Genomic characterization of antibiotic resistance‐encoding genes in clinical isolates of <i>Vibrio cholerae</i> non‐O1/non‐O139 strains from Kolkata, India: generation of novel types of genomic islands containing plural antibiotic resistance genes

Morita, Daichi; Takahashi, Eizo; Morita, Masatomo; Ohnishi, Makoto; Mizuno, Tamaki; Miyoshi, Shin Ichi; Dutta, D; Ramamurthy, Thandavarayan; Chowdhury, Goutam; Mukhopadhyay, Asish K.; Okamoto, Keinosuke

doi:10.1111/1348-0421.12790

Cited by 16 publications

(25 citation statements)

References 36 publications

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“…from North America, although those seem to be devoid of antibiotic resistance genes ( 13 ). IDH‐03944, a cotrimoxazole resistance-conferring GI related to MGI Vch Hai6, was recently reported in a 2011 isolate of V. cholerae O44 recovered from diarrheal patients in Kolkata, India ( 48 ). Comparative genomics revealed a much more diverse set of GIs related to MGI Vch Hai6 in the genome of marine dwelling species and integrated at the 3′ end of trmE and yicC or at the 5′ end of dusA ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…5A ). Only MGI Vch Hai6 and GI Pmi 1, together with IDH‐03944 ( 48 ), contained integrons carrying antibiotic resistance genes, suggesting that these elements are an ancient, large reservoir of antiphage systems, recently hijacked as vectors for drug resistance genes. Most GIs of the MGI Vch Hai6 and MGI Vch Hai6s clades share a gene encoding a predicted RhuM-like virulence factor, usually immediately upstream or downstream of mobI M ( Fig.…”

Section: Discussionmentioning

confidence: 99%

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Antibiotic Resistance in Vibrio cholerae: Mechanistic Insights from IncC Plasmid-Mediated Dissemination of a Novel Family of Genomic Islands Inserted at trmE

Rivard

Colwell

Burrus

2020

mSphere

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Cholera remains a formidable disease, and reports of multidrug-resistant strains of the causative agent Vibrio cholerae have become common during the last 3 decades. The pervasiveness of resistance determinants has largely been ascribed to mobile genetic elements, including SXT/R391 integrative conjugative elements, IncC plasmids, and genomic islands (GIs). Conjugative transfer of IncC plasmids is activated by the master activator AcaCD whose regulatory network extends to chromosomally integrated GIs. MGIVchHai6 is a multidrug resistance GI integrated at the 3′ end of trmE (mnmE or thdF) in chromosome 1 of non-O1/non-O139 V. cholerae clinical isolates from the 2010 Haitian cholera outbreak. In the presence of an IncC plasmid expressing AcaCD, MGIVchHai6 excises from the chromosome and transfers at high frequency. Herein, the mechanism of mobilization of MGIVchHai6 GIs by IncC plasmids was dissected. Our results show that AcaCD drives expression of GI-borne genes, including xis and mobIM, involved in excision and mobilization. A 49-bp fragment upstream of mobIM was found to serve as the minimal origin of transfer (oriT) of MGIVchHai6. The direction of transfer initiated at oriT was determined using IncC plasmid-driven mobilization of chromosomal markers via MGIVchHai6. In addition, IncC plasmid-encoded factors, including the relaxase TraI, were found to be required for GI transfer. Finally, in silico exploration of Gammaproteobacteria genomes identified 47 novel related and potentially AcaCD-responsive GIs in 13 different genera. Despite sharing conserved features, these GIs integrate at trmE, yicC, or dusA and carry a diverse cargo of genes involved in phage resistance. IMPORTANCE The increasing association of the etiological agent of cholera, Vibrio cholerae serogroup O1 and O139, with multiple antibiotic resistance threatens to deprive health practitioners of this effective tool. Drug resistance in cholera results mainly from acquisition of mobile genetic elements. Genomic islands conferring multidrug resistance and mobilizable by IncC conjugative plasmids were reported to circulate in non-O1/non-O139 V. cholerae clinical strains isolated from the 2010 Haitian cholera outbreak. As these genomic islands can be transmitted to pandemic V. cholerae serogroups, their mechanism of transmission needed to be investigated. Our research revealed plasmid- and genomic island-encoded factors required for the resistance island excision, mobilization, and integration, as well as regulation of these functions. The discovery of related genomic islands carrying diverse phage resistance genes but lacking antibiotic resistance-conferring genes in a wide range of marine dwelling bacteria suggests that these elements are ancient and recently acquired drug resistance genes.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Antibiotic Resistance in Vibrio cholerae: Mechanistic Insights from IncC Plasmid-Mediated Dissemination of a Novel Family of Genomic Islands Inserted at trmE

Rivard

Colwell

Burrus

2020

mSphere

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“…In clinical and environmental isolates ARGs which have never been detected in VC previously thereby conferring resistance to antibiotics which worked successfully in its treatment earlier have started appearing, like, the bla NDM-1 carbapenemase encoding gene isolated in environmental and clinical strains of VC (25,26). Above and over that, novel MGEs have started being frequently isolated and the genetic analysis of these novel ARGs (25,26) and MGEs (27,28) and the frequency of their isolation indicate frequent genetic exchange of VC with other bacterial species (29). Some common drugs which have been historically successfully used worldwide against VC are: ampicillin, azithromycin, chloramphenicol, ciprofloxacin, ceftriaxone, doxycycline, erythromycin, gentamycin, neomycin, nalidixic acid, norfloxacin, ofloxacin, streptomycin, cotrimoxazole, tetracycline, meropenam, spiromycin, aztreonem singly or in combination (30).…”

Section: Introductionmentioning

confidence: 99%

“…The microbiome plays a potential role in the dissemination of ARGs and in shaping the genome and hence the AMR profile of pathogens (24,39). Most of the AMR determinants discovered in VC from time to time have been found to originate in taxonomically related and unrelated organisms (23,28,42). The spread of ARGs is facilitated in polymicrobial ecosystems like the gut and environment where the different inhabitants of the ecosystem are exposed to an interactive milieu conducive for genetic exchange of ARGs (24,43).…”

Section: Introductionmentioning

confidence: 99%

Mobile Genetic Elements of Vibrio cholerae and the Evolution of Its Antimicrobial Resistance

2021

Front. Trop. Dis

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Vibrio cholerae (VC) is the causative agent of the severe dehydrating diarrheal disease cholera. The primary treatment for cholera is oral rehydration therapy (ORT). However, in case of moderate to severe dehydration, antibiotics are administered to reduce morbidity. Due to the emergence of multidrug resistant (MDR) strains of VC routinely used antibiotics fail to be effective in cholera patients. Antimicrobial resistance (AMR) is encoded in the genome of bacteria and is usually acquired from other organisms cohabiting in the environment or in the gut with which it interacts in the gut or environmental niche. The antimicrobial resistance genes (ARGs) are usually borne on mobile genetic elements (MGEs) like plasmids, transposons, integrons and SXT constin. Horizontal gene transfer (HGT) helps in the exchange of ARGs among bacteria leading to dissemination of AMR. In VC the acquisition and loss of AMR to many antibiotics have been found to be a dynamic process. This review describes the different AMR determinants and mechanisms of resistance that have been discovered in VC. These ARGs borne usually on MGEs have been recovered from isolates associated with past and present epidemics worldwide. These are responsible for resistance of VC to common antibiotics and are periodically lost and gained contributing to its genetic evolution. These resistance markers can be routinely used for AMR surveillance in VC. The review also presents a precise perspective on the importance of the gut microbiome in the emergence of MDR VC and concludes that the gut microbiome is a potential source of molecular markers and networks which can be manipulated for the interception of AMR in the future.

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“…The concentration of Na + in almost river water in Japan lies between 3.0 and 7.9 mg/L. 6) The concentration of Na + in PAS (under 100% of ionization degree) is 50.6 mg/L. We used the 11 fold-diluted PAS, in which the concentration of Na + is 4.6 mg/L, as the artificial low ionic strength aquatic solution in this experiment.…”

Section: Introductionmentioning

confidence: 99%

Low Viability of Cholera Toxin-Producing <i>Vibrio cholerae</i> O1 in the Artificial Low Ionic Strength Aquatic Solution

Paul¹,

Takahashi

Chowdhury

et al. 2020

Biological & Pharmaceutical Bulletin

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It has been well known that Vibrio cholerae inhabit in environmental water. As many patients infected with cholera toxin-producing V. cholerae O1 (toxigenic V. cholerae O1) emerge in Kolkata, India, it has been thought that toxigenic V. cholerae O1 is easily detected in environmental water in Kolkata. However, we could not isolate toxigenic V. cholerae O1 from environmental water in Kolkata, though NAG Vibrio (generic name of V. cholerae non-O1/non-O139) is constantly detected. To clear the reason for the non-isolation of toxigenic V. cholerae O1, we examined the viability of V. cholera O1 and NAG Vibrios in the artificial low ionic strength aquatic solution. We found that the viability of toxigenic V. cholerae O1 in the solution is low, but that of NAG Vibrios is high. Subsequently, we examined the viability of NAG Vibrios possessing cholera toxin gene (ctx) in the same condition and found that the viability of these NAG Vibrios is low. These results indicate that the existence of ctx in V. cholerae affects the viability of V. cholerae in the aquatic solution used in this experiment. We thought that there was closely relation between the low viability of toxigenic V. cholerae O1 in the artificial low ionic strength aquatic solution and the low frequency of isolation of the strain from environmental water.

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Genomic characterization of antibiotic resistance‐encoding genes in clinical isolates of Vibrio cholerae non‐O1/non‐O139 strains from Kolkata, India: generation of novel types of genomic islands containing plural antibiotic resistance genes

Cited by 16 publications

References 36 publications

Antibiotic Resistance in Vibrio cholerae: Mechanistic Insights from IncC Plasmid-Mediated Dissemination of a Novel Family of Genomic Islands Inserted at trmE

Antibiotic Resistance in Vibrio cholerae: Mechanistic Insights from IncC Plasmid-Mediated Dissemination of a Novel Family of Genomic Islands Inserted at trmE

Mobile Genetic Elements of Vibrio cholerae and the Evolution of Its Antimicrobial Resistance

Low Viability of Cholera Toxin-Producing <i>Vibrio cholerae</i> O1 in the Artificial Low Ionic Strength Aquatic Solution

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