Abstract

Bacteriophages (phages) and their bacterial hosts were the most abundant and genetically highly diverse organisms on the earth. In this study, a series of phage-resistant mutant (PRM) strains derived from Vibrio alginolyticus were isolated and Infrequent-restriction-site PCR (IRS-PCR) was used to investigate the genetic diversity of the PRM strains. Phenotypic variations of eight PRM strains were analyzed using profiles of utilizing carbon sources and chemical sensitivity. Genetic variations of eight PRM strains and coevolved V. alginolyticus populations with phages were analyzed by whole-genome sequencing and resequencing, respectively. The results indicated that eight genetically discrepant PRM stains exhibited abundant and abundant phenotypic variations. Eight PRM strains and coevolved V. alginolyticus populations (VE1, VE2, and VE3) contained numerous single nucleotide variations (SNVs) and insertions/indels (InDels) and exhibited obvious genetic divergence. Most of the SNVs and InDels in coding genes were related to the synthesis of flagellar, extracellular polysaccharide (EPS), which often served as the receptors of phage invasion. The PRM strains and the coevolved cell populations also contained frequent mutations in tRNA and rRNA genes. Two out of three coevolved populations (VE1 and VE2) contained a large mutation segment severely deconstructing gene nrdA, which was predictably responsible for the booming of mutation rate in the genome. In summary, numerous mutations and genetic divergence were detected in the genomes of V. alginolyticus PRM strains and in coevolved cell populations of V. alginolyticus under phage infection stress. The phage infection stress may provide an important force driving genomic evolution of V. alginolyticus.

Highlights

  • Bacteriophages and their bacterial hosts are the most abundant and genetically highly diverse organisms on the earth (Suttle, 2005; Weitz et al, 2013; Batinovic et al, 2019)

  • Biolog assays clearly indicated that eight phageresistant mutant (PRM) strains generated rich and obvious phenotypic changes and these changes were not significantly associated with anti-phage infection, which suggested the genetic variations harbored in these PRM strains

  • In three PRM strains, three variant genes related to flagella synthesis and regulation, flhA, fliF, and fleQ, were detected, among which the single nucleotide variations (SNVs) in flhA and fliF resulted in the premature termination of flagella synthesis

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Summary

Introduction

Bacteriophages (phages) and their bacterial hosts are the most abundant and genetically highly diverse organisms on the earth (Suttle, 2005; Weitz et al, 2013; Batinovic et al, 2019). Bacteria–phage interaction is believed as an important driver of ecological and evolutionary processes for both communities (Fuhrman, 1999; Koskella and Brockhurst, 2014; Shabbir et al, 2016; Hampton et al, 2020), studies on genetic variations of PRM strains and genomic evolution of coevolved bacterial populations with phages are very rare. Scanlan et al (2015) first revealed that coevolution with phage Phi drives genomic-wide host evolution and constrains the acquisition of abiotic-beneficial mutations in Pseudomonas fluorescens through whole-genome sequencing, and the isolates with discrepant phenotypes in coevolved populations exhibited much more numerous mutations and much higher genetic divergence compared to these in evolved populations (Scanlan et al, 2015). As the technique was only used to investigate occurrence frequencies of mutation sites from the perspective of phage φ2 when it was coevolved with its host P. fluorescens (Paterson et al, 2010)

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