Skip to main content

Advertisement

SpringerLink
Log in

Chironomid Egg Masses as a Natural Reservoir of Vibrio cholerae Non-O1 and Non-O139 in Freshwater Habitats

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Cholera is a diarrheal disease caused by the gram-negative bacterium Vibrio cholerae, and an estimated 120,000 deaths from cholera occur globally every year. The natural reservoir of the bacterium is environmental. A recent report indicated an association between V. cholerae and chironomid egg masses. Chironomids, the “non-biting midges” (Diptera; Chironomidae), are the most widely distributed and frequently the most abundant insects in freshwater. Females attach egg masses, each containing hundreds of eggs encased in a layer of gelatin, to the water’s edge where bacteria are abundant and may encounter the nutrient-rich substrate. Here we report the isolation of non-O1 and non-O139 V. cholerae from chironomid egg masses from different freshwater bodies in Israel, India, and Africa. In a yearly survey in Israel, chironomid populations were found to peak biannually, and it seemed that those peaks were followed by subsequent bacterial growth and disappearance during the winter in the Mediterranean region. The bacterial population rose as water temperature surpassed 25°C. Thirty-five different serogroups of V. cholerae were identified among the bacteria isolated from chironomids, demonstrating population heterogeneity. Two strains of V. cholerae O37 and O201 that were isolated from chironomid egg masses in Zanzibar Island were NAG-ST positive. Our findings support the hypothesis that the association found between chironomids and the cholera bacteria is not a rare coincidence, indicating that chironomid egg masses may serve as yet another potential reservoir for V. cholerae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. InstitutionalAuthorNameAPHA, AWWA, WPCF (1992) Standard methods for the examination of water and wastewater, 18th ed. American Public Health Association Washington, DC

    Google Scholar 

  2. P Armitage PS Cranston LCV Pinder (1995) . P Armitage PS Cranston LCV Pinder (Eds) The Chironomidae: The Biology and Ecology of Non-biting Midges. Chapman and Hall London

    Google Scholar 

  3. M Broza M Halpern M Inbar (2000) ArticleTitleNon-biting midges (Diptera; Chironomidae) in waste stabilization ponds: an intensifying nuisance in Israel. Wat Sci Technol 42 71–74

    Google Scholar 

  4. M Broza M Halpern L Gahanma M Inbar (2003) ArticleTitleNuisance chironomids in waste stabilization ponds: monitoring and action threshold assessment, based on public complaints. J Vector Ecol 28 31–36 Occurrence Handle1:STN:280:DC%2BD3szgtlSjuw%3D%3D Occurrence Handle12831126

    CAS  PubMed  Google Scholar 

  5. M Broza M Halpern (2001) ArticleTitleChironomid egg masses and Vibrio cholerae. Nature 412 40 Occurrence Handle10.1038/35083691 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Crsrc%3D

    Article  CAS  Google Scholar 

  6. K Bagchi P Echeverria JD Arthur O Sethabutr O Serichantalergs CW Hoge (1993) ArticleTitleEpidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J Clin Microbiol 31 1315–1317 Occurrence Handle1:STN:280:ByyB2szpsV0%3D Occurrence Handle8501234

    CAS  PubMed  Google Scholar 

  7. S Chakraborty AK Mukhopadhyay RK Bhadra AN Ghosh R Mitra T Shimada S Yamasaki SM Faruque Y Takeda RR Colwell GB Nair (2000) ArticleTitleVirulence genes in environmental strains of Vibrio cholerae. Appl Environ Microbiol 66 4022–4028 Occurrence Handle10.1128/AEM.66.9.4022-4028.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVajsLY%3D Occurrence Handle10966424

    Article  CAS  PubMed  Google Scholar 

  8. CT Codeco (2001) ArticleTitleEndemic and epidemic dynamics of cholera: the role of the aquatic reservoir. BMC Infect Dis 1 1 Occurrence Handle10.1186/1471-2334-1-1 Occurrence Handle1:STN:280:DC%2BD38votF2htQ%3D%3D Occurrence Handle11208258

    Article  CAS  PubMed  Google Scholar 

  9. RR Colwell (1996) ArticleTitleGlobal climate and infectious disease: the cholera paradigm. Science 274 2025–2031 Occurrence Handle10.1126/science.274.5295.2025 Occurrence Handle1:CAS:528:DyaK2sXivVCm Occurrence Handle8953025

    Article  CAS  PubMed  Google Scholar 

  10. RR Colwell A Huq (1999) ArticleTitleGlobal microbial ecology: biogeography and diversity of Vibrios as a model. J Appl Microbiol Symp Supp 85 134S–137S

    Google Scholar 

  11. RR Colwell A Huq (2001) ArticleTitleMarine ecosystems and cholera. Hydrobiologia 460 141–145 Occurrence Handle10.1023/A:1013111016642

    Article  Google Scholar 

  12. JH Epler (2001) Identification manual for the larval Chironomidae (Diptera) of North and South Carolina. JH Epler (Eds) . North Carolina Department of Environment and Natural Resources Division of Water Quality .

    Google Scholar 

  13. M Halpern H Gancz M Broza Y Kashi (2003) ArticleTitle Vibrio cholerae hemagglutinin/protease degrades chironomid egg masses. Appl Environ Microbiol 69 4200–4204 Occurrence Handle10.1128/AEM.69.7.4200-4204.2003 Occurrence Handle1:CAS:528:DC%2BD3sXlsFagu7g%3D Occurrence Handle12839800

    Article  CAS  PubMed  Google Scholar 

  14. A Huq EB Small PA West R Rahman RR Colwell (1983) ArticleTitleEcology of V. cholerae with special reference to planktonic crustacean copepods. Appl Environ Microbiol 45 275–283 Occurrence Handle1:STN:280:BiyC38rltl0%3D Occurrence Handle6337551

    CAS  PubMed  Google Scholar 

  15. MS Islam BS Drasar RB Sack (1996) Ecology of Vibrio cholerae: role of aquatic flora and fauna. BS Drasar BD Forrest (Eds) Cholera and the Ecology of Vibrio cholerae. Chapman and Hall London 187–227

    Google Scholar 

  16. AM Kamal (1971) ArticleTitleOutbreak of gastro-enteritis by non-agglutinable (NAG) vibrios in the republic of the Sudan. J Egypt Public Health Assoc XLVI 125–159

    Google Scholar 

  17. SM Lewin (1996) Zoological microhabitats of Vibrio cholerae. BS Drasar BD Forrest (Eds) Cholera and the Ecology of Vibrio cholerae. Chapman and Hall London 228–254

    Google Scholar 

  18. M Li T Shimada G Morris Jr A Sulakvelidze S Sozhamannan (2002) ArticleTitleEvidence for the emergence of non-O1 and non-O139 Vibrio cholerae strains with pathogenic potential by exchange of O-antigen biosynthesis regions. Infec Immun 70 2441–2453 Occurrence Handle10.1128/IAI.70.5.2441-2453.2002 Occurrence Handle1:CAS:528:DC%2BD38XjtFKgu78%3D

    Article  CAS  Google Scholar 

  19. AK Mukhopadhyay S Garg R Mitra A Basu K Rajendran D Dutta SK Bhattacharya T Shimada T Takeda Y Takeda GB Nair (1996) ArticleTitleTemporal shifts in traits of Vibrio cholerae strains isolated from hospitalized patients in Calcutta: a 3-year (1993 to 1995) analysis. J Clin Microbiol 34 2537–2543 Occurrence Handle1:CAS:528:DyaK28XmtVSmtL8%3D Occurrence Handle8880516

    CAS  PubMed  Google Scholar 

  20. U Nolte (1993) ArticleTitleEgg masses of Chironomidae (Diptera). A review, including new observations and a preliminary key. Ent Scand Suppl 43 5–75

    Google Scholar 

  21. M Pascual MJ Bouma AP Dobson (2002) ArticleTitleCholera and climate: revisiting the quantitative evidence. review. Microb Infect 4 237–245 Occurrence Handle10.1016/S1286-4579(01)01533-7

    Article  Google Scholar 

  22. IN Rivera J Chun A Huq RB Sack RR Colwell (2001) ArticleTitleGenotypes associated with virulence in environmental isolates of Vibrio cholerae. Appl Environ Microbiol 67 2421–2429 Occurrence Handle10.1128/AEM.67.6.2421-2429.2001 Occurrence Handle1:CAS:528:DC%2BD3MXkt1Cis7Y%3D Occurrence Handle11375146

    Article  CAS  PubMed  Google Scholar 

  23. T Shimada E Arakawa K Itoh T Okitsu A Matsushima Y Asai S Yamai T Nakazato GB Nair MJ Albert Y Takeda (1994) ArticleTitleExtended serotyping scheme for Vibrio cholerae. Curr Microbiol 28 175–178

    Google Scholar 

  24. R Tauxe L Seminario R Tapia M Libel (1994) The Latin America Epidemic. IK Wachsmuth PA Blake . Olsvik (Eds) Vibrio cholerae and Cholera: Molecular to Global Perspective. ASM Press Washington, DC 321–344

    Google Scholar 

  25. WJ De Van Bund D Groenendijk (1994) ArticleTitleSeasonal dynamics and burrowing of littoral chironomid larvae in relation to competition and predation. Arch Hydrobiol 132 213–225

    Google Scholar 

  26. WJ Van De Bund C Davids SJH Spaas (1995) ArticleTitleSeasonal dynamics and spatial distribution of chydorid cladocerans in relation to chironomid larvae in the sandy littoral zone of an oligo-mesotrophic lake. Hydrobiologia 299 125–138

    Google Scholar 

  27. G Wolfram K Donabaum M Schager VA Kowarc (1999) ArticleTitleThe zoobenthic community of shallow salt pans in Austria—preliminary results on phenology and the impact of salinity on benthic invertebrates. Hydrobiologia 408/409 193–202 Occurrence Handle10.1023/A:1017011414599

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Moshe Inbar for his fruitful advice and help in the statistical analysis, Dr. Ariel Kushmaro for his comments on an earlier draft of the manuscript, and Amikam Shoob for photographing Fig. 1a.

Author information

Authors and Affiliations

  1. Faculty of Science and Science Education, University of Haifa, Oranim, Tivon 36006, Israel

    M. Halpern, S. Mittler & M. Broza

  2. Carmel Medical Center, Haifa, Israel

    Y. B. Broza

  3. National Institute of Infectious Diseases, Toyama, 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan

    E. Arakawa

Authors
  1. M. Halpern
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. B. Broza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Mittler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Arakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Broza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Broza.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Halpern, M., Broza, Y., Mittler, S. et al. Chironomid Egg Masses as a Natural Reservoir of Vibrio cholerae Non-O1 and Non-O139 in Freshwater Habitats . Microb Ecol 47, 341–349 (2004). https://doi.org/10.1007/s00248-003-2007-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-2007-6

Keywords

Search

Navigation