Skip to main content

Advertisement

Log in

Chironomid Microbiome

  • Minireviews
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Chironomids are abundant insects in freshwater habitats. They undergo a complete metamorphosis of four life stages: eggs, larvae, and pupae in water, and a terrestrial adult stage. Chironomids are known to be pollution-tolerant, but little is known about their resistance mechanisms to toxic substances. Here we review current knowledge regarding the chironomid microbiome. Chironomids were found as natural reservoirs of Vibrio cholerae and Aeromonas spp. A stable bacterial community was found in the egg masses and the larvae when both culture-dependent and -independent methods were used. A large portion of the endogenous bacterial species was closely related to species known as toxicant degraders. Bioassays based on Koch’s postulates demonstrated that the chironomid microbiome plays a role in protecting its host from toxic hexavalent chromium and lead. V. cholerae, a stable resident in chironomids, is present at low prevalence. It degrades the egg masses by secreting haemagglutinin/protease, prevents eggs from hatching, and exhibits host pathogen interactions with chironomids. However, the nutrients from the degraded egg masses may support the growth of the other microbiome members and consequently control V. cholerae numbers in the egg mass. V. cholerae, other chironomid endogenous bacteria, and their chironomid host exhibit complex mutualistic relationships.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Zchori-Fein E, Bourtzis K (2012) Manipulative tenants: bacteria associated with arthropods. Taylor and Francis Group, LLC, Abingdon

    Google Scholar 

  2. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  3. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735

    Article  CAS  PubMed  Google Scholar 

  4. Rosenberg E, Zilber-Rosenberg I (2011) Symbiosis and development: the hologenome concept. Birth Defects Res C Embryo Today 93:56–66

    Article  CAS  PubMed  Google Scholar 

  5. Rosenberg E, Zilber-Rosenberg I (2013) The hologenome concept: human, animal and plant microbiota. Springer, Berlin Heidelberg

    Book  Google Scholar 

  6. Armitage P, Cranston PS, Pinder LCV (1995) The Chironomidae: the biology and ecology of non-biting midges. Chapman and Hall, London

    Book  Google Scholar 

  7. Broza M, Gancz H, Kashi Y (2008) The association between non-biting midges and Vibrio cholerae. Environ Microbiol 10:3193–3200

    Article  PubMed  Google Scholar 

  8. Ali A (1996) A concise review of chironomid midges (Diptera: Chironomidae) as pests and their management. J Vector Biol 21:105–121

    Google Scholar 

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

    Google Scholar 

  10. Broza M, Halpern M, Gahanma L, Inbar M (2003) Nuisance chironomids in waste stabilization ponds: monitoring and action threshold assessment, based on public complaints. J Vector Ecol 28:31–36

    CAS  PubMed  Google Scholar 

  11. Broza M, Halpern M, Teltsch B, Porat R, Gasit A (1998) Shock chlorination: potential treatment for Chironomidae (Diptera) larvae nuisance abatement in water supply systems. J Econ Entomol 91:834–840

    Article  CAS  PubMed  Google Scholar 

  12. Halpern M, Gasith A, Porat R, Telsch B, Broza M (1999) Chloramine and copper sulfate as control agents of planktonic larvae of Chironomus luridus in water supply systems. J Am Mosq Control Assoc 15:453–457

    CAS  PubMed  Google Scholar 

  13. Halpern M, Gasith A, Broza M (2002) Does the tube of a benthic chironomid larva play a role in protecting its dweller against chemical toxicants? Hydrobiologia 470:49–55

    Article  CAS  Google Scholar 

  14. Coffman WP, Ferrington LC (1984) Chironomidae. In: Merritt RW, Cummins KW (eds) An introduction to the aquatic insects of North America, 2nd edn. Kendall/Hunt, Dubuque, pp 551–652

    Google Scholar 

  15. Pinder LCV (1986) Biology of freshwater chironomidae. Ann Rev Entomol 31:1–23

    Article  Google Scholar 

  16. Salomons W, de Rooij NM, Kerdijk H, Bril J (1987) Sediment as a source for contaminants. Hydrobiologia 149:13–30

    Article  CAS  Google Scholar 

  17. Zieba J (1985) Ecology of some waters in the forest-agricultural basin of River Brynica near the Upper Silesian industrial region: 10. bottom insects with special regard to Chironomidae. Acta Hydrobiol 27:547–560

    Google Scholar 

  18. Thorne RSJ, Williams WP (1997) The response of benthic macroinvertebrates to pollution in developing countries: a multimetric system of bioassessment. Freshwat Biol 37:671–686

    Article  Google Scholar 

  19. Winner RW, Bossel MW, Farrel MP (1980) Insect community structure as an index of heavy-metal pollution in lotic ecosystems. Can J Fish Aquat Sci 37:647–655

    Article  CAS  Google Scholar 

  20. Richardson JS, Kiffney PM (2000) Responses of a macroinvertebrate community from a pristine, southern British Columbia, Canada, stream to metals in experimental mesocosms. Environ Toxicol Chem 19:736–743

    Article  CAS  Google Scholar 

  21. Senderovich Y, Halpern M (2012) Bacterial community composition associated with chironomid egg masses. J Insect Sci 12:149 http://www.insectscience.org/12.149

  22. Senderovich Y, Halpern M (2013) The protective role of endogenous bacterial communities in chironomid egg masses and larvae. ISME J 7:2147–2158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Kaper JB, Morris JG, Levine MM (1995) Cholera. Clin Microbiol Rev 8:48–86

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Colwell RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274:2025–2031

    Article  CAS  PubMed  Google Scholar 

  25. Sack DA, Sack RB, Nair GB, Siddique AK (2004) Cholera. Lancet 363:223–233

    Article  CAS  PubMed  Google Scholar 

  26. Broza M, Halpern M (2001) Chironomid egg masses and Vibrio cholerae. Nature 412:40

    Article  CAS  PubMed  Google Scholar 

  27. Halpern M, Gancz H, Broza B, Kashi Y (2003) Vibrio cholerae Hemagglutinin/Protease degrades chironomid egg masses. Appl Environ Microbiol 69:4200–4204

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Halpern M, Broza Y, Mittler S, Arakawa E, Broza M (2004) Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb Ecol 47:341–349

    Article  CAS  PubMed  Google Scholar 

  29. Halpern M, Raats D, Lavion R, Mittler S (2006) Dependent population dynamics between chironomids (non-biting midges) and Vibrio cholerae. FEMS Microb Ecol 55:98–104

    Article  CAS  Google Scholar 

  30. Halpern M, Landsberg O, Raats D, Rosenberg E (2007) Culturable and VBNC Vibrio cholera: interactions with chironomid egg masses and their bacterial population. Microb Ecol 53:285–298

    Article  CAS  PubMed  Google Scholar 

  31. Senderovich Y, Gershtein Y, Halewa E, Halpern M (2008) Vibrio cholerae and Aeromonas: do they share a mutual host? ISME J 2:276–283

    Article  CAS  PubMed  Google Scholar 

  32. Halpern M (2011) Chironomids and Vibrio cholerae. In: Rosenberg E, Gophna U (eds) Beneficial microorganisms in multicultural life forms. Springer, Berlin Heidelberg, pp 43–56

    Google Scholar 

  33. Raz N, Danin-Poleg Y, Broza YY, Arakawa E, Ramakrishna BS, Broza M, Kashi Y (2010) Environmental monitoring of Vibrio cholerae using chironomids in India. Environ Microbiol Rep 2:96–103

    Article  CAS  PubMed  Google Scholar 

  34. Broza M, Gancz H, Halpern M, Kashi Y (2005) Adult non-biting midges: possible windborne carriers of Vibrio cholerae non-O1 non-O139. Environ Microbiol 7:576–585

    Article  PubMed  Google Scholar 

  35. Ng WL, Bassler BL (2009) Bacterial quorum sensing network architectures. Annu Rev Genet 43:197–222

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Halpern M (2010) Novel insights into Hemagglutinin Protease (HAP) gene regulation in Vibrio cholerae. Mol Ecol 19:4108–4112

    Article  PubMed  Google Scholar 

  37. Joelsson A, Liu Z, Zhu J (2006) Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect Immun 74:1141–1147

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Figueras MJ (2005) Clinical relevance of Aeromonas sM503. Rev Med Microbiol 16:145–153

    Article  Google Scholar 

  39. Farmer JJ, Arduino MJ, Hickman-Brenner FW (2006) The genera Aeromonas and Plesiomonas. In: Rosenberg E, Stackebrandt E, Thompson F, Lory S, DeLong EF (eds) The prokaryotes - a handbook on the biology of bacteria: Vol. 6: Proteobacteria: gamma subclass. Springer, Berlin Heidelberg, pp 564–596

  40. Janda JM, Abbott SL (2010) The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin Microbiol Rev 23:35–73

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Senderovich Y, Ken-Dror S, Vainblat I, Blau D, Izhaki I, Halpern M (2012) A molecular study on the prevalence and virulence potential of Aeromonas spp. recovered from patients suffering from diarrhea in Israel. PLoS One 7:e30070

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Figueras MJ, Beaz-Hidalgo R, Senderovich Y, Laviad S, Halpern M (2011) Re-identification of Aeromonas isolates from chironomid egg masses as the potential pathogenic bacteria Aeromonas aquariorum. Environ Microbiol Rep 3:239–244

    Article  PubMed  Google Scholar 

  43. Beaz-Hidalgo R, Shaked T, Laviad S, Halpern M, Figueras MJ (2012) Chironomid egg masses harbour the clinical species Aeromonas taiwanensis and Aeromonas sanarellii. FEMS Microbiol Lett 337:48–54

    Article  CAS  PubMed  Google Scholar 

  44. Shaked T (2011) Evaluation and assimilation of the Real-Time PCR method for detection of Vibrio cholerae in drinking water and for monitoring V. cholerae and Aeromonas spp. populations in chironomid egg masses. University of Haifa (in Hebrew)

  45. Rouf MA, Rigney MM (1993) Bacterial florae in larvae of the lake fly Chironomus plumosus. Appl Environ Microbiol 59:1236–1241

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Raats D, Halpern M (2007) Oceanobacillus chironomi sp. nov., a halotolerant and facultative alkaliphilic species isolated from a chironomid egg mass. Int J Syst Evol Microbiol 57:255–259

    Article  CAS  PubMed  Google Scholar 

  47. Halpern M, Senderovich Y, Snir S (2007) Rheinheimera chironomi sp. nov., isolated from a chironomid (Diptera; Chironomidae) egg mass. Int J Syst Evol Microbiol 57:1872–1875

    Article  PubMed  Google Scholar 

  48. Halpern M, Shaked T, Pukall R, Schumann P (2009) Leucobacter chironomi sp. nov., a chromate resistant bacterium isolated from a chironomid egg mass. Int J Syst Evol Microbiol 59:665–670

    Article  CAS  PubMed  Google Scholar 

  49. Halpern M, Shaked T, Schumann P (2009) Brachymonas chironomi sp. nov., isolated from a chironomid egg mass, and emended description of the genus Brachymonas. Int J Syst Evol Microbiol 59:3025–3029

    Article  CAS  PubMed  Google Scholar 

  50. Garbisu C, Alkorta I, Carlson DE, Leghton T, Buchanan BB (1997) Selenite bioremediation potential of indigenous microorganisms from industrial activated sludge. Microbiologia 13:437–444

    CAS  PubMed  Google Scholar 

  51. Williams P, Sayers JR (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas. Biodegradation 5:195–217

    Article  CAS  PubMed  Google Scholar 

  52. Cruz A, Caetano T, Suzuki S, Mendo S (2007) Aeromonas veronii, a tributyltin (TBT)-degrading bacterium isolated from an estuarine environment, Ria de Aveiro in Portugal. Mar Environ Res 64:639–650

    Article  CAS  PubMed  Google Scholar 

  53. Lee CM (1994) Effects of immobilized cells on the biodegradation of chlorinated phenols. Water Sci Technol 30:87–90

    CAS  Google Scholar 

  54. Lambo AJ, Patel TR (2007) Biodegradation of polychlorinated biphenyls in Aroclor 1232 and production of metabolites from 2,4,40-trichlorobiphenyl at low temperature by psychrotolerant Hydrogenophaga sp. strain IA3-A. J Appl Microbiol 102:1318–1329

    Article  CAS  PubMed  Google Scholar 

  55. Ohtsubo Y, Goto H, Nagata Y, Kudo T, Tsuda M (2006) Identification of a response regulator gene for catabolite control from a PCB-degrading Betaproteobacteria, Acidovorax sp. KKS102. Mol Microbiol 60:1563–1575

    Article  CAS  PubMed  Google Scholar 

  56. Chakraborty R, O’Connor SM, Chan E, Coates JD (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and xylene ompounds by Dechloromonas strain RCB. Appl Environ Microbiol 71:8649–8655

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Srinath T, Khare S, Ramteke PW (2001) Isolation of hexavalent chromium-reducing Cr-tolerant facultative anaerobes from tannery effluent. J Gen Appl Microbiol 47:307–312

    Article  CAS  PubMed  Google Scholar 

  58. Michel C, Brugna M, Aubert C, Bernadac A, Bruschi M (2001) Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria. Key role of polyheme cytochromes C and hydrogenases. Appl Microbiol Biotechnol 55:95–100

    Article  CAS  PubMed  Google Scholar 

  59. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

  60. Halpern M, Senderovich Y, Izhaki I (2008) Waterfowl — the missing link in epidemic and pandemic cholera dissemination? PLoS Pathog 4:e1000173

    Article  PubMed Central  PubMed  Google Scholar 

  61. Senderovich Y, Izhaki I, Halpern M (2010) Fish as reservoirs and vectors of Vibrio cholerae. PLoS One 5:e8607

    Article  PubMed Central  PubMed  Google Scholar 

  62. Halpern M, Izhaki I (2010) The environmental reservoirs and vector of Vibrio cholerae. In: Holmgren A, Borg G (eds) Handbook of disease outbreaks: prevention, detection and control. Nova, New York, pp 309–320

    Google Scholar 

  63. Koren O, Knezevic V, Ron EZ, Rosenberg E (2003) Petroleum pollution bioremediation using water-insoluble uric acid as the nitrogen source. Appl Environ Microbiol 69:6337–6339

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Okieimen CO, Okieimen FE (2005) Bioremediation of crude oil-polluted soil effect of poultry droppings and natural rubber processing sludge application on biodegrading of petroleum hydrocarbons. J Environ Sci 12:001–008

    CAS  Google Scholar 

  65. Ezenne GI, Nwoke OA, Ezikpe DE, Obalum SE, Ugwuishiwu BO (2012) Use of poultry droppings for remediation of crude-oil-polluted soils: effects of application rate on total and poly-aromatic hydrocarbon concentrations. Int J Biol Chem Sci 6:493–503

    Google Scholar 

  66. Gupta G, Baummer J III (1996) Biodegradation of atrazine in soil using poultry litter. J Hazard Mater 45:185–192

    Article  CAS  Google Scholar 

  67. Adams GO, Tawari-Fufeyin P, Igelenyah E, Odukoya E (2014) Assessment of heavy metals bioremediation potential of microbial consortia from poultry litter and spent oil contaminated site. Int J Environ Bioremed Biodegrad 2:84–92

    Google Scholar 

Download references

Acknowledgments

Our thanks go to Professor Simcha Lev-Yadun for his helpful comments. This study was supported by the Civilian Research & Development Foundation (CRDF) with support from the National Institute of Allergy and Infectious Diseases (NIAID), Grant no. ILB1-7045-HA-11.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Malka Halpern.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Bacterial abundances at the genus level in chironomid egg masses and larvae. The table presents OTUs identified at the genus level in both the egg masses and the larvae. About 40 % and 25 % of all bacterial communities identified to the genus level from the egg mass and the larva, respectively, may potentially have detoxifying abilities. More details can be found in Senderovich and Halpern, 2013 [22]. Boldface indicates that species from these genera were also identified in culture [21, 22, 30, 31, 4548]. (DOCX 18.4 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Halpern, M., Senderovich, Y. Chironomid Microbiome. Microb Ecol 70, 1–8 (2015). https://doi.org/10.1007/s00248-014-0536-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0536-9

Keywords

Navigation