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Bacterial communities associated with the midgut microbiota of wild Anopheles gambiae complex in Burkina Faso

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Abstract

Plasmodium falciparum is transmitted by mosquitoes from the Anopheles gambiae sensu lato (s.l) species complex and is responsible for severe forms of malaria. The composition of the mosquitoes’ microbiota plays a role in P. falciparum transmission, so we studied midgut bacterial communities of An. gambiae s.l from Burkina Faso. DNA was extracted from 17 pools of midgut of mosquitoes from the Anopheles gambiae complex from six localities in three climatic areas, including cotton-growing and cotton-free localities to include potential differences in insecticide selection pressure. The v3–v4 region of the 16S rRNA gene was targeted and sequenced using Illumina Miseq (2 × 250 nt). Diversity analysis was performed using QIIME and R software programs. The major bacterial phylum was Proteobacteria (97.2%) in all samples. The most abundant genera were Enterobacter (32.8%) and Aeromonas (29.8%), followed by Pseudomonas (11.8%), Acinetobacter (5.9%) and Thorsellia (2.2%). No statistical difference in operational taxonomic units (OTUs) was found (Kruskal–Wallis FDR—p > 0.05) among the different areas, fields or localities. Richness and diversity indexes (observed OTUs, Chao1, Simpson and Shannon indexes) showed significant differences in the cotton-growing fields and in the agroclimatic zones, mainly in the Sudano-Sahelian area. OTUs from seven bacterial species that mediate refractoriness to Plasmodium infection in An. gambiae s.l were detected. The beta diversity analysis did not show any significant difference. Therefore, a same control strategy of using bacterial species refractoriness to Plasmodium to target mosquito midgut bacterial community and affect their fitness in malaria transmission may be valuable tool for future malaria control efforts in Burkina Faso.

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files. Fastq reads were submitted and are available in the NCBI (National Center for Biotechnology Information) Sequence Read Archive (SRA) under BioProjectPRJNA558839.

Abbreviations

An. gambiae s.l:

Anopheles gambiae sensu lato

DNA:

Deoxyribonucleic acid

OTUs:

Operational taxonomic units

PCR:

Polymerase chain reaction

References

  1. WHO (2018) World Malaria Report. World Health Organization, Geneva

    Google Scholar 

  2. Karunamoorthi K, Sabesan S (2013) Insecticide resistance in insect vectors of disease with special reference to mosquitoes: a potential threat to global public health. Heal Scope 2:4–18. https://doi.org/10.17795/jhealthscope-9840

    Article  Google Scholar 

  3. Hemingway J, Ranson H, Magill A et al (2016) Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet 387:1785–1788. https://doi.org/10.1016/S0140-6736(15)00417-1

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hemingway J, Shretta R, Wells TNC et al (2016) Tools and strategies for malaria control and elimination: what do we need to achieve a grand convergence in malaria? PLoS Biol 14:e1002380. https://doi.org/10.1371/journal.pbio.1002380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sharma A, Dhayal D, Singh OP et al (2013) Gut microbes influence fitness and malaria transmission potential of Asian malaria vector Anopheles stephensi. Acta Trop 128:41–47. https://doi.org/10.1016/j.actatropica.2013.06.008

    Article  PubMed  Google Scholar 

  6. Tchioffo MT, Boissière A, Churcher TS et al (2013) Modulation of malaria infection in Anopheles gambiae mosquitoes exposed to natural midgut bacteria. PLoS ONE 8:4–12. https://doi.org/10.1371/journal.pone.0081663

    Article  CAS  Google Scholar 

  7. Gendrin M, Rodgers FH, Yerbanga RS et al (2015) Antibiotics in ingested human blood affect the mosquito microbiota and capacity to transmit malaria. Nat Commun 6:1–7. https://doi.org/10.1038/ncomms6921

    Article  Google Scholar 

  8. Gendrin M, Christophides GK (2013) The anopheles mosquito microbiota and their impact on pathogen transmission. Anopheles Mosquitoes. https://doi.org/10.5772/55107

    Article  Google Scholar 

  9. Wang Y, Gilbreath TM 3rd, Kukutla P et al (2011) Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE 6:e24767. https://doi.org/10.1371/journal.pone.0024767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ricci I, Valzano M, Ulissi U et al (2012) Symbiotic control of mosquito borne disease. Pathog Glob Health 106:380–385. https://doi.org/10.1179/2047773212Y.0000000051

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wang S, Jacobs-Lorena M (2013) Genetic approaches to interfere with malaria transmission by vector mosquitoes. Trends Biotechnol 2(31):185–193. https://doi.org/10.1016/j.tibtech.2013.01.001.Genetic

    Article  Google Scholar 

  12. Guerin PJ, Olliaro P, Nosten F, Druilhe P, Laxminarayan R, Fred Binka, Kilama WL, Ford N, White NL (2002) Malaria: current status of control, diagnosis, treatment, and a proposed agenda for research and development. LANCET Infect Dis 2:564–573. https://doi.org/10.1016/S1473-3099(02)00372-9

    Article  PubMed  Google Scholar 

  13. Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025

    Article  CAS  PubMed  Google Scholar 

  14. Favia G, Ricci I, Marzorati M et al (2008) Bacteria of the genus Asaia: a potential paratransgenic weapon against malaria. In: Aksoy S (ed) Transgenesis and the management of vector-borne disease. Springer, New York, pp 49–59

    Chapter  Google Scholar 

  15. Dennison NJ, Jupatanakul N, Dimopoulos G (2014) The mosquito microbiota influences vector competence for human pathogens. Curr Opin Insect Sci 3:6–13. https://doi.org/10.1016/j.cois.2014.07.004

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kim CH, Lampman RL, Muturi EJ (2015) Bacterial communities and midgut microbiota associated with mosquito populations from Waste Tires in East-Central Illinois. J Med Entomol 52:63–75. https://doi.org/10.1093/jme/tju011

    Article  PubMed  Google Scholar 

  17. Gonzalez-Ceron L, Santillan F, Rodriguez MH et al (2003) Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J Med Entomol 40:371–374. https://doi.org/10.1603/0022-2585-40.3.371

    Article  PubMed  Google Scholar 

  18. Habtewold T, Duchateau L, Christophides GK (2016) Flow cytometry analysis of the microbiota associated with the midguts of vector mosquitoes. Parasites Vectors 9:1–10. https://doi.org/10.1186/s13071-016-1438-0

    Article  CAS  Google Scholar 

  19. Chandler JA, Liu RM, Bennett SN (2015) RNA shotgun metagenomic sequencing of Northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front Microbiol 6:1–16. https://doi.org/10.3389/fmicb.2015.00185

    Article  Google Scholar 

  20. Lindh JM, Lindh JM, Terenius O et al (2005) 16S rRNA gene-based identication of midgut bacteria from field-caught. Appl Environ Microbiol 71:7217–7223. https://doi.org/10.1128/AEM.71.11.7217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yadav KK, Bora A, Datta S et al (2015) Molecular characterization of midgut microbiota of Aedes albopictus and Aedes aegypti from Arunachal Pradesh, India. Parasites Vectors 8:1–8. https://doi.org/10.1186/s13071-015-1252-0

    Article  CAS  Google Scholar 

  22. Aguilar R, Dong Y, Warr E, Dimopoulos G (2005) Anopheles infection responses: laboratory models versus field malaria transmission systems. Acta Trop 95:285–291. https://doi.org/10.1016/j.actatropica.2005.06.005

    Article  PubMed  Google Scholar 

  23. Dong Y, Manfredini F, Dimopoulos G (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000423

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cirimotich CM, Dong Y, Garver LS et al (2010) Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 34:387–395. https://doi.org/10.1016/j.dci.2009.12.005

    Article  CAS  PubMed  Google Scholar 

  25. Alavi Y, Arai M, Mendoza J et al (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 33:933–943. https://doi.org/10.1016/S0020-7519(03)00112-7

    Article  CAS  PubMed  Google Scholar 

  26. Hegde S, Rasgon JL, Hughes GL (2015) The microbiome modulates arbovirus transmission in mosquitoes. Curr Opin Virol 15:97–102. https://doi.org/10.1016/j.coviro.2015.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mancini MV, Spaccapelo R, Damiani C et al (2016) Paratransgenesis to control malaria vectors: a semi-field pilot study. Parasites Vectors 9:1–9. https://doi.org/10.1186/s13071-016-1427-3

    Article  CAS  Google Scholar 

  28. Ricci I, Damiani C, Capone A et al (2012) Mosquito/microbiota interactions: from complex relationships to biotechnological perspectives. Curr Opin Microbiol 15:278–284. https://doi.org/10.1016/j.mib.2012.03.004

    Article  PubMed  Google Scholar 

  29. Minard G, Mavingui P, Moro CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites Vectors 6:1. https://doi.org/10.1186/1756-3305-6-146

    Article  Google Scholar 

  30. Kyrou K, Hammond AM, Galizi R et al (2018) OPEN A CRISPR—Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat Biotechnol. https://doi.org/10.1038/nbt.4245

    Article  PubMed  PubMed Central  Google Scholar 

  31. Abiodun GJ, Maharaj R, Witbooi P, Okosun KO (2016) Modelling the influence of temperature and rainfall on the population dynamics of Anopheles arabiensis. Malar J 15:1–15. https://doi.org/10.1186/s12936-016-1411-6

    Article  Google Scholar 

  32. Kabore B, Kam S, Ouedraogo GWP, Bathiebo DJ (2017) Etude de l’évolution climatique au Burkina Faso de 1983 à 2012: cas des villes de Bobo dioulasso, Ouagadougou et Dori. Arab J Earth Sci 4:50–59

    Google Scholar 

  33. Ministère de la Santé du Burkina Faso (2018) Annuaire statistique 2017. Direction, Ouagadougou

    Google Scholar 

  34. Gillies MT, Meillon DB (1968) The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region). South African Institute for Medical Research, Johannesburg

    Google Scholar 

  35. Gillies MT, Coetzee M (1987) A supplement to the Anophelinae of Africa South of the Sahara. Publ South African Inst Med Res 55:63. https://doi.org/10.1046/j.1365-294X.1997.00177.x

    Article  Google Scholar 

  36. Boissiere A, Tchioffo MT, Bachar D et al (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 8:e1002742. https://doi.org/10.1371/journal.ppat.1002742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pruesse E, Quast C, Knittel K et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. https://doi.org/10.1093/nar/gkm864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  40. Mcmurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Foster ZSL, Sharpton TJ, Gru NJ (2017) Metacoder: an R package for visualization and manipulation of community taxonomic diversity data. PLoS Comput Biol 13:e1005404. https://doi.org/10.1371/journal.pcbi.1005404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Cirimotich CM, Dong Y, Clayton AM et al (2011) Natural microbe-mediated refractoriness to plasmodium infection in Anopheles gambiae. Science 332:855–858. https://doi.org/10.1126/science.1201618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ngo CT, Romano-Bertrand S, Manguin S, Jumas-Bilak E (2016) Diversity of the bacterial microbiota of Anopheles mosquitoes from binh Phuoc Province, Vietnam. Front Microbiol 7:1–11. https://doi.org/10.3389/fmicb.2016.02095

    Article  Google Scholar 

  44. Duguma D, Rugman-Jones P, Kaufman MG et al (2013) Bacterial communities associated with Culex mosquito larvae and two emergent aquatic plants of bioremediation importance. PLoS ONE 8:1–11. https://doi.org/10.1371/journal.pone.0072522

    Article  CAS  Google Scholar 

  45. Kampfer P, Lindh M, Terenius O et al (2006) Thorsellia anophelis gen. nov., sp. nov., a new member of the Gammaproteobacteria. Int J Syst Evol Microbiol 56:335–338. https://doi.org/10.1099/ijs.0.63999-0

    Article  CAS  PubMed  Google Scholar 

  46. Briones AM, Shililu J, Githure J et al (2008) Thorsellia anophelis is the dominant bacterium in a Kenyan population of adult Anopheles gambiae mosquitoes. Int Soc Microb Ecol 2:74–82. https://doi.org/10.1038/ismej.2007.95

    Article  CAS  Google Scholar 

  47. Damiani C, Ricci I, Crotti E et al (2010) Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb Ecol 60:644–654. https://doi.org/10.1007/s00248-010-9704-8

    Article  PubMed  Google Scholar 

  48. Straif SC, Mbogo CNM, Toure AM et al (1998) Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: culicidae) from Kenya and Mali. J Med Entomol 35:222–226. https://doi.org/10.1093/jmedent/35.3.222

    Article  CAS  PubMed  Google Scholar 

  49. Tchioffo MT, Boissière A, Abate L et al (2016) Dynamics of bacterial community composition in the malaria mosquito’s epithelia. Front Microbiol 6:1–9. https://doi.org/10.3389/fmicb.2015.01500

    Article  Google Scholar 

  50. Diallo M, Sangaré D, Traoré A et al (2015) Etude de l’impact des gites larvaires sur l’infectivite des gamétocytes de plasmodium falciparum chez Anopheles gambiae sl en zone d’endémie palustre de Nanguilabougou-Mali. Mali Méd 30:28–33

    PubMed  Google Scholar 

  51. Raharimalala FN, Boukraa S, Bawin T et al (2016) Molecular detection of six (endo-) symbiotic bacteria in Belgian mosquitoes: first step towards the selection of appropriate paratransgenesis candidates. Parasitol Res 115:1391–1399. https://doi.org/10.1007/s00436-015-4873-5

    Article  PubMed  Google Scholar 

  52. Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM (2012) Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol 21:5138–5150. https://doi.org/10.1111/j.1365-294X.2012.05759.x

    Article  CAS  PubMed  Google Scholar 

  53. Buck M, Nilsson LKJ, Brunius C et al (2016) Bacterial associations reveal spatial population dynamics in Anopheles gambiae mosquitoes. Sci Rep 6:1–9. https://doi.org/10.1038/srep22806

    Article  CAS  Google Scholar 

  54. Xia X, Zheng D, Zhong H et al (2013) DNA sequencing reveals the midgut microbiota of Diamondback Moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance. PLoS ONE. https://doi.org/10.1371/journal.pone.0068852

    Article  PubMed  PubMed Central  Google Scholar 

  55. Dada N, Sheth M, Liebman K et al (2018) Whole metagenome sequencing reveals links between mosquito microbiota and insecticide resistance in malaria vectors. Sci Rep 8:1–13. https://doi.org/10.1038/s41598-018-20367-4

    Article  CAS  Google Scholar 

  56. Gomgnimbou APK, Savadogo PW, Nianogo AJ, Millogo-rasolodimby J (2009) Usage des intrants chimiques dans un agrosystème tropical: diagnostic du risque de pollution environnementale dans la région cotonnière de l’ est du Burkina Faso. Biotechnol Agron Soc Environ 13:499–507

    Google Scholar 

  57. Badolo A, Traore A, Jones CM et al (2012) Three years of insecticide resistance monitoring in Anopheles gambiae in Burkina Faso: resistance on the rise? Malar. https://doi.org/10.1186/1475-2875-11-232

    Article  Google Scholar 

  58. Toé KH, Jones CM, N’Fale S et al (2014) Increased pyrethroid resistance in malaria vectors and decreased bed net effectiveness, Burkina Faso. Emerg Infect Dis. https://doi.org/10.3201/eid2010.140619

    Article  PubMed  PubMed Central  Google Scholar 

  59. Dabiré RK, Namountougou M, Diabaté A et al (2014) Distribution and frequency of KDR mutations within Anopheles gambiae sl populations and first report of the ace: 1 G119S mutation in Anopheles arabiensis from Burkina Faso (West Africa). PLoS ONE 9:e101484

    Article  PubMed  PubMed Central  Google Scholar 

  60. Dabiré RK, Namountougou M, Sawadogo SP et al (2012) Population dynamics of Anopheles gambiae sl in Bobo-Dioulasso city: bionomics, infection rate and susceptibility to insecticides. Parasites Vectors 5:127

    Article  PubMed  PubMed Central  Google Scholar 

  61. Namountougou M, Simard F, Baldet T et al (2012) Multiple insecticide resistance in Anopheles gambiae s.l. populations from Burkina Faso, West Africa. PLoS ONE 7:e48412. https://doi.org/10.1371/journal.pone.0048412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Capone A, Ricci I, Damiani C et al (2013) Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in Malaria Symbiotic Control. Parasites Vectors 6:1. https://doi.org/10.1186/1756-3305-6-182

    Article  Google Scholar 

  63. Institut National de la Statistique et de la Démographie (INSD), Programme d’Appui au Développement Sanitaire (PADS), Programme National de Lutte contre le Paludisme (PNL), ICF (2018) Enquête sur les indicateurs du Paludisme (EIPBF) 2017–2018. Rockville, Maryland, USA : INSD, PADS, PNLP et ICF

  64. Baldini F, Segata N, Pompon J et al (2014) Evidence of natural Wolbachia infections in field populations of Anopheles gambiae. Nat Commun 5:3985. https://doi.org/10.1038/ncomms4985

    Article  CAS  PubMed  Google Scholar 

  65. Wiwatanaratanabutr I (2013) Geographic distribution of wolbachial infections in mosquitoes from Thailand. J Invertebr Pathol 114:337–340. https://doi.org/10.1016/j.jip.2013.04.011

    Article  PubMed  Google Scholar 

  66. Jeffries CL, Lawrence GG, Golovko G et al (2018) Novel Wolbachia strains in Anopheles malaria vectors from Sub-Saharan Africa. Wellcome Open Res 3:113. https://doi.org/10.12688/wellcomeopenres.14765.1

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by Islamic Development Bank (IDB) Merit Scholarship Program for High Technology. We are sincerely grateful to all the inhabitants of the mosquito collection villages for participating into this study. We also acknowledge the mosquito collectors (Mrs Tientiga Martin, Zouré Abdou Azaque and Somda Zéphirin.) and Mr Dramé Drissa who identified and dissected the mosquitoes, for their valuable contribution to the successful completion of the study.

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AAZ, AB and FF conceived and designed the study. AAZ, ZS, FY and AB supervised the data and samples collection. AAZ and ARS performed practical work, analyzed, interpreted the results and wrote the manuscript. AB, SM and FF revised the manuscript. All authors were the major contributors in writing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Abdou Azaque Zoure.

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This study was approved by the National Health Ethic Committee (CERS) in Burkina Faso (reference number 2017-9-143 of 12 September 2017).

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For mosquito collection in residential areas, written informed and consent was obtained from homeowners in each location.

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Zoure, A.A., Sare, A.R., Yameogo, F. et al. Bacterial communities associated with the midgut microbiota of wild Anopheles gambiae complex in Burkina Faso. Mol Biol Rep 47, 211–224 (2020). https://doi.org/10.1007/s11033-019-05121-x

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