Pan-Genome Analysis of Delftia tsuruhatensis Reveals Important Traits Concerning the Genetic Diversity, Pathogenicity, and Biotechnological Properties of the Species

Zhiqiu Yin; Xinbei Liu; Chengqian Qian; Li Sun; Shiqi Pang; Jianing Liu; Wei Li; Weiwei Huang; Shiyu Cui; Chengkai Zhang; Weixing Song; Dandan Wang; Zhihong Xie

doi:10.1128/spectrum.02072-21

Microbiology Spectrum (Apr 2022)

Pan-Genome Analysis of Delftia tsuruhatensis Reveals Important Traits Concerning the Genetic Diversity, Pathogenicity, and Biotechnological Properties of the Species

Zhiqiu Yin,
Xinbei Liu,
Chengqian Qian,
Li Sun,
Shiqi Pang,
Jianing Liu,
Wei Li,
Weiwei Huang,
Shiyu Cui,
Chengkai Zhang,
Weixing Song,
Dandan Wang,
Zhihong Xie

Affiliations

Zhiqiu Yin: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Xinbei Liu: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Chengqian Qian: Foshan Haitian Flavouring & Food Co. Ltd. (Haitian), Foshan, Guangdong, People’s Republic of China
Li Sun: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Shiqi Pang: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Jianing Liu: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Wei Li: College of Plant Protection, Shanxi Agricultural University, Taiyuan, People’s Republic of China
Weiwei Huang: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Shiyu Cui: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Chengkai Zhang: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Weixing Song: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Dandan Wang: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China
Zhihong Xie: National Engineering Research Center for Efficient Utilization of Soil and Fertilizer Resources, College of Resources and Environment, Shandong Agricultural University, Tai’an, People’s Republic of China

DOI: https://doi.org/10.1128/spectrum.02072-21
Journal volume & issue: Vol. 10, no. 2

Abstract

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ABSTRACT Delftia tsuruhatensis strains have long been known to promote plant growth and biological control. Recently, it has become an emerging opportunistic pathogen in humans. However, the genomic characteristics of the genetic diversity, pathogenicity, and biotechnological properties have not yet been comprehensively investigated. Here, a comparative pan-genome analysis was constructed. The open pan-genome with a large and flexible gene repertoire exhibited a high degree of genetic diversity. The purifying selection was the main force to drive pan-genome evolution. Significant differences were observed in the evolutionary relationship, functional enrichment, and degree of selective pressure between the different components of the pan-genome. A high degree of genetic plasticity was characterized by the determinations of diverse mobile genetic elements (MGEs), massive genomic rearrangement, and horizontal genes. Horizontal gene transfer (HGT) plays an important role in the genetic diversity of this bacterium and the formation of genomic traits. Our results revealed the occurrence of diverse virulence-related elements associated with macromolecular secretion systems, virulence factors associated with multiple nosocomial infections, and antimicrobial resistance, indicating the pathogenic potential. Lateral flagellum, T1SS, T2SS, T6SS, Tad pilus, type IV pilus, and a part of virulence-related genes exhibited general properties, whereas polar flagellum, T4SS, a part of virulence-related genes, and resistance genes presented heterogeneous properties. The pan-genome also harbors abundant genetic traits related to secondary metabolism, carbohydrate active enzymes (CAZymes), and phosphate transporter, indicating rhizosphere adaptation, plant growth promotion, and great potential uses in agriculture and biological control. This study provides comprehensive insights into this uncommon species from the genomic perspective. IMPORTANCE D. tsuruhatensis is considered a plant growth-promoting rhizobacterium (PGPR), an organic pollutant degradation strain, and an emerging opportunistic pathogen to the human. However, the genetic diversity, the evolutionary dynamics, and the genetic basis of these remarkable traits are still little known. We constructed a pan-genome analysis for D. tsuruhatensis and revealed extensive genetic diversity and genetic plasticity exhibited by open pan-genome, diverse mobile genetic elements (MGEs), genomic rearrangement, and horizontal genes. Our results highlight that horizontal gene transfer (HGT) and purifying selection are important forces in D. tsuruhatensis genetic evolution. The abundant virulence-related elements associated with macromolecular secretion systems, virulence factors, and antimicrobial resistance could contribute to the pathogenicity of this bacterium. Therefore, clinical microbiologists need to be aware of D. tsuruhatensis as an opportunistic pathogen. The genetic profiles of secondary metabolism, carbohydrate active enzymes (CAZymes), and phosphate transporter could provide insight into the genetic armory of potential applications for agriculture and biological control of D. tsuruhatensis in general.

Published in Microbiology Spectrum

ISSN: 2165-0497 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/spectrum

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