The mosaic accessory gene structures of the SXT/R391-like integrative and conjugative elements derived from Vibrio spp. isolated from aquatic products and environment in the Yangtze River estuary, China

Abstract

BackgroundThe emergence, resurgence and spread of human food-borne pathogenic Vibrios are one of the major contributors to disease burden and mortality particularly in developing countries with disputable sanitary conditions. Previous research on pathogenic Vibrio cholerae and Vibrio parahaemolitycus derived from clinical samples has proposed links between acquisition of virulence and multiple drug resistance traits and intercellular transmissibility of mobile genetic elements in the environment. To date, very few information is available on environmental Vibrio isolates. In this study, we characterized eleven Vibrio strains bearing the SXT/R391-like integrative and conjugative elements (ICEs) derived from aquatic products and environment in the Yangtze River Estuary, China.ResultsThe eleven Vibrio strains were isolated in 2010 to 2011, and taxonomically identified, which included six Vibrio cholerae, three Vibrio parahaemolyticus, one Vibrio alginolyticus and one Vibrio natriegens. Most of the strains displayed strong resistance phenotypes to ampicillin, mercury and chromium. The majority of their ICEs, which belong to S and R exclusion system groups, contain ICEs-chromosome junction sequences and highly conserved core-genes required for ICE transfer. However, comparative sequence analysis uncovered interesting diversity in their mosaic accessory gene structures, which carry many novel genes that have not been described in any known ICEs to date. In addition, antibiotic resistance was transmitted by ICEVchChn6 and ICEVpaChn1 from V. cholerae, V. parahaemolyticus to E. coli MG1655 via conjugation, respectively. Our data also revealed that the ICEs characterized in this study are phylogenetically distant from most of the SXT/R391 ICEs reported previously, which may represent a novel cluster likely shaped by the ecological environment in the Yangtze River Estuary, China.ConclusionsThis study constitutes the first investigation of ICEs-positive Vibrio spp. in the Yangze River Estuary, China. The newly identified ICEs were characterized with mosaic accessory gene structures and many novel genes. The results demonstrated self-transmissibility of antibiotic resistance mediated by two of the ICEs from V. cholerae, V. parahaemolyticus to E. coli via conjugation, respectively. Our results also revealed that the ICEs examined in this study may represent a novel cluster in the SXT/R391 family.

Comparative genomics for non-O1/O139 Vibrio cholerae isolates recovered from the Yangtze River Estuary versus V. cholerae representative isolates from serogroup O1

“…Additionally, a relatively narrow resistance gene pattern yielded by LMA3984-4 was observed when compared with CHN108B, as some genes for resistance to fluoroquinolone (gyrAB), rifampin (rpoB), penicillin-binding protein (pbp1A), and streptogramin (VatD) were absent from the LMA3984-4 genome, but present in CHN108B, likely resulting from the significant difference in their geographic origin and selective pressure. High incidences of antibiotic resistant V. cholerae isolates of the Yangtze River Estuary origin have been reported previously and presumably arose from the abuse of drugs and the inappropriate release of industrial wastes into the environment (Song et al 2013;He et al 2015a).…”

“…Vibrio cholerae CHN108B was isolated from surface water from the Yangtze River Estuary in Shanghai, China in 2011 (Song et al 2013). The bacterium was identified as non-O1/ O139 serogroup and non-toxic (ct − tcp − ) in a previous study.…”

“…Many comparative analyses of these V. cholerae genomes have been reported (e.g., Banerjee et al 2014;Dutilh et al 2014;Okada et al 2014;Garrine et al 2017;Imamura et al 2017). In the present study, we determined the complete genome sequence of V. cholerae CHN108B (non-O1/O139 serogroup, ct − tcp − ), which was recently isolated from surface water from the Yangtze River Estuary, China (Song et al 2013), to address the lack of complete genome data regarding this bacterium originating from an estuary environment in China (Yi et al 2014). We also conducted comparative genomic analysis between CHN108B and the 8 representative V. cholerae isolates available online when the project began, including N16961, M66-2, O395 uid58425, and O395 uid159869, IEC224, MJ-1236, LMA3984-4 and 2010EL-1786 Table S1).…”

Co-selection of antibiotic and heavy metal resistance in freshwater bacteria

“…Fard and co-workers (2011) isolated 192 enterococcal strains from pigs which were all intermediately resistant to Cu (most of them through the efflux pump tcrB; Hasman and Aarestrup, 2005), and approximatively 40% were also resistant to Zn at different levels. In another case, Vibrio cholerae and Vibrio pahraemoliticus isolated from water and shrimps were resistant to Cu, Cd, Hg, Zn, and Pb (Song et al, 2013). Staphylococcus aureus strains from humans were found resistant to Cu and Cd (Gómez-Sanz et al, 2013), and a clinical Pseudomonas aeruginosa isolate was resistant to Cu and Zn (Ramírez-Díaz et al, 2011).…”

Insights into Vibrio parahaemolyticus CHN25 Response to Artificial Gastric Fluid Stress by Transcriptomic Analysis

“…To gain an insight into the V. parahaemolyticus CHN25 tolerance to acid conditions, we determined growth curves of the bacterium, recently isolated and identified by Song et al [ 15 ], in Tryptic Soy Broth (TSB) with the pH range of 1.5–12.5 at 37 °C. As illustrated in Figure 1 A, V. parahaemolyticus CHN25 grows at pH 5.5–11.5, optimally at pH 8.5, demonstrating it is a moderately basophilic bacterium, consistent with previous studies (e.g., [ 5 ]).…”