16S rRNA gene-based identification of elizabethkingia meningoseptica (Flavobacteriales: Flavobacteriaceae) as a dominant midgut bacterium of the asian malaria vector anopheles stephensi (Dipteria: Culicidae) with antimicrobial activities

Journal of Medical Entomology

Volumn 50, Issue 2, 2013, Pages 404-414

  Ngwa, C J ^a   Glockner V ^b   Abdelmohsen, U Ramadan ^b,c   Scheuermayer, M ^a   Fischer, R ^d   Hentschel, U ^b   Pradel, G ^a,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Minia University   (Egypt)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

malaria; midgut microbiota; mosquito; Plasmodium falciparum; transmission

Indexed keywords

RNA 16S;

ANIMAL; ANOPHELES; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; CHRYSEOBACTERIUM; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; DIET; DNA SEQUENCE; ELECTRON MICROSCOPY; FEMALE; GASTROINTESTINAL TRACT; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; ISOLATION AND PURIFICATION; LARVA; MALE; METAGENOME; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; OOCYTE; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION;

ANIMALS; ANOPHELES; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CHRYSEOBACTERIUM; CLONING, MOLECULAR; DENATURING GRADIENT GEL ELECTROPHORESIS; DIET; FEMALE; GASTROINTESTINAL TRACT; GENE LIBRARY; LARVA; MALE; METAGENOME; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; OVUM; PHYLOGENY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PUPA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84874845241     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1603/ME12180     Document Type: Article

References (46)

1. Aminake, M. N., S. Schoof, L. Sologub, M. Leubner, M. Kirschner, H.-D. Arndt, and G. Pradel. 2011. Thiostrepton and derivatives exhibit antimalarial and gametocytocidal activity by dually targeting parasite proteasome and apicoplast. Antimicrob. Agents Chemother. 55: 1338-1348.
2. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71: 7724-7736.
3. Boissière, A., M. T. Tchioffo, D. Bachar, L. Abate, A. Marie, S. E. Nsango, H. R. Shahbazkia, P. H. Awono-Ambene, E. A. Levashina, R. Christen, and I. Morlais. 2012. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 8: E1002742.
4. Chavshin, A. Z., M. A. Oshaghi, H. Vatandoost, M. R. Pourmand, A. Raeisi, A. A. Enayati, N. Mardani, and S. Ghoorchian. 2011. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: A step toward finding suitable paratransgenesis candidates. Acta Trop. 121: 129-134.
5. Cho, M. J., Y. H. Kim, K. Shin, Y. K. Kim, Y. S. Kim, and T. J. Kim. 2010. Symbiotic adaptation of bacteria in the gut of Reticulitermes speratus: Low endo-beta-1,4-glucanase activity. Biochem. Biophys. Res. Commun. 395: 432-435.
6. Coutinho-Abreu, I. V., K. Y. Zhu, and M. Ramalho-Ortigao, 2010. Transgenesis and paratransgenesis to control insect-borne diseases: Current status and future challenges. Parasitol. Int. 59: 1-8.
7. Cranmer, S. L., C. Magowan, J. Liang, R. L. Coppel, and B. M. Cooke. 1997. An alternative to serum for cultivation of Plasmodium falciparum in vitro. Trans. R. Soc. Trop. Med. Hyg. 91: 363-365.
8. Damiani, C., I. Ricci, E. Elena, P. Rossi, A. Rizzi, P. Scuppa, A. Capone, U. Ulissi, S. Epis, M. Genchi, et al. 2010. Mosquito-bacteria symbiosis: The case of Anopheles gambiae and Asaia. Microb. Ecol. 60: 644-654.
9. Dinparast Djadid, N., H. Jazayeri, A. Raz, G. Favia, I. Ricci, and S. Zakeri. 2011. Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PLoS ONE 6: E28484.
10. Dong, Y., and G. Dimopoulos. 2009. Anopheles fibrinogenrelated proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J. Biol. Chem. 284: 9835-9844.
11. Dong, Y., F. Manfredini, and G. Dimopoulos. 2009. Implication of the mosquito microbiota in the defense against malaria parasites. PLoS Pathog. 5: E1000423.
12. Gonzalez-Ceron, L., F. Santillan, M. H. Rodriguez, D. Mendez, and J. E. Hernandez-Avila. 2003. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J. Med. Entomol. 40: 371-374.
13. Hung, P., Y. Lin, C. Lin, M. Liu, and Z. Shi. 2008. Chryseobacterium meningosepticum infection: Antibiotic susceptibility and risk factors for mortality. J. Microbiol. Immunol. Infect. 41: 137-144.
14. Ifediba, T., and J. P. Vanderberg. 1981. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 294: 364-366.
15. Inderlied, C. B., and M. Salfinger. 1995. Antimicrobial agents and susceptibility tests: Mycobacteria, pp. 1385-1404. In P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover, and R. H. Yolken (eds.), Manual of Clinical Microbiology. American Society for Microbiology: Washington, DC.
16. Ka?mpfer, P., H. Matthews, S. P. Glaeser, K. Martin, N. Lodders, and I. Faye. 2011. Elizabethkingia anophelis sp. nov., isolated from the midgut of the mosquito Anopheles gambiae. Int. J. Syst. Evol. Microbiol. 61: 2670-2675.
17. Kariuki, M. M., J. K. Kiaira, F. K. Mulaa, J. K. Mwangi, M. K. Wasunna, and S. K. Martin. 1998. Plasmodium falciparum: Purification of the various gametocyte developmental stages from in vitro-cultivated parasites. Am. J. Trop. Med. Hyg. 59: 505-508.
18. King, E. O. 1959. Studies on a group of previously unclassified bacteria associated with meningitis in infants. Am. J. Clin. Path. 31: 241-247.
19. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65: 418-420.
20. Lane, D. J. 1991. 16S/23S rRNA sequencing, pp. 115-175. In E. Stackebrandt and M. Goodfellow (eds.), Nucleic Acid Techniques in Bacterial Systematics. Wiley, London, United Kingdom.
21. Lin, P., C. Chu, L. Su, C. Huang, W. Chang, and C. Chiu. 2004. Clinical and microbiological analysis of bloodstream infections caused by Chryseobacterium meningosepticum in nonneonatal patients. J. Clin. Microbiol. 42: 3353-3355.
22. Lindh, J. M., O. Terenius, and I. Faye. 2005. 16S rRNA gene-based identification of midgut bacteria from fieldcaught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl. Environ. Microbiol. 71: 7217-7223.
23. Lindh, J. M., A. K. Borg-Karlson, and I. Faye. 2008. Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop. 107: 242-250.
24. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, B. A. Yadhukumar, T. Lai, S. Steppi, G. Jobb, W. Förster, et al. 2004. ARB: A software environment for sequence data. Nucleic Acids Res. 32: 1363-1371.
25. Makler, M. T., and D. J. Hinrichs. 1993. Measurement of the lactate dehydrogenase activity of Plasmodium falciparum as an assessment of parasitemia. Am. J. Trop. Med. Hyg. 48: 205-210.
26. Makler, M. T., J. M. Ries, J. A. Williams, J. E. Bancroft, R. C. Piper, B. L. Gibbins, and D. J. Hinrichs. 1993. Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity. Am. J. Trop. Med. Hyg. 48: 739-741.
27. Meister, S., B. Agianian, F. Turlure, A. Reló gio, I. Morlais, F. C. Kafatos, and G. K. Christophides. 2009. Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog. 5: E1000542.
28. Moll, R. M., W. S. Romoser, M. C. Modrzakowski, A. C. Mon-cayo, and K. Lerdthusnee. 2001. Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J. Med. Entomol. 38: 29-32.
29. Muyzer, G., T Brinkhoff, U. Nübel, C. Santegoeds, H. Scha?fer, and C. Wawer. 1998. Denaturing gradient gel electrophoresis (DGGE) in microbial ecology, pp. 1-27. In A.D.L. Akkermans, J. D. van Elsas, and F. J. De Bruijn (eds.), Molecular Microbial Ecology, Manual 3.4.4. Kluwer, Dordrecht, The Netherland.
30. Osei-Poku, J., C. M. Mbogo, W. J. Palmer, and F. M. Jiggins. 2012. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol. Ecol. 21: 5138-5150.
31. Pradel, G. 2007. Proteins of the malaria parasite sexual stages: Expression, function and potential for transmission blocking strategies. Parasitology 134: 1911-1929.
32. Pruesse, E., J. Peplies, and F. O. Glo?ckner. 2012. SINA: Accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
33. Pumpuni, C. B., M. S. Beier, J. P. Nataro, L. D. Guers, and J. R. Davis. 1993. Plasmodium falciparum: Inhibition of sporogonic development in Anopheles stephensi by gramnegative bacteria. Exp. Parasitol. 77:195-199.
34. Pumpuni, C. B., J. Demaio, M. Kent, J. R. Davis, and J. C. Beier. 1996. Bacterial population dynamics in three anopheline species: The impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg. 54: 214-218.
35. Rani, A., A Sharma, R. Rajagopal, T. Adak, and R. K. Bhatnagar. 2009. Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi: An Asian malarial vector.BMC Microbiol. 9: 96.
36. Riehle, M. A., C. K. Moreira, D. Lampe, C. Lauzon, and M. Jacobs-Lorena. 2007. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int. J. Parasitol. 37: 595-603.
37. Röhrich, C. R., C. J. Ngwa, J. Wiesner, H. Schmidtberg, T. Degenkolb, C. Kollewe, R. Fischer, G. Pradel, and A. Vilcinskas. 2012. Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity. Biol. Lett. 8: 308-311.
38. Schmitt, S., J. B. Weisz, N. Lindquist, and U. Hentschel. 2007. Vertical transmission of a phylogenetically complex yet highly sponge-specific microbial consortium in the viviparous sponge Ircinia felix. Appl. Environ. Microbiol. 73: 2067-2078.
39. Sologub, L., A. Kuehn, S. Kern, J. Przyborski, R. Schillig, and G. Pradel. 2011. Malaria proteases mediate inside-out egress of gametocytes from red blood cells following parasite transmission to the mosquito. Cell Microbiol. 13: 897-912.
40. Steinberg, J. P., and E. M. Burd. 2010. Other gram-negative and gram-variable bacilli, pp. 3015-3033. In G. L. Mandell, J. E. Bennett, and R. Dolin (eds.), Principles and Practice of Infectious Diseases. Churchill Livingstone Elsevier, Philadelphia, PA.
41. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193: 673-675.
42. Vaughan, J. A., B. H. Noden, and J. C. Beier. 1994. Sporogonic development of cultured Plasmodium falciparum in six species of laboratory-reared Anopheles. Am. J. Trop. Med. Hyg. 51: 233-243.
43. Wang, Y., T. M. Gilbreath, 3rd, P. Kukutla, G. Yan, and J. Xu. 2011. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE 6: E24767.
44. Warr, E., S. Das, Y. Dong, and G. Dimopoulos. 2008. The gram-negative bacteria-binding protein gene family: Its role in the innate immune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Mol. Biol. 17: 39-51.
45. WHO) World Health Organization: World Malaria Report. 2011. World Health Organization, Geneva, Switzerland. (http://www.who.int/malaria/world-malaria- report-2011/en/
46. Yoshida, S., D. Ioka, H. Matsuoka, H. Endo, and A. Ishii. 2001. Bacteria expressing single-chain immunotoxin inhibit malaria parasite development in mosquitoes. Mol. Biochem. Parasitol. 113: 89-96.