Pangenome analysis of Paenibacillus polymyxa strains reveals the existence of multiple and functionally distinct Paenibacillus species.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Applied and Environmental Microbiology Pub Date : 2024-11-20 Epub Date: 2024-10-30 DOI:10.1128/aem.01740-24
Federica Maggi, Anna Maria Giuliodori, Anna Brandi, Lucia Cimarelli, Roberto Alcántara, Stefano Pallotti, Consuelo Amantini, Dezemona Petrelli, Attilio Fabbretti, Roberto Spurio, Valerio Napolioni
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Abstract

Paenibacillus polymyxa, a Gram-positive bacterium commonly found in soil and plant roots, plays an important role in the environment due to its nitrogen-fixing ability and is renowned for producing antibiotics like polymyxin. In this study, we present a robust framework for investigating the evolutionary and taxonomic connections of strains belonging to P. polymyxa available at the National Center for Biotechnology Information, as well as five new additional strains isolated at the University of Camerino (Italy), through pangenome analysis. These strains can produce secondary metabolites active against Staphylococcus aureus and Klebsiella pneumoniae. Employing techniques such as digital DNA-DNA hybridization (dDDH), average nucleotide identity (ANI) estimation, OrthoFinder, and ribosomal multilocus sequence typing, we consistently divided these P. polymyxa strains into four clusters, which differ significantly in terms of ANI and dDDH percentages, both considered as reference indices for separating bacterial species. Moreover, the strains of Cluster 2 were re-classified as belonging to the Paenibacillus ottowii species. By comparing the pangenomes, we identified the core genes of each cluster and analyzed them to recognize distinctive features in terms of biosynthetic/metabolic potential. The comparison of pangenomes also allowed us to pinpoint differences between clusters in terms of genetic variability and the percentage of the genome dedicated to core and accessory genes. In conclusion, the data obtained from our analyses of strains belonging to the P. polymyxa species converge toward a necessary reclassification, which will require a fundamental contribution from microbiologists in the near future.

Importance: The development of sequencing technologies has led to an exponential increase in microbial sequencing data. Accurately identifying bacterial species remains a challenge because of extensive intra-species variability, the need for multiple identification methods, and the rapid rate of taxonomic changes. A substantial contribution to elucidating the relationships among related bacterial strains comes from comparing their genomic sequences. This comparison also allows for the identification of the "pangenome," which is the set of genes shared by all individuals of a species, as well as the set of genes that are unique to subpopulations. Here, we applied this approach to Paenibacillus polymyxa, a species studied for its potential as a biofertilizer and biocontrol agent and known as an antibiotic producer. Our work highlights the need for a more efficient classification of this bacterial species and provides a better delineation of strains with different properties.

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对多粘菌 Paenibacillus polymyxa 菌株进行的泛基因组分析表明,存在多个功能不同的 Paenibacillus 菌种。
多粘杆菌(Paenibacillus polymyxa)是一种常见于土壤和植物根部的革兰氏阳性细菌,因其固氮能力而在环境中发挥着重要作用,并以生产多粘菌素等抗生素而闻名。在本研究中,我们提出了一个强大的框架,通过泛基因组分析,研究美国国家生物技术信息中心提供的多粘菌菌株以及卡梅里诺大学(意大利)分离的另外五株新菌株在进化和分类学上的联系。这些菌株能产生对金黄色葡萄球菌和肺炎克雷伯菌有活性的次级代谢物。利用数字 DNA-DNA 杂交(dDDH)、平均核苷酸同一性(ANI)估算、OrthoFinder 和核糖体多焦点序列分型等技术,我们一致地将这些多粘菌菌株分为四个簇,这四个簇在 ANI 和 dDDH 百分比(均被视为分离细菌物种的参考指标)方面存在显著差异。此外,簇 2 中的菌株被重新归类为属于 Paenibacillus ottowii 菌种。通过比较泛基因组,我们确定了每个群组的核心基因,并对其进行了分析,以识别其在生物合成/代谢潜力方面的显著特征。通过比较庞基因组,我们还能确定不同群组在遗传变异以及核心基因和附属基因在基因组中所占比例方面的差异。总之,我们对属于多粘菌属的菌株进行分析所获得的数据趋向于进行必要的重新分类,这需要微生物学家在不久的将来做出根本性的贡献:测序技术的发展导致微生物测序数据呈指数级增长。由于种内变异性大、需要多种鉴定方法以及分类变化速度快,准确鉴定细菌物种仍是一项挑战。比较相关细菌菌株的基因组序列有助于阐明它们之间的关系。通过比较还可以确定 "泛基因组",即一个物种所有个体共有的基因组,以及亚群特有的基因组。在这里,我们将这种方法应用于多粘毛芽孢杆菌(Paenibacillus polymyxa),该菌种因其具有生物肥料和生物控制剂的潜力而被研究,并以生产抗生素而闻名。我们的工作强调了对这种细菌进行更有效分类的必要性,并对具有不同特性的菌株进行了更好的划分。
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来源期刊
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
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