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 Microbiology

Volumn 9, Issue , 2009, Pages

  Rani, Asha ^a   Sharma, Anil ^a   Rajagopal, Raman ^a   Adak, Tridibesh ^b   Bhatnagar, Raj K ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^b NATIONAL INSTITUTE OF MALARIA RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOSOME RNA; BACTERIAL DNA; RNA 16S;

ACINETOBACTER; ANOPHELES STEPHENSI; ARTICLE; BACILLUS; BACTERIUM; BACTERIUM CULTURE; BACTERIUM DETECTION; COMAMONAS; CRYSEOBACTERIUM MENINQOSEPTICUM; DISEASE CARRIER; ENTEROBACTER; FEMALE; HERBASPIRILLUM; INTESTINE FLORA; KLEBSIELLA; LARVA; MALARIA; MALE; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PAENIBACILLACEAE; PAENIBACILLUS; PHYLOGENY; PSEUDOMONAS MENDOCINA; RHIZOBIUM; SERRATIA MARCESCENS; STAPHYLOCOCCUS HOMINIS; STAPHYLOCOCCUS SAPROPHYTICUS; UNINDEXED SEQUENCE; ANIMAL; ANOPHELES; BACTERIUM IDENTIFICATION; BIODIVERSITY; CLASSIFICATION; DIGESTIVE SYSTEM; DNA SEQUENCE; GENE LIBRARY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; SYMBIOSIS;

ANOPHELES STEPHENSI; BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; HEXAPODA; OTUS; PAENIBACILLACEAE; PLASMODIUM VIVAX; SERRATIA MARCESCENS;

ANIMALS; ANOPHELES; BACTERIA; BACTERIAL TYPING TECHNIQUES; BIODIVERSITY; DIGESTIVE SYSTEM; DNA, BACTERIAL; FEMALE; GENE LIBRARY; INSECT VECTORS; LARVA; MALE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 67650621368     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-9-96     Document Type: Article

References (57)

1. Wolbachia and virus protection in insects. LM Hedges JC Brownlie SL O'Neill KN Johnson, Science 2008 322 702 10.1126/science.1162418 18974344
2. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. CJ McMeniman RV Lane BN Cass AWC Fong M Sidhu YF Wang SL O'Neill, Science 2009 323 141 144 10.1126/science.1165326 19119237
3. Transcriptional analysis of an immune-responsive serine protease from Indian malarial vector, Anopheles culicifacies. J Rodrigues N Agrawal A Sharma P Malhotra T Adak VS Chauhan RK Bhatnagar, BMC Molecular Biol 2007 8 33 10.1186/1471-2199-8-33
4. Plasmodium infection upregulates prophenoloxidase (AcPPO6A) in Anopheles culicifacies. J Rodrigues A Sharma M Kajla N Agrawal T Adak RK Bhatnagar, Innate Immunity 2009 1
5. Genetic manipulation of mosquitoes: an approach to controlling disease. J Carlson, Trends Biotechnol 1996 1 447 448 10.1016/S0167-7799(96)10057-3
6. A novel approach to preventing insect-borne diseases. JE Conte, N Engl J Med 1997 337 785 786 10.1056/NEJM199709113371112 9287238
7. Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. CB Beard C Cordon-Rosales RV Durvasula, Annu Rev Entomol 2002 47 123 141 10.1146/annurev.ento.47.091201.145144 11729071
8. Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. RM Moll WS Romoser MC Modrakowski AC Moncayo K Lerdthusnee, J Med Entomol 2001 38 29 32 11268687 (Pubitemid 33613114)
9. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. CB Pumpuni J DeMaio M Kent JR Davis JC Beier, Am J Trop Med Hyg 1996 54 214 218 8619451 (Pubitemid 26083610)
10. Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. SC Straif CN Mbogo AM Toure ED Walker M Kaufman YT Toure JC Beier, J Med Entomol 1998 35 222 226 9615538 (Pubitemid 128462276)
11. Role of Pseudomonas in the sporogenesis of the hematozoon of malaria in the mosquito. J Jadin IH Vincke A Dunjic JP Delville M Wery J Bafort M Scheepers-Biva, Bull Soc Pathol Exot Filiales 1966 59 514 525 6014213
12. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. L Gonzalez-Ceron F Santillan MH Rodriguez D Mendez JE Hernandez-Avila, J Med Entomol 2003 40 371 374 12943119 (Pubitemid 37399433)
13. Thorsellia anophelis is the dominant bacterium in a Kenyan population of adult Anopheles gambiae mosquitoes. AM Briones J Shililu J Githure R Novak L Ras, The ISME Journal 2008 2 74 82 10.1038/ismej.2007.95 18180748
14. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. G Favia I Ricci C Damiani N Raddadi E Crotti M Marzorati A Rizzi R Urso L Brusetti S Borin D Mora P Scuppa L Pasqualini E Clementi M Genchi S Corona I Negri G Grandi A Alma L Kramer F Esposito C Bandi L Sacchi D Daffonchio, Proc Natl Acad Sci USA 2007 104 9047 9051 17502606 10.1073/pnas.0610451104
15. Concomitant infections of Anopheles stephensi with Plasmodium berghei and Serratia marcescens: additive detrimental effects. HM Seitz WA Maier M Rottok H Becker-Feldmann, Zentralbl Bakteriol Hyg 1987 266 155 166 (Pubitemid 17136115)
16. 16S rRNA Gene-Based Identification of Midgut Bacteria from Field-Caught Anopheles gambiae sensu lato and A. funestus mosquitoes reveals new species related to known insect symbionts. JM Lindh O Terenius I Faye, Appl Environ Microbiol 2005 71 7217 7223 16269761 10.1128/AEM.71.11.7217-7223.2005
17. Global patterns in bacterial diversity. CA Lozupone R Knight, Proc Natl Acad Sci USA 2007 104 11436 11440 17592124 10.1073/pnas.0611525104
18. Ecological diversity and its measurement. AE Magurran, Prinston University Press, Prinston, NJ 1998 9784218
19. Prevention of insect borne diseases: an approach using transgenic symbiotic bacteria. RV Durvasula A Gumbs A Panackal O Kruglov S Aksoy RB Merrifield FF Richards CB Beard, Proc Natl Acad Sci USA 1997 94 3274 3278 9096383 10.1073/pnas.94.7.3274
20. Bacterial symbiosis in arthropods and the control of disease transmission. CB Beard RV Durvasula FF Richards, Emerg Infect Dis 1998 4 581 591 9866734 (Pubitemid 28553682)
21. A novel bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of Flavescence Doree in Vitis vinifera. M Marzorati A Alma L Sacchi M Pajoro S Palermo L Brusetti N Raddadi A Balloi R Tedeschi E Clementi S Corona F Quaglino PA Bianco T Beninati C Bandi D Daffonchio, Appl Environ Microbiol 2006 72 1467 1475 16461701 10.1128/AEM.72.2.1467-1475.2006
22. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. S Zabalou M Riegler M Theodorakopoulou C Stauffer C Savakis K Bourtzis, Proc Natl Acad Sci USA 2004 101 15042 15045 15469918 10.1073/pnas.0403853101
23. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. E Zchori-Fein Y Gottlieb SE Kelly JK Brown JM Wilson TL Karr MS Hunter, Proc Natl Acad Sci USA 2001 98 12555 12560 11592990 10.1073/pnas.221467498
24. Sequence and expression analysis of the ompA gene of Rickettsia peacockii, an endosymbiont of the Rocky Mountain Wood Tick, Dermacentor andersoni. GD Baldridge NY Burkhardt JA Simser TJ Kurtti UG Munderloh, Appl Environ Microbiol 2004 70 6628 6636 15528527 10.1128/AEM.70.11.6628-6636.2004
25. Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. CB Beard EM Dotson PM Pennington S Eichler C Cordon Rosales RV Durvasula, Int J Parasitol 2001 31 621 627 10.1016/S0020-7519(01)00165-5 11334952 (Pubitemid 32382065)
26. Efficient expression of mosquito-larvicidal proteins in a gram-negative bacterium capable of recolonization in the guts of Anopheles dirus larva. P Khampang W Chungjatupornchai P Luxananil S Panyim, Appl Microbiol Biotechnol 1999 51 79 84 10.1007/s002530051366 10077823
27. Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies. MA Riehle M Jacobs-Lorena, Insect Biochem Mol Biol 2005 35 699 707 10.1016/j.ibmb.2005.02.008 15894187
28. The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens and Psorophora columbiae mosquitoes. J DeMaio CB Pumpuni M Kent JC Beier, Am J Trop Med Hyg 1996 54 219 223 8619452 (Pubitemid 26083611)
29. Genome interdependence in insect-bacterium symbioses. EF Zientz J Silva R Gross, Genome Biol 2001 2 1032.1 1032.6 10.1186/gb-2001-2-12-reviews1032
30. Plasmodium falciparum-Inhibition of sporogonic development in Anopheles stephensi by Gram-negative bacteria. CB Pumpuni MS Beier JP Nataro LD Guers JR Davis, Exp Parasitol 1993 77 195 199 10.1006/expr.1993.1076 8375488
31. Counting the uncountable: Statistical approaches to estimating microbial diversity. JB Hughes JJ Hellmann TH Ricketts BJM Bohannan, Appl Environ Microbiol 2001 67 4399 4406 11571135 10.1128/AEM.67.10.4399-4406.2001
32. Using ecological diversity measures with bacterial communities. TCJ Hill KA Walsh JA Harris BF Moffett, FEMS Microbiol Ecol 2003 43 1 11 10.1111/j.1574-6941.2003.tb01040.x (Pubitemid 36173508)
33. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. M Wang S Ahrné B Jeppsson G Molin, FEMS Microbiol Ecol 2005 54 219 231 10.1016/j.femsec.2005.03. 012 16332321
34. Diversity of the human intestinal microbial flora. PB Eckburg EM Bik CN Bernstein E Purdom L Dethlefsen M Sargent SR Gill KE Nelson DA Relman, Science 2005 308 1635 1638 15831718 10.1126/science.1110591
35. Phylogenetic analysis and in situ identification of bacteria in activated sludge. J Snaidr R Amann I Huber W Ludwig KH Schleifer, Appl Environ Microbiol 1997 63 2884 2896 9212435 (Pubitemid 27292891)
36. Analysis of bacterial community composition by oligonucleotide fingerprinting of rRNA genes. L Valinsky G Della Vedova AJ Scupham S Alvey A Figueroa B Yin RJ Hartin M Chrobak DE Crowley T Jiang J Borneman, Appl Environ Microbiol 2002 68 3243 3250 12089000 10.1128/AEM.68.7.3243-3250.2002
37. Assessing microbial diversity by culture-dependent and independent approaches for efficient functioning of effluent treatment plants. A Rani S Porwal R Sharma A Kapley HJ Purohit VC Kalia, Bioresour Technol 2008 99 7098 7107 10.1016/j.biortech.2008.01.003 18280146
38. Hydrogen and polyhydroxybutyrate producing abilities of microbes from diverse habitats by dark fermentative process. S Porwal T Kumar S Lal A Rani S Kumar S Cheema HJ Purohit R Sharma SKS Patel VC Kalia, Bioresour Technol 2008 99 5444 5451 10.1016/j.biortech.2007.11.011 18083024
39. Microorganisms from the midgut of larval and adult Culex quinquefasciatus Say. J Chao GA Wistreich, J Insect Pathol 1960 2 220 224
40. Aeromonas culicicola sp. nov., from the midgut of Culex quinquefasciatus. VJ Pidiyar A Kaznowski N Badri Narayan MS Patole YS Shouche, Int J Syst Evol Microbiol 2002 52 1723 1728 10.1099/ijs.0.02019-0 12361279
41. Effect of paraaminobenzenoic acid, insulin and gentamicin on Plasmodium falciparum development in Anopheline mosquitoes (Diptera: Culicidae). MS Beier CB Pumpuni JC Bizio JR Davis, J Med Entomol 1994 31 561 565 7932602
42. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. G Dimopoulos A Richman HM Muller FC Kafatos, Proc Natl Acad Sci USA 1997 94 11508 11513 9326640 10.1073/pnas.94.21.11508
43. Effect of midgut bacterial flora of Aedes aegypti on the susceptibility of mosquitoes to Dengue viruses. DT Mourya VJ Pidiyar MS Patole MD Gokhale YS Shouche, Dengue Bull 2002 26 190 194 (Pubitemid 37168502)
44. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16S ribosomal RNA gene analysis. VJ Pidiyar K Jangid MS Patole YS Shouche, Am J Trop Med Hyg 2004 70 597 603 15210998 (Pubitemid 38802386)
45. Antimicrobial defense and persistent infection in insects. ER Haine Y Moret MT Siva-Jothy J Rolff, Science 2008 322 1257 1259 10.1126/science.1165265 19023083
46. Indian Anophelines. BN Nagpal VP Sharma, Oxford and IBH publishing Company Pvt Ltd, New Delhi, India 1995 1 409
47. 16S/23S rRNA sequencing. DJ Lane, Nucleic acid techniques in bacterial systematics John Wiley & Sons, Inc., New York, N.Y, Stackebrandt E, Goodfellow M, 1991 115 175
48. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. NA Broderick KF Raffa RM Goodman J Handelsman, Appl Environ Microbiol 2004 70 293 300 14711655 10.1128/AEM.70.1.293-300.2004
49. The RDP (Ribosomal Database Project) continues. BL Maidak JR Cole TG Lilburn CT Parker PR Saxman JM Stredwick GM Garrity B Li GJ Olsen S Pramanik TM Schmidt JM Tiedje, Nucleic Acids Res 2000 28 173 174 10592216 10.1093/nar/28.1.173 (Pubitemid 30047749)
50. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. JR Cole B Chai RJ Farris Q Wang SA Kulam DM McGarrell GM Garrity JM Tiedje, Nucleic Acids Res 2005 33 294 296 10.1093/nar/gki038
51. Bellerophon; a program to detect chimeric sequences in multiple sequence alignments. T Huber G Faulkner P Hugenholtz, Bioinformatics 2004 20 2317 2319 10.1093/bioinformatics/bth226 15073015
52. Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases. P Hugenholtz T Huber, Int J Syst Evol Microbiol 2003 53 289 293 10.1099/ijs.0.02441-0 12656186
53. Clustal W, improving the sensitivity of progressive multiple sequences alignment through sequence weighting, position-specific gap penalties and weight matrix choice. D Thompson DG Higgins TJ Gibson, Nucleic Acids Res 1994 22 4673 4680 7984417 10.1093/nar/22.22.4673 (Pubitemid 24354800)
54. Phylip (Phylogeny Inference Package) version 3.57c. J Felsenstein, Department of Genetics, University of Washington, Seattle. Distribution 1993 http://evolution.genetics.washington.edu/phylip.html
55. TreeView: an application to display phylogenetic trees on personal computer. RDM Page, Comput Appl Biosci 1996 12 357 358 8902363
56. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. PD Schloss J Handelsman, Appl Environ Microbiol 2005 71 1501 1506 15746353 10.1128/AEM.71.3.1501-1506.2005
57. The population frequencies of species and the estimation of population parameters. IJ Good, Biometrica 1953 40 237 264