| BMC Microbiology | |
| 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 | |
| Lanming Chen3  Hua Wang1  Yinying Zhao3  Jian Cong3  Xiaojun Zhang2  Yingjie Pan3  Bailin Li3  Pan Yu3  Yuze Song3  | |
| [1] The Ohio State University, 2015 Fyffe Court, Columbus, OH 43210, USA;Shanghai Center for Systems Biomedicine, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan road, Minhang Campus, Shanghai 200240, PR China;Key Laboratory of Quality and Safety Risk Assessment for Aquatic Products on Storage and Preservation (Shanghai), China Ministry of Agriculture, Engineering Centre for Quality Control and Risk Assessment of Aquatic Products, College of Food Science and Technology, Shanghai Ocean University, 999 Hu Cheng Huan Road, Shanghai 201306, PR China | |
| 关键词: Estuary; Aquatic products; Drug and heavy metal resistance; ICEs; Vibrios; | |
| Others : 1143006 DOI : 10.1186/1471-2180-13-214 |
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| received in 2013-03-25, accepted in 2013-09-23, 发布年份 2013 | |
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【 摘 要 】
Background
The 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.
Results
The 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.
Conclusions
This 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.
【 授权许可】
2013 Song et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150328211307794.pdf | 793KB | ||
| Figure 2. | 69KB | Image | |
| Figure 1. | 76KB | Image |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Wozniak RA, Waldor MK: Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 2010, 8:552-563.
- [2]Gogarten JP, Townsend JP: Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 2005, 3:679-687.
- [3]Nakayama K, Yamashita A, Kurokawa K, Morimoto T, Ogawa M, Fukuhara M, Urakami H: The whole-genome sequencing of the obligate intracellular bacterium orientia tsutsugamushi revealed massive gene amplification during reductive genome evolution. DNA Res 2008, 15:185-199.
- [4]Burrus V, Waldor MK: Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 2004, 155:376-386.
- [5]Scott JR, Churchward GG: Conjugative transposition. Annu Rev Microbiol 1995, 49:367-397.
- [6]Whittle G, Shoemaker NB, Salyers AA: The role of Bacteroides conjugative transposons in the dissemination of antibiotic resistance genes. Cell Mol Life Sci 2002, 59:2044-2054.
- [7]Burrus V, Marrero J, Waldor MK: The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid 2006, 55:173-183.
- [8]Bani S, Mastromarino PN, Ceccarelli D, Van AL, Salvia AM, Viet QTN, Hai DH, Bacciu D, Cappuccinelli P, Colombo MM: Molecular characterization of ICEVchVieO and its disappearance in Vibrio cholerae O1 strains isolated in 2003 in Vietnam. FEMS Microbiol Lett 2007, 266:42-48.
- [9]Taviani E, Ceccarelli D, Lazaro N, Bani S, Cappuccinelli P, Colwell RR, Colombo MM: Environmental Vibrio spp., isolated in Mozambique, contain a polymorphic group of integrative conjugative elements and class1 integrons. FEMS Microbiol Ecol 2008, 64:45-54.
- [10]Rodríguez-Blanco A, Lemos ML, Osorio CR: Integrating conjugative elements as vectors of antibiotic, mercury, and quaternary ammonium compound resistance in marine aquaculture environments. Antimicrob Agents Chemother 2012, 56:2619-2626.
- [11]Thompson FL, Klose KE, AVIB Group: Vibrio 2005: the first international conference on the biology of vibrios. J Bacteriol 2006, 188:4592-4596.
- [12]Pruss A, Havelaar A: The global burden of disease study and applications in water, sanitation and hygiene. In Water quality: guidelines, standards and health. Edited by Fewtrell L, Bartram J. London: IWA Publishing; 2001:43-59.
- [13]Wilcox BA, Colwell RR: Emerging and reemerging infectious diseases: biocomplexity as an interdisciplinary paradigm. Ecohealth 2005, 2:244-257.
- [14]Waldor MK, Tschape H, Mekalanos JJ: A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol 1996, 178:4157-4165.
- [15]Coetzee JN, Datta N, Hedges RW: R factors from Proteus rettgeri. J Gen Microbiol 1972, 72:543-552.
- [16]Beaber JW, Hochhut B, Waldor MK: Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J Bacteriol 2002, 184:4259-4269.
- [17]Ochman H, Lawrence JG, Groisman EA: Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405:299-304.
- [18]Ochman H, Moran NA: Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 2001, 292:1096-1098.
- [19]Ghosh A, Ramamurthy T: Antimicrobials & cholera: are we stranded? The Ind J Med Res 2011, 133:225-231.
- [20]Chen CC, Gong GC, Shiah FK: Hypoxia in the east china Sea: one of the largest coastal low-oxygen areas in the world. Mar Environ Res 2007, 64:399-408.
- [21]Wang S, Duan H, Zhang W, Li J-W: Analysis of bacterial foodborne disease outbreaks in China between 1994 and 2005. FEMS Immun Med Microbiol 2007, 51:8-13.
- [22]Thompson FL, Iida T, Swings J: Biodiversity of Vibrios. Microbiol Mol Biol Rev 2004, 68:403-431.
- [23]Wozniak RA, Fouts DE, Spagnoletti M, Colombo MM, Ceccarelli D, Ve Garriss G, De’ry C, Burrus V, Waldor MK: Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLOS Genet 2009, 5(12):e10007865.
- [24]Caliani JCF, Muñoz FR, Galán E: Clay mineral and heavy metal distributions in the lower estuary of Huelva and adjacent Atlantic shelf SW, Spain. Sci Total Environ 1997, 198:181-200.
- [25]Juan JVM, María DGR, Manuel GV, María DGC: Bioavailability of heavy metals monitoring water, sediments and fish species from a polluted estuary. J Hazard Mater 2009, 162:823-836.
- [26]An Q, Wu YQ, Wang JH, Li ZE: Assessment of dissolved heavy metal in the Yangtze river estuary and its adjacent sea, China. Environ Monit Assess 2010, 164:173-187.
- [27]Zhao S, Feng C, Quan W, Chen X, Niu J, Shen Z: Role of living environments in the accumulation characteristics of heavy metals in fishes and crabs in the Yangtze river estuary, China. Mar Pollut Bull 2012, 64:1163-1171.
- [28]Pembroke JT, Piterina AV: A novel ICE in the genome of Shewanella putrefaciens W3-18-1: comparison with the SXT/R391 ICE-like elements. FEMS Microbiol Lett 2006, 264:80-88.
- [29]Beaber JW, Burrus V, Hochhut B, Waldor MK: Comparison of SXT and R391, two conjugative integrating elements: definition of a genetic backbone for the mobilization of resistance determinants. Cell Mol Life Sci 2002, 59:2065-2070.
- [30]McGrath BM, O’Halloran JA, Piterina AV, Pembroke JT: Molecular tools to detect the IncJ elements: a family of integrating, antibiotic resistant mobile genetic elements. J Microbiol Methods 2006, 66:32-42.
- [31]Hochhut B, Waldor MK: Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol Microbiol 1999, 32:99-110.
- [32]Llosa M, Gomis-Rüth FX, Coll M, de la Cruz F: Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 2002, 45:1-8.
- [33]Burrus V, Waldor MK: Control of SXT integration and excision. J Bacteriol 2003, 185:5045-5054.
- [34]Nair GB, Faruque SM, Bhuiyan NA, Kamruzzaman M, Siddique AK, Sack DA: New variants of Vibrio cholerae O1 biotype El Tor with attributes of the classical biotype from hospitalized patients with acute diarrhea in Bangladesh. J Clin Microbiol 2002, 40:3296-3299.
- [35]Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, Luscombe NM, Abdellah Z, Arrosmith C, Atkin B, Chillingworth T, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Walker D, Whithead S, Thomson NR, Rather PN, Parkhill J, Mobley HLT: Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol 2008, 190:4027-4037.
- [36]Burrus V, Quezada-Calvillo R, Marrero J, Waldor MK: SXT-related integrating conjugative element in New world Vibrio cholerae. Appl Environ Microbiol 2006, 72:3054-3057.
- [37]Wozniak RA, Waldor MK: A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet 2009, 5(3):e1000439.
- [38]Iwanaga M, Toma C, Miyazato T, Insisiengmay S, Nakasone N, Ehara M: Antibiotic resistance conferred by a class I integron and SXT constin in Vibrio cholerae O1 strains isolated in laos. Antimicrob Agents Chemother 2004, 48:2364-2369.
- [39]Hochhut B, Lotfi Y, Mazel D, Faruque SM, Woodgate R, Waldor MK: Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1 SXT constins. Antimicrob Agents Chemother 2001, 45:2991-3000.
- [40]Ceccarelli D, Spagnoletti M, Bacciu D, Danin-Poleg Y, Mendiratta DK, Kashi Y, Cappuccinelli P, Burrus V, Colombo MM: ICEVchInd5 Is prevalent in epidemic Vibrio cholerae O1 El Tor strains isolated in India. Int J Med Microbiol 2011, 301:318-324.
- [41]Boltner D, MacMahon C, Pembroke JT, Strike P, Osborn AM: R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements. J Bacteriol 2002, 184:5158-5169.
- [42]Achtman M, Manning PA, Kusecek B, Schwuchow S, Willetts N: A genetic analysis of F sex factor cistrons needed for surface exclusion in Escherichia coli. J Mol Biol 1980, 138:779-795.
- [43]Marrero J, Waldor MK: The SXT/R391 family of integrative conjugative elements is composed of two exclusion groups. J Bacteriol 2007, 189:3302-3305.
- [44]Marrero J, Waldor MK: Interactions between inner membrane proteins in donor and recipient cells limit conjugal DNA transfer. Dev Cell 2005, 8:963-970.
- [45]Osborn AM, Bruce KD, Ritchie DA, Strike P: The mercury resistance operon of the IncJ plasmid pMERPH exhibits structural and regulatory divergence from other Gram-negative mer operons. Microbiol 1996, 142(Pt 2):337-345.
- [46]Weisburg WG, Barns SM, Pelletier DA, Lane DJ: 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991, 173:697-703.
- [47]Panicker G, Call DR, Krug MJ, Bej AK: Detection of pathogenic Vibrio spp. in shellfish by using multiplex PCR and DNA microarrays. Appl Environ Microbiol 2004, 70:7436-7444.
- [48]Fields PI, Popovic T, Wachsmuth K, Olsvik O: Use of polymerase chain reaction for detection of toxigenic Vibrio cholerae O1 strains from the latin American cholera epidemic. J Clin Microbiol 1992, 30:2118-2121.
- [49]Larkin MA, Blackshields G, Brown NP, Chenna R, NcGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
- [50]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
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