Abstract
Multi-drug resistance and transfer of mobile genetic elements among enteric pathogens is being reported to have increased rapidly. Commensal Escherichia coli was previously known to acquire mobile genetic elements from other genus/species. E. coli is also capable of disseminating these elements containing antimicrobial resistance determinants through horizontal transfer. Similarly, for Shigellae the antimicrobial resistance are on rise for fluoroquinolones and cephalosporins due to accumulation of mobile elements. Thus the study was hypothesized to investigate the role of transferable plasmids in commensal MDR E. coli vs Salmonella spp, and MDR Shigella flexneri vs Salmonella spp. pKP3-A plasmid containing qnrS1 was successfully transferred from E. coli to Salmonella spp. Similarly, a plasmid containing qnrS1 and blaCTX-M-15 was transferred from Shigella to Salmonella spp. However, blaCTX-M-15 was not transferred from E. coli as it was integrated into chromosome that was revealed by next-generation sequencing. This might be a reason that fluoroquinolone-resistant determinants are more frequently transferred than the cephalosporin resistant determinants. Findings from the study emphasize that mobile elements with AMR determinants are significant public health concern that has potential to rapidly disseminate.
Similar content being viewed by others
References
Dantas G, Sommer MOA (2014) How to fight back against antibiotic resistance. Am Sci 102:42–51
Kemboi WK, Raphael W, Ramesh F (2014) Horizontal gene transfer of drug resistance genes between Salmonella and Escherichia coli. Int J Bioassays 3:3066–3072
Von Wintersdorff CJ, Penders J, Stobberingh EE, Oude Lashof AM, Hoebe CJ, Savelkoul PH, Wolffs PF (2014) High rates of antimicrobial drug resistance gene acquisition after international travel, The Netherlands. Emerg Infect Dis 20:649–657
Szmolka A, Nagy B (2013) Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol 4:258
Gua B, Kea X, Pana S, Caoa Y, Zhuangc L, Yud R, Qianc H, Liua G, Tong M (2013) Prevalence and trends of aminoglycoside resistance in Shigella worldwide, 1999-2010. J Biomed Res 27:103–115
World Health Organization (2005) Guidelines for the control of Shigellosis, including epidemics due to Shigella dysenteriae 1
Patil DP, Lava R (2012) Identification, characterization and antibiotic susceptibility of Shigella species isolated from stool samples in children. Int J Biol Med Res 3:1640–1643
Taneja N (2007) Changing Epidemiology of Shigellosis and Emergence of Ciprofloxacin resistant Shigellae in India. J Clin Microbiol 45:678
Ling JM, Chan EW, Lam AW, Cheng AF (2003) Mutations in topoisomerase genes of fluoroquinolone-resistant Salmonellae in Hong Kong. Antimicrob Agents Chemother 47:3567–3573
Afzal A, Sarwar Y, Ali A, Haque A (2012) Current status of fluoroquinolone and cephalosporin resistance in Salmonella enterica serovar Typhi isolates from Faisalabad, Pakistan. Pak J Med Sci 28:602–607
Centre for Disease Dynamics, Economics and Policy. https://www.resistancemap.cddep.org/. Accessed 08 Sep 2018
Ghosh S, Pazhani GP, Niyogi SK, Nataro JP, Ramamurthy T (2014) Genetic characterization of Shigella spp. isolated from diarrhoeal and asymptomatic children. J Med Microbiol 63:903–910
Taneja N, Mewara A, Kumar A, Verma G, Sharma M (2012) Cephalosporin-resistant Shigella flexneri over 9 years (2001-09) in India. J Antimicrob Chemother 67:1347–1353
Menezes GA, Khan MA, Harish BN, Parija SC, Goessens W, Vidyalakshmi K, Baliga S, Hays JP (2010) Molecular characterization of antimicrobial resistance in non-typhoidal Salmonellae associated with systemic manifestations from India. J Med Microbiol 59:1477–1483
Muthuirulandi Sethuvel DP, Anandan S, Devanga Ragupathi NK, Veeraraghavan B, Vinod O, Walia K (2015) Association of bla CTX-M-15 and qnr genes in multidrug-resistant Salmonella Typhimurium and Shigella spp from India. J Infect Dev Ctries 30:1294–1297
CLSI (2014) Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement M100-S24
Perez-Perez FJ, Hanson ND (2002) Detection of plasmid-mediated AmpC -Lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40:2153–2162
Gay K, Robicsek AA, Strahilevitz AJ, Park CH, Jacoby G, Barrett TJ, Medalla F, Chiller TM, Hooper DC (2006) Plasmid-mediated quinolone resistance in non-typhi serotypes of Salmonella enterica. Clin Infect Dis 43:297–304
Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T, Gabbard JL, Gillespie JJ, Gough R, Hix D, Kenyon R, Machi D, Mao C, Nordberg EK, Olson R, Overbeek R, Pusch GD, Shukla M, Schulman J, Stevens RL, Sullivan DE, Vonstein V, Warren A, Will R, Wilson MJC, Seung Yoo H, Zhang C, Zhang Y, Sobral BW (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucl Acids Res 42:D581–D591
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid Annotations using Subsystems Technology. BMC Genomics 9:75
Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365
Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42:D206–D214
Sun D, Zhang Y, Mei Y, Jiang H, Xie Z, Liu H, Chen X, Shen P (2006) Escherichia coli is naturally transformable in a novel transformation system. FEMS Microbiol Lett 265:249–255
Pornsukarom S, Thakur S (2017) Horizontal dissemination of antimicrobial resistance determinants in multiple Salmonella serotypes following isolation from the environment of commercial swine operations after manure application. Appl Environ Microbiol 1:1–10. https://doi.org/10.1128/AEM.01503-17
Levy SB (1997) Antibiotic resistance: an ecological imbalance. In: Chadwick DJ, Jamie A (eds) Antibiotic resistance: origins, evolution, selection and spread. Wiley, New York, pp 1–14
Tauxe RV, Cavanagh TR, Cohen ML (1989) Interspecies gene transfer in vivo producing an outbreak of multiply resistant Shigellosis. J Infect Dis 160:1067–1070
Su LH, Chiu CH, Chu C, Ou JT (2004) Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin Infect Dis 39:546–551
Xiao-Ying P, Jing-Cao P, Hao-Qiu W, Zhang W, Zhi-Cheng H, Yang-Ming Gu (2009) Characterization of fluoroquinolone-resistant Shigella flexneri in Hangzhou area of China. J Antimicrob Chemother 63:917–920
Potron A, Nordmann P, Lafeuille E, Al Maskari Z, Al Rashdi F, Poirel L (2011) Characterization of OXA-181, a carbapenem-hydrolyzing class D beta-lactamase from Klebsiella pneumoniae. Antimicrob Agents Chemother 55:4896–4899
Sidjabat HE, Kennedy K, Silvey A, Collignon P, Paterson DL (2013) Emergence of bla(OXA-181)-carrying ColE plasmid in Klebsiella pneumoniae in Australia. Int J Antimicrob Agents 41:294–296
Cheung TK, Chu YW, Tsang GK, Ngan JY, Hui IS, Kam KM (2005) Emergence of CTX-M-type beta-lactam resistance in Shigella spp in Hong Kong. Int J Antimicrob Agents 25:350–352
Auda IG (2014) Occurrence of CTX-M-I and CTX-M-III genes on plasmids of Shigella species isolated from cases of diarrhea in Baghdad. World J Pharm Res 3:1273–1280
Hopkins KL, Liebana E, Villa L, Batchelor M, Threlfall EJ, Carattoli A (2006) Replicon typing of plasmids carrying CTX-M or CMY β-lactamases circulating among Salmonella and Escherichia coli isolates. Antimicrob Agents Chemother 50:3203–3206
Akiba M, Sekizuka T, Yamashita A, Kuroda M, Fujii Y, Murata M, Lee K-I, Joshua DI, Balakrishna K, Bairy I, Subramanian K, Krishnan P, Munuswamy N, Sinha RK, Iwata T, Kusumoto M, Guruge KS (2016) Distribution and relationships of antimicrobial resistance determinants among extended-spectrum-cephalosporin-resistant or carbapenem-resistant Escherichia coli isolates from rivers and sewage treatment plants in India. Antimicrob Agents Chemother 60:2972–2980. https://doi.org/10.1128/AAC.01950-15
Li Y, Xie X, Xu X, Wang X, Chang H, Wang C, Wang A, He Y, Yu H, Wang X, Zeng M (2014) Nontyphoidal Salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog Dis 11:200–206
Bhavnani D, Goldstick JE, Cevallos W, Trueba G, Eisenberg JN (2012) Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: evidence from a community-based study in northwestern Ecuador. Am J Epidemiol 176:387–395
Liu Y, Feng Y, Wu Xie Y, Wang X, Zhang X, Zong CZ (2015) First report of OXA-181-producing Escherichia coli in china and characterization of the isolate using whole-genome sequencing. Antimicrob Agents Chemother 59:5022–5025
Zurfluh K, Klumpp J, Poirel L, Nordmann P, Stephan R (2015) First detection of Klebsiella variicola producing OXA-181 carbapenemase in fresh vegetable imported from Asia to Switzerland. Antimicrob Resist Infect Control 4:38
Veeraraghavan B, Anandan S, Muthuirulandi Sethuvel DP, Puratchiveeran N, Walia K, Devanga Ragupathi NK (2016) Molecular characterization of intermediate susceptible Typhoidal Salmonella to ciprofloxacin and its impact. Mol Diagn Ther 20:213–219
Nordmann P, Dortet L, Poirel L (2012) Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med 18:263–272
da Costa PM, Loureiro L, Matos AJ (2013) Transfer of multidrug-resistant bacteria between intermingled ecological niches: the interface between humans, animals and the environment. Int J Environ Res Public Health 10:278–294
Acknowledgements
The authors gratefully acknowledge the Institutional Review Board of the Christian Medical College, Vellore (83-i/11/13) for approving the study and providing lab space and facilities.
Funding
The study was funded by the Indian Council of Medical Research (ICMR), New Delhi (Ref. No: AMR/TF/55/13ECDII dated 23/10/2013).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Devanga Ragupathi, N.K., Muthuirulandi Sethuvel, D.P., Gajendran, R. et al. Horizontal Transfer of Antimicrobial Resistance Determinants Among Enteric Pathogens Through Bacterial Conjugation. Curr Microbiol 76, 666–672 (2019). https://doi.org/10.1007/s00284-019-01676-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-019-01676-x