Comparative genomic analysis of six new-found integrative conjugative elements (ICEs) in Vibrio alginolyticus

Peng Luo,Xiangyan He,Yanhong Wang,Qiuting Liu,Chaoqun Hu

doi:10.1186/s12866-016-0692-9

Abstract

BackgroundVibrio alginolyticus is ubiquitous in marine and estuarine environments. In 2012–2013, SXT/R391-like integrative conjugative elements (ICEs) in environmental V. alginolyticus strains were discovered and found to occur in 8.9 % of 192 V. alginolyticus strains, which suggests that V. alginolyticus may be a natural pool possessing resourceful ICEs. However, complete ICE sequences originating from this bacterium have not been reported, which represents a significant barrier to characterizing the ICEs of this bacterium and exploring their relationships with other ICEs. In the present study, we acquired six ICE sequences from five V. alginolyticus strains and performed a comparative analysis of these ICE genomes.ResultsA sequence analysis showed that there were only 14 variable bases dispersed between ICEValE0601 and ICEValHN492. ICEValE0601 and ICEValHN492 were treated as the same ICE. ICEValA056-1, ICEValE0601 and ICEValHN492 integrate into the 5′ end of the host’s prfC gene, and their Int and Xis share at least 97 % identity with their counterparts from SXT. ICEValE0601 or ICEValHN492 contain 50 of 52 conserved core genes in the SXT/R391 ICEs (not s025 or s026). ICEValA056-2, ICEValHN396 and ICEValHN437 have a different tRNA-ser integration site and a distinct int/xis module; however, the remaining backbone genes are highly similar to their counterparts in SXT/R391 ICEs. DNA sequences inserted into hotspot and variable regions of the ICEs are of various sizes. The variable genes of six ICEs encode a large array of functions to bestow various adaptive abilities upon their hosts, and only ICEValA056-1 contains drug-resistant genes. Many variable genes have orthologous and functionally related genes to those found in SXT/R391 ICEs, such as genes coding for a toxin-antitoxin system, a restriction-modification system, helicases and endonucleases. Six ICEs also contain a large number of unique genes or gene clusters that were not found in other ICEs. Six ICEs harbor more abundant transposase genes compared with other parts of their host genomes. A phylogenetic analysis indicated that transposase genes in these ICEs are highly diverse.ConclusionsICEValA056-1, ICEValE0601 and ICEValHN492 are typical members of the SXT/R391 family. ICEValA056-2, ICEValHN396 and ICEValHN437 form a new atypical group belonging to the SXT/R391 family. In addition to the many genes found to be present in other ICEs, six ICEs contain a large number of unique genes or gene clusters that were not found in other ICEs. ICEs may serve as a carrier for transposable genetic elements (TEs) and largely facilitate the dissemination of TEs.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-016-0692-9) contains supplementary material, which is available to authorized users.

Highlights

Vibrio alginolyticus is ubiquitous in marine and estuarine environments
And annotation of the integrative conjugative elements (ICEs) in V. alginolyticus To obtain the complete sequences of six ICEs, highthroughput HiSeq 2000 sequencing of the genomes of V. alginolyticus strains, A056, E0601, HN396, HN437 and HN492 (Table 1), was carried out
Gap filling was carried out through PCR followed by sequencing, which yielded the complete sequences of ICEValA056-1, ICEValA056-2, ICEValE0601, ICEValHN396, ICEValHN437 and ICEValHN492

Summary

Introduction

Vibrio alginolyticus is ubiquitous in marine and estuarine environments. In 2012–2013, SXT/R391-like integrative conjugative elements (ICEs) in environmental V. alginolyticus strains were discovered and found to occur in 8.9 % of 192 V. alginolyticus strains, which suggests that V. alginolyticus may be a natural pool possessing resourceful ICEs. In 1996, SXT/R391 ICEs were first described in Vibrio cholerae, the etiologic agent of the diarrheal disease cholerae, and in Providencia rettgeri, which was isolated in 1972 [4, 5]. SXT/R391 ICEs were widely found to be prevalent in the 7th pandemic isolates of V. cholerae, other environmental Vibrio species and in some Enterobacteriaceae species [6,7,8,9,10]. A comparative genomic analysis of 13 widely distributed SXT/R391 ICEs indicated that all of these ICEs consist of the same syntenous and nearly identical 52 core genes, whereas other families of closely related mobile elements, such as lambdoid and T4-like phages, exhibit greater diversity [6]. Five hotspots (HS1–HS5) and four variable regions (VR I–IV) are interspaced into the conserved backbone of ICEs, and these variable DNAs generally code for resistance to antibiotics, heavy metals and bacteriophage infection, toxin/antitoxin (TA) systems or c-di-GMP synthesis [6, 7, 11,12,13,14], which confer hosts adaptive functions to various environments

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