been transported from deeper waters. We believe that the local environmental factors (temperature, external inputs or chemistry) seem to be more relevant than the connection and, eventually, transport of microbial cells within the aquifer in determining the highly divergent structures. Notably, most of the reconstructed genomes belonged to undescribed bacterial lineages and from them two high-quality MAGs could be classified as novel taxa named following the rules of the Code for Nomenclature of Prokaryotes Described from Sequence Data (SeqCode). Accordingly, we propose the new species and genus Costitxia debesea gen. nov., sp. nov., affiliated with the novel family Costitxiaceae fam. nov., order Costitxiales ord. nov. and class Costitxiia class. nov.; and the new new species and genus Lloretia debesea gen. nov. sp. nov. affiliated with the novel family Lloretiaceae fam. nov.
{"title":"Metagenomics of two aquifers with thermal anomalies in Mallorca Island, and proposal of new uncultivated taxa named following the rules of SeqCode","authors":"Juan F. Gago , Tomeu Viver , Mercedes Urdiain , Elaine Ferreira , Pedro Robledo , Ramon Rossello-Mora","doi":"10.1016/j.syapm.2024.126506","DOIUrl":"https://doi.org/10.1016/j.syapm.2024.126506","url":null,"abstract":"<div><p>Groundwater offers an intriguing blend of distinctive physical and chemical conditions, constituting a challenge for microbial life. In Mallorca, the largest island of Balearic archipelago, harbours a variety of thermal anomalies (i.e., geothermal manifestation where surface aquifers exhibiting temperatures exceeding the regional average). The metagenomes of two aquifers in the centre and southern of the island showed <em>Pseudomonadota</em> to be the most represented phylum when using extracted 16S rRNA gene sequences. However, the microbial structures within and between aquifers were remarkably diverse but similar in their metabolic profiles as revealed by the metagenome-assembled genomes (MAGs) pointing to a prevalence of aerobic chemolithoautotrophic and heterotrophic metabolisms, especially in the Llucmajor aquifer. Also, some evidences of anaerobic lifestyles were detected, which would indicate that these environments either could suffer episodes of oxygen depletion or the anaerobes had been transported from deeper waters. We believe that the local environmental factors (temperature, external inputs or chemistry) seem to be more relevant than the connection and, eventually, transport of microbial cells within the aquifer in determining the highly divergent structures. Notably, most of the reconstructed genomes belonged to undescribed bacterial lineages and from them two high-quality MAGs could be classified as novel taxa named following the rules of the Code for Nomenclature of Prokaryotes Described from Sequence Data (SeqCode). Accordingly, we propose the new species and genus <em>Costitxia debesea</em> gen. nov., sp. nov., affiliated with the novel family <em>Costitxiaceae</em> fam. nov<em>.</em>, order <em>Costitxiales</em> ord. nov. and class <em>Costitxiia</em> class. nov.; and the new new species and genus <em>Lloretia debesea</em> gen. nov. sp. nov. affiliated with the novel family <em>Lloretiaceae</em> fam. nov.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126506"},"PeriodicalIF":3.4,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0723202024000201/pdfft?md5=1a25fb9ae3fca24ad4164b29088d3762&pid=1-s2.0-S0723202024000201-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140606939","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}
Pub Date : 2024-03-25DOI: 10.1016/j.syapm.2024.126504
Melandré van Lill , Stephanus N. Venter , Esther K. Muema , Marike Palmer , Wai Y. Chan , Chrizelle W. Beukes , Emma T. Steenkamp
South Africa is well-known for the diversity of its legumes and their nitrogen-fixing bacterial symbionts. However, in contrast to their plant partners, remarkably few of these microbes (collectively referred to as rhizobia) from South Africa have been characterised and formally described. This is because the rules of the International Code of Nomenclature of Prokaryotes (ICNP) are at odds with South Africa's National Environmental Management: Biodiversity Act and its associated regulations. The ICNP requires that a culture of the proposed type strain for a novel bacterial species be deposited in two international culture collections and be made available upon request without restrictions, which is not possible under South Africa’s current national regulations. Here, we describe seven new Mesorhizobium species obtained from root nodules of Vachellia karroo, an iconic tree legume distributed across various biomes in southern Africa. For this purpose, 18 rhizobial isolates were delineated into putative species using genealogical concordance, after which their plausibility was explored with phenotypic characters and average genome relatedness. For naming these new species, we employed the rules of the recently published Code of Nomenclature of Prokaryotes described from Sequence Data (SeqCode), which utilizes genome sequences as nomenclatural types. The work presented in this study thus provides an illustrative example of how the SeqCode allows for a standardised approach for naming cultivated organisms for which the deposition of a type strain in international culture collections is currently problematic.
{"title":"SeqCode facilitates naming of South African rhizobia left in limbo","authors":"Melandré van Lill , Stephanus N. Venter , Esther K. Muema , Marike Palmer , Wai Y. Chan , Chrizelle W. Beukes , Emma T. Steenkamp","doi":"10.1016/j.syapm.2024.126504","DOIUrl":"10.1016/j.syapm.2024.126504","url":null,"abstract":"<div><p>South Africa is well-known for the diversity of its legumes and their nitrogen-fixing bacterial symbionts. However, in contrast to their plant partners, remarkably few of these microbes (collectively referred to as rhizobia) from South Africa have been characterised and formally described. This is because the rules of the International Code of Nomenclature of Prokaryotes (ICNP) are at odds with South Africa's National Environmental Management: Biodiversity Act and its associated regulations. The ICNP requires that a culture of the proposed type strain for a novel bacterial species be deposited in two international culture collections and be made available upon request without restrictions, which is not possible under South Africa’s current national regulations. Here, we describe seven new <em>Mesorhizobium</em> species obtained from root nodules of <em>Vachellia karroo</em>, an iconic tree legume distributed across various biomes in southern Africa. For this purpose, 18 rhizobial isolates were delineated into putative species using genealogical concordance, after which their plausibility was explored with phenotypic characters and average genome relatedness. For naming these new species, we employed the rules of the recently published Code of Nomenclature of Prokaryotes described from Sequence Data (SeqCode), which utilizes genome sequences as nomenclatural types. The work presented in this study thus provides an illustrative example of how the SeqCode allows for a standardised approach for naming cultivated organisms for which the deposition of a type strain in international culture collections is currently problematic.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126504"},"PeriodicalIF":3.4,"publicationDate":"2024-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0723202024000183/pdfft?md5=885b47be2491e2918543c1a10b18b6fa&pid=1-s2.0-S0723202024000183-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140403534","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}
Pub Date : 2024-03-22DOI: 10.1016/j.syapm.2024.126505
Juliana Botero , Charlotte Peeters , Evelien De Canck , David Laureys , Anneleen D. Wieme , Ilse Cleenwerck , Eliza Depoorter , Jessy Praet , Denis Michez , Guy Smagghe , Peter Vandamme
The increase in studies on bee microbiomes is prompted by concerns over global pollinator declines. Bumble bees host core and non-core microbiota which may contribute to increased lifetime fitness. The presence of Fructobacillus in the gut microbiomes of bumble bee workers, or the replacement of core symbionts with Fructobacillus bacteria, has been considered a marker of dysbiosis. A phylogenomic analysis and functional genomic characterization of the genomes of 21 Fructobacillus isolates from bumble bees demonstrated that they represented four species, i.e. Fructobacillus cardui, Fructobacillus fructosus, Fructobacillus tropaeoli, and the novel species Fructobacillus evanidus sp. nov. Our results confirmed and substantiated the presence of two phylogenetically and functionally distinct Fructobacillus species clades that differ in genome size, percentage G + C content, the number of coding DNA sequences and metabolic characteristics. Clade 1 and clade 2 species differed in amino acid and, to a lesser extent, in carbohydrate metabolism, with F. evanidus and F. tropaeoli genomes featuring a higher number of complete metabolic pathways. While Fructobacillus genomes encoded genes that allow adhesion, biofilm formation, antibacterial activity and detoxification, other bacteria isolated from the bumble bee gut appeared better equipped to co-exist with the bumble bee host. The isolation and identification of multiple Fructobacillus species from several bumble bee gut samples in the present study also argued against a specific partnership between Fructobacillus species and their bumble bee hosts.
对蜜蜂微生物组研究的增加是由于对全球授粉者减少的担忧。大黄蜂寄生的核心和非核心微生物群可能有助于提高其一生的适应能力。大黄蜂工蜂肠道微生物组中果酸杆菌的存在,或果酸杆菌对核心共生菌的替代,一直被认为是菌群失调的标志。对从大黄蜂中分离出的 21 个果酸杆菌基因组进行的系统发生组分析和功能基因组鉴定表明,它们代表了 4 个物种,即卡氏果酸杆菌(Fructobacillus cardui)、果寡糖果酸杆菌(Fructobacillus fructosus)、滋养果酸杆菌(Fructobacillus tropaeoli)和新物种埃瓦尼德果酸杆菌(Fructobacillus evanidus sp.nov)。我们的研究结果证实了两个在系统发育和功能上截然不同的果酸杆菌物种支系的存在,它们在基因组大小、G + C 含量百分比、编码 DNA 序列数量和代谢特征上都有所不同。支系 1 和支系 2 的物种在氨基酸代谢方面存在差异,在碳水化合物代谢方面差异较小,其中 F. evanidus 和 F. tropaeoli 的基因组具有较多的完整代谢途径。虽然果杆菌基因组编码的基因可以实现粘附、生物膜形成、抗菌活性和解毒,但从大黄蜂肠道中分离出的其他细菌似乎更适合与大黄蜂宿主共存。本研究从几种大黄蜂肠道样本中分离并鉴定出多种果酸杆菌,这也证明果酸杆菌与大黄蜂宿主之间并不存在特定的伙伴关系。
{"title":"A comparative genomic analysis of Fructobacillus evanidus sp. nov. from bumble bees","authors":"Juliana Botero , Charlotte Peeters , Evelien De Canck , David Laureys , Anneleen D. Wieme , Ilse Cleenwerck , Eliza Depoorter , Jessy Praet , Denis Michez , Guy Smagghe , Peter Vandamme","doi":"10.1016/j.syapm.2024.126505","DOIUrl":"10.1016/j.syapm.2024.126505","url":null,"abstract":"<div><p>The increase in studies on bee microbiomes is prompted by concerns over global pollinator declines. Bumble bees host core and non-core microbiota which may contribute to increased lifetime fitness. The presence of <em>Fructobacillus</em> in the gut microbiomes of bumble bee workers, or the replacement of core symbionts with <em>Fructobacillus</em> bacteria, has been considered a marker of dysbiosis. A phylogenomic analysis and functional genomic characterization of the genomes of 21 <em>Fructobacillus</em> isolates from bumble bees demonstrated that they represented four species, i.e. <em>Fructobacillus cardui</em>, <em>Fructobacillus fructosus, Fructobacillus tropaeoli</em>, and the novel species <em>Fructobacillus evanidus</em> sp. nov. Our results confirmed and substantiated the presence of two phylogenetically and functionally distinct <em>Fructobacillus</em> species clades that differ in genome size, percentage G + C content, the number of coding DNA sequences and metabolic characteristics. Clade 1 and clade 2 species differed in amino acid and, to a lesser extent, in carbohydrate metabolism, with <em>F. evanidus</em> and <em>F. tropaeoli</em> genomes featuring a higher number of complete metabolic pathways. While <em>Fructobacillus</em> genomes encoded genes that allow adhesion, biofilm formation, antibacterial activity and detoxification, other bacteria isolated from the bumble bee gut appeared better equipped to co-exist with the bumble bee host. The isolation and identification of multiple <em>Fructobacillus</em> species from several bumble bee gut samples in the present study also argued against a specific partnership between <em>Fructobacillus</em> species and their bumble bee hosts.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126505"},"PeriodicalIF":3.4,"publicationDate":"2024-03-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140279708","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}
Pub Date : 2024-03-12DOI: 10.1016/j.syapm.2024.126503
Ze-Shen Liu , Xiao-Kang Wang , Ke-Huan Wang , Mei-Ling Yang , De-Feng Li , Shuang-Jiang Liu
A taxonomic investigation was conducted on four bacterial strains isolated from soil contaminated with polycyclic aromatic hydrocarbons and heavy metals. Phylogenetic analysis revealed that these strains belonged to the family Chitinophagaceae. Examination of the 16S rRNA genes indicated that their sequence identities were below 97.6 % compared to any known and validly nominated bacterial species. The genomes of the four strains ranged from 4.12 to 8.76 Mb, with overall G + C molar contents varying from 41.28 % to 50.39 %. Predominant cellular fatty acids included iso-C15:0, iso-C15:1 G, and iso-C17:0 3-OH. The average nucleotide identity ranged from 66.90 % to 74.63 %, and digital DNA-DNA hybridization was 12.5–12.8 %. Based on the genomic and phenotypic features of the new strains, four novel species and two new genera were proposed within the family Chitinophagaceae. The ecological distributions were investigated by data-mining of NCBI databases, and results showed that additional strains or species of the newly proposed taxa were widely distributed in various environments, including polluted soil and waters. Functional analysis demonstrated that strains H1-2-19XT, JS81T, and JY13-12T exhibited resistance to arsenite (III) and chromate (VI). The proposed names for the four novel species are Paraflavitalea pollutisoli (type strain H1-2-19XT = JCM 36460T = CGMCC 1.61321T), Terrimonas pollutisoli (type strain H1YJ31T = JCM 36215T = CGMCC 1.61343T), Pollutibacter soli (type strain JS81T = JCM 36462T = CGMCC 1.61338T), and Polluticoccus soli (type strain JY13-12T = JCM 36463T = CGMCC 1.61341T).
{"title":"Paraflavitalea pollutisoli sp. nov., Pollutibacter soli gen. nov. sp. nov., Polluticoccus soli gen. nov. sp. nov., and Terrimonas pollutisoli sp. nov., four new members of the family Chitinophagaceae from polluted soil","authors":"Ze-Shen Liu , Xiao-Kang Wang , Ke-Huan Wang , Mei-Ling Yang , De-Feng Li , Shuang-Jiang Liu","doi":"10.1016/j.syapm.2024.126503","DOIUrl":"10.1016/j.syapm.2024.126503","url":null,"abstract":"<div><p>A taxonomic investigation was conducted on four bacterial strains isolated from soil contaminated with polycyclic aromatic hydrocarbons and heavy metals. Phylogenetic analysis revealed that these strains belonged to the family <em>Chitinophagaceae</em>. Examination of the 16S rRNA genes indicated that their sequence identities were below 97.6 % compared to any known and validly nominated bacterial species. The genomes of the four strains ranged from 4.12 to 8.76 Mb, with overall G + C molar contents varying from 41.28 % to 50.39 %. Predominant cellular fatty acids included <em>iso</em>-C<sub>15:0</sub>, <em>iso</em>-C<sub>15:1</sub> G, and <em>iso</em>-C<sub>17:0</sub> 3-OH. The average nucleotide identity ranged from 66.90 % to 74.63 %, and digital DNA-DNA hybridization was 12.5–12.8 %. Based on the genomic and phenotypic features of the new strains, four novel species and two new genera were proposed within the family Chitinophagaceae. The ecological distributions were investigated by data-mining of NCBI databases, and results showed that additional strains or species of the newly proposed taxa were widely distributed in various environments, including polluted soil and waters. Functional analysis demonstrated that strains H1-2-19X<sup>T</sup>, JS81<sup>T</sup>, and JY13-12<sup>T</sup> exhibited resistance to arsenite (III) and chromate (VI). The proposed names for the four novel species are <em>Paraflavitalea pollutisoli</em> (type strain H1-2-19X<sup>T</sup> = JCM 36460<sup>T</sup> = CGMCC 1.61321<sup>T</sup>), <em>Terrimonas pollutisoli</em> (type strain H1YJ31<sup>T</sup> = JCM 36215<sup>T</sup> = CGMCC 1.61343<sup>T</sup>), <em>Pollutibacter soli</em> (type strain JS81<sup>T</sup> = JCM 36462<sup>T</sup> = CGMCC 1.61338<sup>T</sup>), and <em>Polluticoccus soli</em> (type strain JY13-12<sup>T</sup> = JCM 36463<sup>T</sup> = CGMCC 1.61341<sup>T</sup>).</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126503"},"PeriodicalIF":3.4,"publicationDate":"2024-03-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140127464","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}
Pub Date : 2024-03-07DOI: 10.1016/j.syapm.2024.126501
Zi-Wen Yang , Wen-Li Liu , Peng Zhang , Dan-Yuan Guo , Hong-Chuan Wang , Jia-Ling Li , Pan-Deng Wang , Gui-Xin Dong , Guo-Xing Nie , Wen-Jun Li
Two novel actinobacteria, designated as SYSU M7M538T and SYSU M7M531, were isolated from oral of Eumetopias jubatus in Zhuhai Chimelong Ocean Kingdom, China. The cells of these microorganisms stained Gram-positive and were rod shaped. These strains were facultative anaerobic, and catalase-positive. Optimal growth occurred at 37 °C and pH 7.0 over 7 days of cultivation. Both strains possessed diphosphatidylglycerol, phosphatidylglycerol and phosphocholine as the major polar lipids. The main menaquinone was MK-9(H4). The major fatty acids were C16:0, C17:1w8c, C17:0, C18:1w9c and C18:0. Analyses of genome sequences revealed that the genome size of SYSU M7M538T was 2.1 Mbp with G + C content of 52.5 %, while the genome size of SYSU M7M531 was 2.3 Mbp with G + C content of 52.7 %. The ANI and 16S rRNA gene analysis results showed that the pairwise similarities between the two strains and other recognized Nitriliruptoria species were less than 64.9 % and 89.0 %, respectively. Phylogenetic analysis of the 16S rRNA gene sequences indicated that strains SYSU M7M538T and SYSU M7M531 formed a well-separated phylogenetic branch distinct from other orders of Nitriliruptoria. Based on the data presented here, these two strains are considered to represent a novel species of a novel genus, for which the name Stomatohabitans albus gen. nov., sp. nov., with the type strain SYSU M7M538T (=KCTC 59113T = GDMCC 1.4286T), are proposed. We also propose that these organisms represent a novel family named Stomatohabitantaceae fam. nov. of a novel order Stomatohabitantales ord. nov.
{"title":"Stomatohabitans albus gen. nov., sp. nov., an oral living facultative anaerobic actinobacteria isolated form Steller sea lion, and proposal of Stomatohabitantaceae fam. nov. and Stomatohabitantales ord. nov","authors":"Zi-Wen Yang , Wen-Li Liu , Peng Zhang , Dan-Yuan Guo , Hong-Chuan Wang , Jia-Ling Li , Pan-Deng Wang , Gui-Xin Dong , Guo-Xing Nie , Wen-Jun Li","doi":"10.1016/j.syapm.2024.126501","DOIUrl":"https://doi.org/10.1016/j.syapm.2024.126501","url":null,"abstract":"<div><p>Two novel actinobacteria, designated as SYSU M7M538<sup>T</sup> and SYSU M7M531, were isolated from oral of <em>Eumetopias jubatus</em> in Zhuhai Chimelong Ocean Kingdom, China. The cells of these microorganisms stained Gram-positive and were rod shaped. These strains were facultative anaerobic, and catalase-positive. Optimal growth occurred at 37 °C and pH 7.0 over 7 days of cultivation. Both strains possessed diphosphatidylglycerol, phosphatidylglycerol and phosphocholine as the major polar lipids. The main menaquinone was MK-9(H<sub>4</sub>). The major fatty acids were C<sub>16:0</sub>, C<sub>17:1</sub> <em><sub>w</sub></em><sub>8</sub><em><sub>c</sub></em>, C<sub>17:0</sub>, C<sub>18:1</sub> <em><sub>w</sub></em><sub>9</sub><em><sub>c</sub></em> and C<sub>18:0</sub>. Analyses of genome sequences revealed that the genome size of SYSU M7M538<sup>T</sup> was 2.1 Mbp with G + C content of 52.5 %, while the genome size of SYSU M7M531 was 2.3 Mbp with G + C content of 52.7 %. The ANI and 16S rRNA gene analysis results showed that the pairwise similarities between the two strains and other recognized <em>Nitriliruptoria</em> species were less than 64.9 % and 89.0 %, respectively. Phylogenetic analysis of the 16S rRNA gene sequences indicated that strains SYSU M7M538<sup>T</sup> and SYSU M7M531 formed a well-separated phylogenetic branch distinct from other orders of <em>Nitriliruptoria</em>. Based on the data presented here, these two strains are considered to represent a novel species of a novel genus, for which the name <em>Stomatohabitans albus</em> gen. nov., sp. nov., with the type strain SYSU M7M538<sup>T</sup> (=KCTC 59113<sup>T</sup> = GDMCC 1.4286<sup>T</sup>), are proposed. We also propose that these organisms represent a novel family named <em>Stomatohabitantaceae</em> fam. nov. of a novel order <em>Stomatohabitantales</em> ord. nov.</p></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"47 2","pages":"Article 126501"},"PeriodicalIF":3.4,"publicationDate":"2024-03-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140066881","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}