Unbiased Characterization of Anopheles Mosquito Blood Meals by Targeted High-Throughput Sequencing

PLoS Neglected Tropical Diseases

Volumn 10, Issue 3, 2016, Pages

  Logue, Kyle ^a,b   Keven, John Bosco ^c,d   Cannon, Matthew V ^a   Reimer, Lisa ^e   Siba, Peter ^d   Walker, Edward D ^c   Zimmerman, Peter A ^b   Serre, David ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Michigan State University   (United States)

^d PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; RIBOSOME DNA;

ANOPHELES; ANOPHELES PUNCTULATUS; ARTICLE; BAT; BLOOD COMPONENT; BLOOD MEAL; COMPUTER MODEL; CONTROLLED STUDY; DNA ISOLATION; DNA POLYMORPHISM; DOBSONIA MOLUCCENSIS; DOBSONIA PRAEDATRIX; DOG; FEMALE; GENE SEQUENCE; HAPLOTYPE; HIGH THROUGHPUT SEQUENCING; HUMAN; MARSUPIAL; MITOCHONDRIAL GENOME; NONHUMAN; PIG; POLYMERASE CHAIN REACTION; SPILOCUSCUS MACULATUS; ANIMAL; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; EVALUATION STUDY; FEEDING BEHAVIOR; GENETICS; MEAL; MOLECULAR GENETICS; PAPUA NEW GUINEA; PHYLOGENY; PHYSIOLOGY; PROCEDURES; ZOOLOGY;

ANIMALS; ANOPHELES; CLUSTER ANALYSIS; DNA, RIBOSOMAL; ENTOMOLOGY; FEEDING BEHAVIOR; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MEALS; MOLECULAR SEQUENCE DATA; PAPUA NEW GUINEA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84962374825     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004512     Document Type: Article

References (58)

1. Lounibos LP, Invasions by insect vectors of human disease. Annual review of entomology. 2002;47:233–66. doi: 10.1146/annurev.ento.47.091201.14520611729075.
2. Gratz NG, Emerging and resurging vector-borne diseases. Annual review of entomology. 1999;44:51–75. doi: 10.1146/annurev.ento.44.1.519990716.
3. Tempelis CH, Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. Journal of medical entomology. 1975;11(6):635–53. 235647.
4. Washino RK, Tempelis CH, Mosquito host bloodmeal identification: methodology and data analysis. Annual review of entomology. 1983;28:179–201. doi: 10.1146/annurev.en.28.010183.0011436131641.
5. Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP, 2ndet al. Bloodmeal identification by direct enzyme-linked immunosorbent assay (ELISA), tested on Anopheles (Diptera: Culicidae) in Kenya. Journal of medical entomology. 1988;25(1):9–16. 3357176.
6. Lardeux F, Loayza P, Bouchite B, Chavez T, Host choice and human blood index of Anopheles pseudopunctipennis in a village of the Andean valleys of Bolivia. Malaria journal. 2007;6:8. doi: 10.1186/1475-2875-6-817241459; PubMed Central PMCID: PMC1783659.
7. Kent RJ, Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Molecular ecology resources. 2009;9(1):4–18. doi: 10.1111/j.1755-0998.2008.02469.x21564560.
8. Kent RJ, Norris DE, Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. The American journal of tropical medicine and hygiene. 2005;73(2):336–42. 16103600; PubMed Central PMCID: PMC4147110.
9. Ngo KA, Kramer LD, Identification of mosquito bloodmeals using polymerase chain reaction (PCR) with order-specific primers. Journal of medical entomology. 2003;40(2):215–22. 12693851.
10. Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, et al. Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. Journal of medical entomology. 2008;45(1):125–8. 18283952.
11. Crabtree MB, Kading RC, Mutebi JP, Lutwama JJ, Miller BR, Identification of host blood from engorged mosquitoes collected in western Uganda using cytochrome oxidase I gene sequences. Journal of wildlife diseases. 2013;49(3):611–26. doi: 10.7589/2012-08-21323778610.
12. Allan BF, Goessling LS, Storch GA, Thach RE, Blood meal analysis to identify reservoir hosts for Amblyomma americanum ticks. Emerging infectious diseases. 2010;16(3):433–40. doi: 10.3201/eid1603.09091120202418; PubMed Central PMCID: PMC3322017.
13. Che Lah EF, Yaakop S, Ahamad M, Md Nor S, Molecular identification of blood meal sources of ticks (Acari, Ixodidae) using cytochrome b gene as a genetic marker. ZooKeys. 2015;(478):27–43. doi: 10.3897/zookeys.478.803725685009; PubMed Central PMCID: PMC4319051.
14. Pichon B, Egan D, Rogers M, Gray J, Detection and identification of pathogens and host DNA in unfed host-seeking Ixodes ricinus L. (Acari: Ixodidae). Journal of medical entomology. 2003;40(5):723–31. 14596289
15. Valinsky L, Ettinger G, Bar-Gal GK, Orshan L, Molecular identification of bloodmeals from sand flies and mosquitoes collected in Israel. Journal of medical entomology. 2014;51(3):678–85. 24897862.
16. Haouas N, Pesson B, Boudabous R, Dedet JP, Babba H, Ravel C, Development of a molecular tool for the identification of Leishmania reservoir hosts by blood meal analysis in the insect vectors. The American journal of tropical medicine and hygiene. 2007;77(6):1054–9. 18165521.
17. Soares VY, Silva JC, Silva KR, Pires e Cruz Mdo S, Santos MP, Ribolla PE, et al. Identification of blood meal sources of Lutzomyia longipalpis using polymerase chain reaction-restriction fragment length polymorphism analysis of the cytochrome B gene. Memorias do Instituto Oswaldo Cruz. 2014;109(3):379–83. 24821056; PubMed Central PMCID: PMC4131795.
18. Steuber S, Abdel-Rady A, Clausen PH, PCR-RFLP analysis: a promising technique for host species identification of blood meals from tsetse flies (Diptera: Glossinidae). Parasitology research. 2005;97(3):247–54. doi: 10.1007/s00436-005-1410-y15999278.
19. Muturi CN, Ouma JO, Malele II, Ngure RM, Rutto JJ, Mithofer KM, et al. Tracking the feeding patterns of tsetse flies (Glossina genus) by analysis of bloodmeals using mitochondrial cytochromes genes. PloS one. 2011;6(2):e17284. doi: 10.1371/journal.pone.001728421386971; PubMed Central PMCID: PMC3046180.
20. Norris LC, Fornadel CM, Hung WC, Pineda FJ, Norris DE, Frequency of multiple blood meals taken in a single gonotrophic cycle by Anopheles arabiensis mosquitoes in Macha, Zambia. The American journal of tropical medicine and hygiene. 2010;83(1):33–7. doi: 10.4269/ajtmh.2010.09–029620595474; PubMed Central PMCID: PMC2912572.
21. Chow-Shaffer E, Sina B, Hawley WA, De Benedictis J, Scott TW, Laboratory and field evaluation of polymerase chain reaction-based forensic DNA profiling for use in identification of human blood meal sources of Aedes aegypti (Diptera: Culicidae). Journal of medical entomology. 2000;37(4):492–502. 10916289.
22. Ansell J, Hamilton KA, Pinder M, Walraven GE, Lindsay SW, Short-range attractiveness of pregnant women to Anopheles gambiae mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2002;96(2):113–6. 12055794.
23. Michael E, Ramaiah KD, Hoti SL, Barker G, Paul MR, Yuvaraj J, et al. Quantifying mosquito biting patterns on humans by DNA fingerprinting of bloodmeals. The American journal of tropical medicine and hygiene. 2001;65(6):722–8. 11791964.
24. Scott TW, Githeko AK, Fleisher A, Harrington LC, Yan G, DNA profiling of human blood in anophelines from lowland and highland sites in western Kenya. The American journal of tropical medicine and hygiene. 2006;75(2):231–7. 16896124.
25. De Benedictis J, Chow-Shaffer E, Costero A, Clark GG, Edman JD, Scott TW, Identification of the people from whom engorged Aedes aegypti took blood meals in Florida, Puerto Rico, using polymerase chain reaction-based DNA profiling. The American journal of tropical medicine and hygiene. 2003;68(4):437–46. 12875293.
26. Replogle J, Lord WD, Budowle B, Meinking TL, Taplin D, Identification of host DNA by amplified fragment length polymorphism analysis: preliminary analysis of human crab louse (Anoplura: Pediculidae) excreta. Journal of medical entomology. 1994;31(5):686–90. 7966171.
27. Mumcuoglu KY, Gallili N, Reshef A, Brauner P, Grant H, Use of human lice in forensic entomology. Journal of medical entomology. 2004;41(4):803–6. 15311479.
28. Beebe NW, Russell T, Burkot TR, Cooper RD, Anopheles punctulatus group: evolution, distribution, and control. Annual review of entomology. 2015;60:335–50. doi: 10.1146/annurev-ento-010814-02120625341094.
29. Beebe NW, Cooper RD, Distribution and evolution of the Anopheles punctulatus group (Diptera: Culicidae) in Australia and Papua New Guinea. International journal for parasitology. 2002;32(5):563–74. 11943229.
30. Charlwood JD, Dagoro H, Paru R, Blood-feeding and resting behaviour in the Anopheles punctulatus Donitz complex (Diptera: Culicidae) from coastal Papua New Guinea. Bulletin of Entomological Research. 1985;75(3):463–76. http://dx.doi.org/10.1017/S0007485300014577.
31. Burkot TR, Graves PM, Paru R, Lagog M, Mixed blood feeding by the malaria vectors in the Anopheles punctulatus complex (Diptera: Culicidae). Journal of medical entomology. 1988;25(4):205–13. 3404539.
32. Burkot TR, Russell TL, Reimer LJ, Bugoro H, Beebe NW, Cooper RD, et al. Barrier screens: a method to sample blood-fed and host-seeking exophilic mosquitoes. Malaria journal. 2013;12:49. doi: 10.1186/1475-2875-12-4923379959; PubMed Central PMCID: PMC3574015.
33. Belkin J, The Mosquitoes of the South Pacfic (Diptera: Culicidae). Berkeley, CA: University of California Press; 1962.
34. Logue K, Small ST, Chan ER, Reimer L, Siba PM, Zimmerman PA, et al. Whole-genome sequencing reveals absence of recent gene flow and separate demographic histories for Anopheles punctulatus mosquitoes in Papua New Guinea. Molecular ecology. 2015;24(6):1263–74. doi: 10.1111/mec.1310725677924.
35. Henry-Halldin CN, Reimer L, Thomsen E, Koimbu G, Zimmerman A, Keven JB, et al. High throughput multiplex assay for species identification of Papua New Guinea malaria vectors: members of the Anopheles punctulatus (Diptera: Culicidae) species group. The American journal of tropical medicine and hygiene. 2011;84(1):166–73. doi: 10.4269/ajtmh.2011.10–043821212222; PubMed Central PMCID: PMC3005508.
36. Taylor PG, Reproducibility of ancient DNA sequences from extinct Pleistocene fauna. Molecular biology and evolution. 1996;13(1):283–5. 8583902.
37. Navia-Gine WG, Loaiza JR, Miller MJ, Mosquito-host interactions during and after an outbreak of equine viral encephalitis in Eastern Panama. PloS one. 2013;8(12):e81788. doi: 10.1371/journal.pone.008178824339965; PubMed Central PMCID: PMC3858258.
38. Paradis E, Claude J, Strimmer K, APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20(2):289–90. 14734327.
39. Epp LS, Boessenkool S, Bellemain EP, Haile J, Esposito A, Riaz T, et al. New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Molecular ecology. 2012;21(8):1821–33. doi: 10.1111/j.1365-294X.2012.05537.x22486821.
40. Duggan AT, Evans B, Friedlaender FR, Friedlaender JS, Koki G, Merriwether DA, et al. Maternal history of Oceania from complete mtDNA genomes: contrasting ancient diversity with recent homogenization due to the Austronesian expansion. American journal of human genetics. 2014;94(5):721–33. doi: 10.1016/j.ajhg.2014.03.01424726474; PubMed Central PMCID: PMC4067553.
41. Katoh K, Standley DM, MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution. 2013;30(4):772–80. doi: 10.1093/molbev/mst01023329690; PubMed Central PMCID: PMC3603318.
42. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic acids research. 2012;40(15):e115. doi: 10.1093/nar/gks59622730293; PubMed Central PMCID: PMC3424584.
43. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD, PANDAseq: paired-end assembler for illumina sequences. BMC bioinformatics. 2012;13:31. doi: 10.1186/1471-2105-13-3122333067; PubMed Central PMCID: PMC3471323.
44. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and environmental microbiology. 2009;75(23):7537–41. doi: 10.1128/AEM.01541-0919801464; PubMed Central PMCID: PMC2786419.
45. Langmead B, Salzberg SL, Fast gapped-read alignment with Bowtie 2. Nature methods. 2012;9(4):357–9. Epub 2012/03/06. doi: 10.1038/nmeth.192322388286; PubMed Central PMCID: PMC3322381.
46. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular biology and evolution. 2013;30(12):2725–9. doi: 10.1093/molbev/mst19724132122; PubMed Central PMCID: PMC3840312.
47. Leister D, Origin, evolution and genetic effects of nuclear insertions of organelle DNA. Trends in genetics: TIG. 2005;21(12):655–63. doi: 10.1016/j.tig.2005.09.00416216380.
48. WHO. Vector-borne diseases Fact sheet March 2014. Available from: http://www.who.int/mediacentre/factsheets/fs387/en/.
49. Graham SP, Hassan HK, Chapman T, White G, Guyer C, Unnasch TR, Serosurveillance of eastern equine encephalitis virus in amphibians and reptiles from Alabama, USA. The American journal of tropical medicine and hygiene. 2012;86(3):540–4. doi: 10.4269/ajtmh.2012.11–028322403333; PubMed Central PMCID: PMC3284378.
50. Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR, Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerging infectious diseases. 2006;12(3):468–74. doi: 10.3201/eid1205.05100416704786; PubMed Central PMCID: PMC3291451.
51. Molaei G, Andreadis TG, Armstrong PM, Bueno R, Jr.Dennett JA, Real SV, et al. Host feeding pattern of Culex quinquefasciatus (Diptera: Culicidae) and its role in transmission of West Nile virus in Harris County, Texas. The American journal of tropical medicine and hygiene. 2007;77(1):73–81. 17620633.
52. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America. 1989;86(16):6196–200. 2762322; PubMed Central PMCID: PMC297804.
53. Koella JC, Sorensen FL, Anderson RA, The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proceedings Biological sciences / The Royal Society. 1998;265(1398):763–8. doi: 10.1098/rspb.1998.03589628035; PubMed Central PMCID: PMC1689045.
54. Darbro JM, Dhondt AA, Vermeylen FM, Harrington LC, Mycoplasma gallisepticum infection in house finches (Carpodacus mexicanus) affects mosquito blood feeding patterns. The American journal of tropical medicine and hygiene. 2007;77(3):488–94. 17827365.
55. Gokool S, Smith DF, Curtis CF, The use of PCR to help quantify the protection provided by impregnated bednets. Parasitology today. 1992;8(10):347–50. 15463534.
56. Gokool S, Curtis CF, Smith DF, Analysis of mosquito bloodmeals by DNA profiling. Medical and veterinary entomology. 1993;7(3):208–15. 8369554.
57. Norris LC, Norris DE, Heterogeneity and changes in inequality of malaria risk after introduction of insecticide-treated bed nets in Macha, Zambia. The American journal of tropical medicine and hygiene. 2013;88(4):710–7. doi: 10.4269/ajtmh.11-059523382169; PubMed Central PMCID: PMC3617857.
58. Soremekun S, Maxwell C, Zuwakuu M, Chen C, Michael E, Curtis C, Measuring the efficacy of insecticide treated bednets: the use of DNA fingerprinting to increase the accuracy of personal protection estimates in Tanzania. Tropical medicine & international health: TM & IH. 2004;9(6):664–72. doi: 10.1111/j.1365-3156.2004.01250.x15189456.