Horizontal Gene Transfer Clarifies Taxonomic Confusion and Promotes the Genetic Diversity and Pathogenicity of Plesiomonas shigelloides

Abstract

Plesiomonas shigelloides is an emerging pathogen that has been shown to be involved in gastrointestinal diseases and extraintestinal infections in humans. However, the taxonomic position, evolutionary dynamics, and pathogenesis of P. shigelloides remain unclear. We reported the draft genome sequences of 12 P. shigelloides strains representing different serogroups. We were able to determine a clear distinction between P. shigelloides and other members of Enterobacterales via core genome phylogeny, Neighbor-Net network, and average genome identity analysis. The pan-genome analysis of P. shigelloides revealed extensive genetic diversity and presented large flexible gene repertoires, while the core genome phylogeny exhibited a low level of clonality. The discordance between the core genome phylogeny and the pan-genome phylogeny indicated that flexible accessory genomes account for an important proportion of the evolution of P. shigelloides, which was subsequently characterized by determinations of hundreds of horizontally transferred genes (horizontal genes), massive gene expansions and contractions, and diverse mobile genetic elements (MGEs). The apparently high levels of horizontal gene transfer (HGT) in P. shigelloides were conferred from bacteria with novel properties from other taxa (mainly Vibrionaceae and Aeromonadaceae), which caused the historical taxonomic confusion and shaped the virulence gene pools. Furthermore, P. shigelloides genomes contain many macromolecular secretion system genes, virulence factor genes, and resistance genes, indicating its potential to cause intestinal and invasive infections. Collectively, our work provides insights into the phylogenetic position, evolutionary dynamic, and pathogenesis of P. shigelloides at the genomic level, which could facilitate the observation and research of this important pathogen. IMPORTANCE The taxonomic position of P. shigelloides has been the subject of debate for a long time, and until now, the evolutionary dynamics and pathogenesis of P. shigelloides were unclear. In this study, pan-genome analysis indicated extensive genetic diversity and the presence of large and variable gene repertoires. Our results revealed that horizontal gene transfer was the focal driving force for the genetic diversity of the P. shigelloides pan-genome and might have contributed to the emergence of novel properties. Vibrionaceae and Aeromonadaceae were found to be the predominant donor taxa for horizontal genes, which might have caused the taxonomic confusion historically. Comparative genomic analysis revealed the potential of P. shigelloides to cause intestinal and invasive diseases. Our results could advance the understanding of the evolution and pathogenesis of P. shigelloides, particularly in elucidating the role of horizontal gene transfer and investigating virulence-related elements.

Metabacillus dongyingensis sp. nov. Is Represented by the Plant Growth-Promoting Bacterium BY2G20 Isolated from Saline-Alkaline Soil and Enhances the Growth of Zea mays L. under Salt Stress

“…Comparisons of the genomic characteristics to saline-alkaline adaptation between BY2G20 and M. idriensis DSM-19097 T yielded significantly lower average K a / K s values (0.052 ± 0.034; t test P value < 0.01) compared to that of the core genome (average K a / K s = 0.084 ± 0.07), indicating the predominant action of purifying selection. The genes with lower K a / K s values have a stronger tendency to keep their functions ( 39 ). It can be inferred that the genes adapted to saline-alkaline ecosystems under functional constraints maintained a stable and adapted genomic characteristic for BY2G20.…”

Comprehensive Scanning of Prophages in Lactobacillus : Distribution, Diversity, Antibiotic Resistance Genes, and Linkages with CRISPR-Cas Systems

“…However, in some cases, prophages can be induced into a lytic cycle by stressful environmental factors ( 1 ), and as a result, their DNA is excised from bacterial genomes ( 2 ), replicated, and packaged into complete phage particles, facilitating horizontal gene transfer (HGT) ( 3 ). Prophages are involved in several bacterial life processes; the expression of prophage functional genes can confer survival advantages on lysogens in adverse environments ( 4 , 5 ); virulent genes carried by prophages not only increase the virulence of the host bacteria ( 6 ) but can even convert a nonvirulent strain into a pathogenic strain ( 7 ); antibiotic resistance genes (ARGs) can be disseminated via phage-mediated transduction ( 8 ), possibly enhancing bacterial pathogenicity. Therefore, it is becoming increasingly evident that elucidation of the roles of prophages in the bacterial life cycle is pertinent to the complete understanding of bacterial physiology, evolution, and population dynamics.…”

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

“…1A ), suggesting extensive genetic diversity and high recombination rates. Similarly, Vibrio cholerae and Plesiomonas shigelloides have been reported to exhibit low-level clonality because of extensive genetic diversity and high recombination rates ( 26 , 27 ). We also performed Neighbor-Net network analysis to better visualize the relationships between D. tsuruhatensis genomes.…”