Cargando…

Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India

Cholera toxin (CT)-producing Vibrio cholerae O1 and O139 cause acute diarrheal disease and are proven etiological agents of cholera epidemics and pandemics. On the other hand, V. cholerae non-O1/non-O139 are designated as non-agglutinable (NAG) vibrios and are not associated with epidemic cholera. T...

Descripción completa

Detalles Bibliográficos
Autores principales: Takahashi, Eizo, Ochi, Sadayuki, Mizuno, Tamaki, Morita, Daichi, Morita, Masatomo, Ohnishi, Makoto, Koley, Hemanta, Dutta, Moumita, Chowdhury, Goutam, Mukhopadhyay, Asish K., Dutta, Shanta, Miyoshi, Shin-Ichi, Okamoto, Keinosuke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8417801/
https://www.ncbi.nlm.nih.gov/pubmed/34489915
http://dx.doi.org/10.3389/fmicb.2021.726273
_version_ 1783748455962771456
author Takahashi, Eizo
Ochi, Sadayuki
Mizuno, Tamaki
Morita, Daichi
Morita, Masatomo
Ohnishi, Makoto
Koley, Hemanta
Dutta, Moumita
Chowdhury, Goutam
Mukhopadhyay, Asish K.
Dutta, Shanta
Miyoshi, Shin-Ichi
Okamoto, Keinosuke
author_facet Takahashi, Eizo
Ochi, Sadayuki
Mizuno, Tamaki
Morita, Daichi
Morita, Masatomo
Ohnishi, Makoto
Koley, Hemanta
Dutta, Moumita
Chowdhury, Goutam
Mukhopadhyay, Asish K.
Dutta, Shanta
Miyoshi, Shin-Ichi
Okamoto, Keinosuke
author_sort Takahashi, Eizo
collection PubMed
description Cholera toxin (CT)-producing Vibrio cholerae O1 and O139 cause acute diarrheal disease and are proven etiological agents of cholera epidemics and pandemics. On the other hand, V. cholerae non-O1/non-O139 are designated as non-agglutinable (NAG) vibrios and are not associated with epidemic cholera. The majority of NAG vibrios do not possess the gene for CT (ctx). In this study, we isolated three NAG strains (strains No. 1, 2, and 3) with ctx from pond water in Kolkata, India, and examined their pathogenic properties. The enterotoxicity of the three NAG strains in vivo was examined using the rabbit ileal intestinal loop test. Strain No. 1 induced the accumulation of fluid in the loop, and the volume of fluid was reduced by simultaneous administration of anti-CT antiserum into the loop. The volume of fluid in the loop caused by strains No. 2 and 3 was small and undetectable, respectively. Then, we cultured these three strains in liquid medium in vitro at two temperatures, 25°C and 37°C, and examined the amount of CT accumulated in the culture supernatant. CT was accumulated in the culture supernatant of strain No.1 when the strain was cultured at 25°C, but that was low when cultured at 37°C. The CT amount accumulated in the culture supernatants of the No. 2 and No. 3 strains was extremely low at both temperature under culture conditions examined. In order to clarify the virulence properties of these strains, genome sequences of the three strains were analyzed. The analysis showed that there was no noticeable difference among three isolates both in the genes for virulence factors and regulatory genes of ctx. However, vibrio seventh pandemic island-II (VSP-II) was retained in strain No. 1, but not in strains No. 2 or 3. Furthermore, it was revealed that the genotype of the B subunit of CT in strain No. 1 was type 1 and those of strains No. 2 and 3 were type 8. Histopathological examination showed the disappearance of villi in intestinal tissue exposed to strain No. 1. In addition, fluid accumulated in the loop due to the action of strain No. 1 had hemolytic activity. This indicated that strain No. 1 may possesses virulence factors to induce severe syndrome when the strain infects humans, and that some strains of NAG vibrio inhabiting pond water in Kolkata have already acquired virulence, which can cause illness in humans. There is a possibility that these virulent NAG vibrios, which have acquired genes encoding factors involved in virulence of V. cholerae O1, may emerge in various parts of the world and cause epidemics in the future.
format Online
Article
Text
id pubmed-8417801
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-84178012021-09-05 Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India Takahashi, Eizo Ochi, Sadayuki Mizuno, Tamaki Morita, Daichi Morita, Masatomo Ohnishi, Makoto Koley, Hemanta Dutta, Moumita Chowdhury, Goutam Mukhopadhyay, Asish K. Dutta, Shanta Miyoshi, Shin-Ichi Okamoto, Keinosuke Front Microbiol Microbiology Cholera toxin (CT)-producing Vibrio cholerae O1 and O139 cause acute diarrheal disease and are proven etiological agents of cholera epidemics and pandemics. On the other hand, V. cholerae non-O1/non-O139 are designated as non-agglutinable (NAG) vibrios and are not associated with epidemic cholera. The majority of NAG vibrios do not possess the gene for CT (ctx). In this study, we isolated three NAG strains (strains No. 1, 2, and 3) with ctx from pond water in Kolkata, India, and examined their pathogenic properties. The enterotoxicity of the three NAG strains in vivo was examined using the rabbit ileal intestinal loop test. Strain No. 1 induced the accumulation of fluid in the loop, and the volume of fluid was reduced by simultaneous administration of anti-CT antiserum into the loop. The volume of fluid in the loop caused by strains No. 2 and 3 was small and undetectable, respectively. Then, we cultured these three strains in liquid medium in vitro at two temperatures, 25°C and 37°C, and examined the amount of CT accumulated in the culture supernatant. CT was accumulated in the culture supernatant of strain No.1 when the strain was cultured at 25°C, but that was low when cultured at 37°C. The CT amount accumulated in the culture supernatants of the No. 2 and No. 3 strains was extremely low at both temperature under culture conditions examined. In order to clarify the virulence properties of these strains, genome sequences of the three strains were analyzed. The analysis showed that there was no noticeable difference among three isolates both in the genes for virulence factors and regulatory genes of ctx. However, vibrio seventh pandemic island-II (VSP-II) was retained in strain No. 1, but not in strains No. 2 or 3. Furthermore, it was revealed that the genotype of the B subunit of CT in strain No. 1 was type 1 and those of strains No. 2 and 3 were type 8. Histopathological examination showed the disappearance of villi in intestinal tissue exposed to strain No. 1. In addition, fluid accumulated in the loop due to the action of strain No. 1 had hemolytic activity. This indicated that strain No. 1 may possesses virulence factors to induce severe syndrome when the strain infects humans, and that some strains of NAG vibrio inhabiting pond water in Kolkata have already acquired virulence, which can cause illness in humans. There is a possibility that these virulent NAG vibrios, which have acquired genes encoding factors involved in virulence of V. cholerae O1, may emerge in various parts of the world and cause epidemics in the future. Frontiers Media S.A. 2021-08-20 /pmc/articles/PMC8417801/ /pubmed/34489915 http://dx.doi.org/10.3389/fmicb.2021.726273 Text en Copyright © 2021 Takahashi, Ochi, Mizuno, Morita, Morita, Ohnishi, Koley, Dutta, Chowdhury, Mukhopadhyay, Dutta, Miyoshi and Okamoto. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Takahashi, Eizo
Ochi, Sadayuki
Mizuno, Tamaki
Morita, Daichi
Morita, Masatomo
Ohnishi, Makoto
Koley, Hemanta
Dutta, Moumita
Chowdhury, Goutam
Mukhopadhyay, Asish K.
Dutta, Shanta
Miyoshi, Shin-Ichi
Okamoto, Keinosuke
Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title_full Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title_fullStr Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title_full_unstemmed Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title_short Virulence of Cholera Toxin Gene-Positive Vibrio cholerae Non-O1/non-O139 Strains Isolated From Environmental Water in Kolkata, India
title_sort virulence of cholera toxin gene-positive vibrio cholerae non-o1/non-o139 strains isolated from environmental water in kolkata, india
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8417801/
https://www.ncbi.nlm.nih.gov/pubmed/34489915
http://dx.doi.org/10.3389/fmicb.2021.726273
work_keys_str_mv AT takahashieizo virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT ochisadayuki virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT mizunotamaki virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT moritadaichi virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT moritamasatomo virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT ohnishimakoto virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT koleyhemanta virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT duttamoumita virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT chowdhurygoutam virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT mukhopadhyayasishk virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT duttashanta virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT miyoshishinichi virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia
AT okamotokeinosuke virulenceofcholeratoxingenepositivevibriocholeraenono1nono139strainsisolatedfromenvironmentalwaterinkolkataindia