Identification of chironomid species as natural reservoirs of toxigenic vibrio cholerae strains with pandemic potential

Sivan Laviad-Shitrit, Rotem Sela, Leena Thorat, Yehonatan Sharaby, Ido Izhaki, Bimalendu B. Nath, Malka Halpern

Research output: Contribution to journalArticlepeer-review

Abstract

Vibrio cholerae causes the fatal cholera diarrhea. Chironomids (Diptera; Chironomidae) are abundant in freshwater aquatic habitats and estuaries and are natural reservoirs of V. cho-lerae. Until now, only the non-O1/O139 serogroups of V. cholerae were identified in chirono-mids. Here, we explored whether chironomids are natural reservoirs of V. cholerae O1/ O139 serogroups, which are associated with cholera endemics and pandemics. All four life stages of chironomids were sampled from two rivers, and a laboratory culture in Pune, India, and from a pond in Israel. In total, we analyzed 223 chironomid samples. The presence of V. cholerae O1/O139 serogroups was verified using molecular tools. Nine chironomid species were identified; of them, Chironomus circumdatus was the most abundant. The presence of V. cholerae serogroup O1 and the cholera toxin genes were detected in samples from all chironomid species. However, serogroup O139 was detected in only two chironomid spe-cies. Besides PCR to detect specific genes, a metagenomic analysis that was performed in three selected C. ramosus larvae, identified a list of virulence genes associated with V. cho-lerae. The findings provide evidence that chironomids are natural reservoirs of toxigenic V. cholerae O1/O139. Chironomid populations and V. cholerae show biannual peak patterns. A similar pattern is found for cholera epidemics in the Bengal Delta region. Thus, we hypoth-esize that monitoring chironomids in endemic areas of the disease may provide a novel tool for predicting and preventing cholera epidemics. Moreover, serogroup O139 was detected only in two chironomid species that have a restricted distribution in the Indian subcontinent, possibly explaining why the distribution of the O139 serogroup is limited.

Original languageEnglish
Article numbere0008959
Pages (from-to)1-16
Number of pages16
JournalPLoS Neglected Tropical Diseases
Volume14
Issue number12
DOIs
StatePublished - Dec 2020

Bibliographical note

Funding Information:
Funding:ThisworkwassupportedbytheUnited States-IsraelBinationalScienceFoundation,BSF, (grantNo.2015103)(receivedbyMH)andbythe JointUGC-ISF(4thcycle)ResearchGrant(grant No.2728/17)(receivedbyBBNandMH).The fundershadnoroleinstudydesign,datacollection andanalysis,decisiontopublish,orpreparationof themanuscript.

Funding Information:
This work was supported by the United States-Israel Binational Science Foundation, BSF, (grant No. 2015103) (received by MH) and by the Joint UGC-ISF (4th cycle) Research Grant (grant No. 2728/17) (received by BBN and MH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2020 Laviad-Shitrit et al.

ASJC Scopus subject areas

  • Public Health, Environmental and Occupational Health
  • Infectious Diseases

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