A Re-evaluation of the Taxonomy and Classification of the Type III Secretion System in a Pathogenic Bacterium Causing So

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A Re‑evaluation of the Taxonomy and Classification of the Type III Secretion System in a Pathogenic Bacterium Causing Soft Rot Disease of Pleurotus eryngii Feng Xu1 · Hui Yan2 · Yu Liu1 · Shuang Zhao1 · Shuang Song1 · Tongtong Gu1 · Zhongjuan Song1 · Jianbo Xie3 · Chengbo Rong1  Received: 30 October 2019 / Accepted: 13 October 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Pantoea beijingensis, a gram-negative pathogenic bacterium, causes soft rot disease in the fungus Pleurotus eryngii in China. However, the taxonomic classification of this pathogen is controversial due to close relationships between bacteria of the genera Pantoea and Erwinia. This study aimed to resolve the identity of P. beijingensis using phylogenomic and systematic analyses of Pantoea and Erwinia by whole-genome sequencing. Single-copy orthologs identified from the Erwinia/Pantoea core genomes were used to delineate Erwinia/Pantoea phylogeny. P. beijingensis ­LMG27579T clustered within a single Erwinia clade. A whole-genome-based phylogenetic tree and average nucleotide and amino-acid identity values indicate that P. beijingensis ­LMG27579T should be renamed Erwinia beijingensis. The hrp/hrc genes encoding type III secretion system (T3SS) proteins in Erwinia and Pantoea were divided into five groups according to gene contents and organization. Neighbor-joining-inferred phylogenetic trees based on concatenated HrcU, HrcN, and HrcR in the main hrp/hrc cluster showed that E. beijingensis T3SS proteins are closely related to those in Ewingella americana, implying that E. beijingensis and E. americana have a recent common hrp/hrc gene ancestor. Furthermore, T3SS proteins of Erwinia and Pantoea were clustered in different clades separated by other bacterial T3SS proteins. Thus, T3SS genes in Pantoea and Erwinia strains might have been acquired by horizontal gene transfer. Overall, our findings clarify the taxonomy of the bacterium causing soft rot in P. eryngii, as well as the genetic structure and classification of the hrp/hrc T3SS virulence factor. We propose that T3SS acquisition is important for E. beijingensis emergence and pathogenesis.

Introduction Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0028​4-020-02253​-3) contains supplementary material, which is available to authorized users. Feng Xu and Hui Yan have contributed equally to this work. * Jianbo Xie [email protected] * Chengbo Rong [email protected] 1



Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, Beijing 100097, China

2



College of Animal Science and Technology, Hebei Agricultural University, Baoding 071001, China

3

National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China



The genus Pantoea in the family Enterobacteriaceae comprises a diverse group of bacteria, some of which are recogn