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Chironomids and Vibrio cholerae

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Beneficial Microorganisms in Multicellular Life Forms

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Abstract

Chironomids (non-biting midges) are the most widely dispersed freshwater insects. Females deposit egg masses at the water’s edge, each egg mass contains hundreds of eggs embedded in a gelatinous matrix. They undergo complete metamorphosis of four life stages: eggs, larvae, pupae, and adults. Non O1/O139 serogroups of V. cholerae inhabit all the four life stages of chironomids. haemagglutinin protease (HAP), an extracellular enzyme of V. cholerae, degrades the gelatinous matrix of chironomid egg masses and prevents the eggs from hatching. Chironomid populations and the V. cholerae in their egg masses were found to exhibit host–pathogen population dynamics. Quorum-sensing signals, which are known to commonly establish a successful infection in pathogenic bacteria, repress the cholera toxin expression in V. cholerae and upregulate HAP production. Thus, HAP regulation by quorum sensing should be understood with regard to the bacterial role in chironomids rather than humans. Further research is needed to understand the role of cholera toxin in the environmental existence of V. cholerae. Other endogenous bacterial species that inhabit the egg mass may also use the degraded gelatinous matrix as a nutritive source for their growth. By doing so, they probably control the population levels of V. cholerae in the egg mass. Vice versa, V. cholerae support the maintenance of other endogenic bacteria in the egg mass by secreting HAP. The interaction between V. cholerae and chironomids is probably a complicated mutualistic relationship rather than a simple host–pathogen interaction.

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References

  • Aldova E, Laznickova K, Stepankova E, Lietava J (1968) Isolation of nonagglutinable vibrios from an enteritis outbreak in Czechoslovakia. J Infect Dis 118:25–31

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Benitez JA, Silva AJ, Finkelstein RA (2001) Environmental signals controlling production of hemagglutinin/protease in Vibrio cholerae. Infect Immun 69:6549–6553

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Butler SM, Camilli A (2005) Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3:611–620

    Article  PubMed  CAS  Google Scholar 

  • Chen X, SchauderS PN, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum sensing signal containing boron. Nature 415:545–549

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Colwell RR, Huq A (2001) Marine ecosystems and cholera. Hydrobiologia 460:141–145

    Article  Google Scholar 

  • Constantin de Magny G, Murtugudde R, Sapiano MR, Nizam A, Brown CW, Busalacchi AJ, Yunus M, Nair GB, Gil AI, Lanata CF, Calkins J, Manna B, Rajendran K, Bhattacharya MK, Huq A, Sack RB, Colwell RR (2008) Environmental signatures associated with cholera epidemics. Proc Natl Acad Sci USA 105:17676–17681

    Article  PubMed  CAS  Google Scholar 

  • Faruque SM, Naser IB, Islam MJ, Faruque AS, Ghosh AN, Nair GB, Sack DA, Mekalanos JJ (2005) Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci USA 102:1702–1707

    Article  PubMed  CAS  Google Scholar 

  • Fuqua C, Greenberg EP (2002) Listening on Bacteria: acyl-homoserine lactone signaling. Nat Rev Mol Cell Biol 3:685–695

    Article  PubMed  CAS  Google Scholar 

  • Halpern M (2010) Novel insights into Haemagglutinin Protease (HAP) Gene regulation in Vibrio cholerae. Mol Ecol 19:4108–4112

    Article  Google Scholar 

  • 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, Hauppauge, pp 309–320

    Google Scholar 

  • Halpern M, Gancz H, Broza M, Kashi Y (2003) Vibrio cholerae hemagglutinin/protease degrades chironomid egg masses. Appl Environ Microbiol 69:4200–4204

    Article  PubMed  CAS  Google Scholar 

  • Halpern M, Broza YB, 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Halpern M, Landsberg O, Raats D, Rosenberg E (2007a) Culturable and VBNC Vibrio cholerae; interactions with chironomid egg masses and their bacterial population. Microb Ecol 53:285–293

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Halpern M, Senderovich Y, Izhaki I (2008) Waterfowl – the missing link in epidemic and pandemic cholera dissemination? PLoS Pathog 4:e1000173. doi:10.1371/journal.ppat.1000173

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Halpern M, Shakéd T, Schumann P (2009b) 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  PubMed  CAS  Google Scholar 

  • Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883–886

    Article  PubMed  CAS  Google Scholar 

  • Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR (1983) Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45:275–283

    PubMed  CAS  Google Scholar 

  • Jobling MG, Holmes RK (1997) Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol Microbiol 26:1023–1034

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ko WC, Chuang YC, Huang GC, Hsu SY (1998) Infections due to non-O1 Vibrio cholerae in southern Taiwan: predominance in cirrhotic patients. Clin Infect Dis 7:774–780

    Article  Google Scholar 

  • Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69–82

    Article  PubMed  CAS  Google Scholar 

  • Lewin SM (1996) Zoological microhabitats of Vibrio cholerae. In: Drasar BS, Forrest BD (eds) Cholera and the ecology of Vibrio cholerae. Chapman and Hall, London, pp 228–254

    Chapter  Google Scholar 

  • Lin W, Kovacikova G, Skorupski K (2005) Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. J Bacteriol 187:3013–3019

    Article  PubMed  CAS  Google Scholar 

  • Lipp EK, Huq A, Colwell RR (2002) Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15:757–770

    Article  PubMed  Google Scholar 

  • Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303–314

    Article  PubMed  CAS  Google Scholar 

  • Ng W-L, Bassler BL (2009) Bacterial quorum sensing network architectures. Annu Rev Genet 43:197–222

    Article  PubMed  CAS  Google Scholar 

  • Nolte U (1993) Egg masses of Chironomidae (Diptera). A review, including new observations and a preliminary key. Entomol Scand Suppl 43:5–75

    Google Scholar 

  • Parsek MR (2007) Microbiology: bilingual bacteria. Nature 450:805–807

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Samadi AR, Chowdhury MK, Huq MI, Khan MU (1983) Khan seasonality of classical and El tor cholera in Dhaka, Bangladesh: 17-year trends. Trans R Soc Trop Med Hyg 77:853–856

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Senderovich Y, Izhaki I, Halpern M (2010) Fish as reservoirs and vectors of Vibrio cholerae. PLoS ONE 5:e8607. doi:10.1371/journal.pone.0008607

    Article  PubMed  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Tarsi R, Pruzzo C (1999) Role of surface proteins in Vibrio cholerae attachment to chitin. Appl Environ Microbiol 65:1348–1351

    PubMed  CAS  Google Scholar 

  • Thomas KU, Joseph N, Raveendran O, Nair S (2006) Salinity-induced survival strategy of Vibrio cholerae associated with copepods in Cochin backwaters. Mar Pollut Bull 52:1425–1430

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Xavier KB, Bassler BL (2005) Interference with AI-2-mediated bacterial cell-cell communication. Nature 437:750–753

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 99:3129–3134

    Article  PubMed  CAS  Google Scholar 

  • Ziemke F, Hofle MG, Lalucat J, Rossello-Mora R (1998) Reclassification of Shewanella putrefaciens Owen’s genomic group II as Shewanella baltica sp. nov. Int J Syst Bacteriol 1:179–186

    Article  Google Scholar 

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Acknowledgments

I thank Prof. Simcha Lev-Yadun for his helpful comments on an earlier draft of the manuscript.

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Authors and Affiliations

  1. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa, Oranim, Tivon, 36006, Israel

    Malka Halpern

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  1. Malka Halpern
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Correspondence to Malka Halpern .

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Editors and Affiliations

  1. , Dept. of Molecular Microbiology and Biot, University of Tel Aviv, Ramat Aviv, 69978, Israel

    Eugene Rosenberg

  2. , Dept. of Microbiology and Biotechnology, University of Tel Aviv, Ramat Aviv, 69978, Israel

    Uri Gophna

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Halpern, M. (2012). Chironomids and Vibrio cholerae . In: Rosenberg, E., Gophna, U. (eds) Beneficial Microorganisms in Multicellular Life Forms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21680-0_3

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