Annals of Microbiology

, Volume 69, Issue 9, pp 909–922 | Cite as

Analysis of the bacterial communities and endosymbionts of natural populations of Bemisia tabaci in several crop fields from Mexico semi-arid zone

  • Caamal-Chan María Goretty
  • Loera-Muro Abraham
  • Castellanos Thelma
  • Aguilar-Martínez Carlos Julian
  • Marfil-Santana Miguel David
  • Barraza AarónEmail author
Original Article



Bemisia tabaci (Aleyrodidae family) is an insect vector of plant viruses that affects a wide variety of crops around the world. In the following study, we analyzed the variation in the bacterial communities associated with natural populations of B. tabaci (MEAM1) of four different crops from six regions from Mexico semi-arid zone (Baja California Sur).


PCR was used to amplify the mitochondrial cytochrome oxidase I gene (mtCOI), and then to carry out the phylogenetic analysis for genetic identification of the isolated B. tabaci. Next generation sequencing coupled with 16S metagenomic analysis was applied in order to characterize B. tabaci inner microbial community. Finally, bacterial obligate symbiont and facultative symbiont were confirmed by PCR amplification and by phylogenetic analysis.


Ours results pointed toward that B. tabaci MEAM1 inner bacterial communities were predominantly structured by Proteobacteria phylum. Moreover, the most represented endosymbionts were the obligate endosymbiont from the genus “Candidatus Portiera”, as well as two facultative symbionts belonging to genera Rickettsia and Hamiltonella; both obligate and facultative endosymbionts were present for all samples, and their relative abundance varied was crop-independent.


Geographic localization and insect diet play a central role to maintain bacterial community structure of the B. tabaci MEAM1 whitefly at phylum taxonomic level. Agricultural practices were a factor that affected samples of bacterial community structure similarities, reflected in samples clustering. Host plants that are part of B. tabaci diet did not influence directly, in spite of sap nutrient differences, into obligate and facultative endosymbionts relative abundance.


Bemisia tabaci Bacterial communities Endosymbiont Environmental factors 



We thank Jaime Holguín-Peña, Martín Aguilar, Saúl Briceño for technical support for insect samples collections. Angel Carrillo-Garcia and Patricia Hinojosa-Baltazar for technical assistance. Paul Gaytan, Jorge Yañéz, and Eugenio López for primer synthesis and sequencing at Instituto de Biotecnología, Universidad Nacional Autónoma de México. Bruno Gomez-Gil for 16S V3 rDNA sequencing at Laboratorio de Genómica Microbiana, CIAD-Mazatlán, México.


The current investigation was supported by CONACYT/Mexico through the funds provided to CIBNOR.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This research does not involve animals or humans.

Informed consent


Supplementary material

13213_2019_1483_MOESM1_ESM.docx (8.8 mb)
ESM 1 (DOCX 9013 kb)


  1. Azab AK, Megahed MM, E Mirsawi HD (1969) Studies on Bemisia tabaci (Genn.) (Hemiptera Homoptera: Aleyrodidae). Bull Entomol Soc Egypt 53:339–351Google Scholar
  2. Boush MG, Matsumura F (1967) Insecticidal degradation by Pseudomonas melophthora, the bacterial symbiote of the apple maggot. J Econ Entomol 60:918–920. CrossRefGoogle Scholar
  3. Boykin LM, Shatters RG, Rosell RC, McKenzie CL, Bagnall RA, Bagnall RA, De Barro P (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Mol Phylogenet Evol 44:1306–1319. CrossRefPubMedGoogle Scholar
  4. Boykin LM, Bell CD, Evans G, Small I, Barro PJ (2013) Is agriculture driving the diversification of the Bemisia tabaci species complex (Hemiptera:sternorrhyncha:Aleyrodidae)?:dating diversification and biogeographic evidence revealed. BMC Evol Biol 13:228. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66. CrossRefGoogle Scholar
  6. Bushnell B, Rood J, Singer E (2017) BBmerge – accurate paired shotgun read merging via overlap. PLoS One 12(10):e0185056. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Castañeda LE, Barbosa O (2017) Metagenomic analysis exploring taxonomic and functional diversity of soil microbial communities in Chilean vineyards and surrounding native forests. PeerJ 5:e3098. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen W, Hasegawa D, Arumuganathan K, Simmons AM, Wintermantel WM, Fei Z, Ling KS (2015) Estimation of the whitefly Bemisia tabaci genome size based on k-mer and flow cytometric analyses. Insects 6:704–715. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen B, The BS, Sun C, Hu S, Lu X, Boland W, Shao Y (2016) Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci Rep 6:29505. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cheng D, Guo Z, Riegler M, Xi Z, Liang G, Xu Y (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5:13. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL (2017) Horizontal transmission of intracelular insect symbionts via plants. Front Microbiol 8:2237. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chuche J, Auricau-Bouvery N, Jean-Luc D, Thiery D (2017) Use the insiders: could insect facultative symbionts control vector-borne plant diseases? J Pest Sci 90:51–68. CrossRefGoogle Scholar
  13. Chung SH, Scully ED, Peiffer M, Geib S, Rosa C, Hoover K, Felton GW (2017) Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Sci Rep 7:39690. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. CrossRefPubMedGoogle Scholar
  15. De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. CrossRefPubMedGoogle Scholar
  16. Elfekih S, Etter P, Tay WT, Fumagalli M, Gordon K, Johnson E, De Barro P (2018) Genome-wide analyses of the Bemisia tabaci specie complex reveal contrasting patterns of admixture and complex demographic histories. PLoS One 13(1):e0190555. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ewing B, Green P (1998) Base-calling of automated sequences traces using phred II. Genome Res 8:186–194. CrossRefPubMedGoogle Scholar
  18. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred I. accuracy assessment. Genome Res 8:175–185. CrossRefPubMedGoogle Scholar
  19. Gnankiné O, Mouton L, Henri H, Terraz G, Houndeté T, Martin T, Vavre F, Fleury F (2013) Distribution of Bemisia tabaci (Homoptera:Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6:411–421. CrossRefGoogle Scholar
  20. Gressel J (2018) Microbiome facilitated pest resistance potential problem and uses. Pest Manag Sci 74:511–515. CrossRefPubMedGoogle Scholar
  21. Hendry TA, Hunter MS, Baltrus DA (2014) The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Environ Microbiol 80:7161–7168. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jing X, Wong A, Chaston JM, Colvin J, Mckenzie CL, Douglas A (2014) The bacterial communities in plant phloem sap feeding insects. Mol Ecol 23:1433–1444. CrossRefPubMedGoogle Scholar
  23. Kakumanu ML, Reeves AM, Anderson TD, Rodrigues RR, Williams MA (2016) Honey bee gut microbiome is altered by in-hive pesticide exposures. Front Microbiol 7:1255. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kostic AD, Howitt MR, Garrett WS (2013) Exploring host-microbiota interactions in animal models and humans. Genes Dev 27(7):701–718. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li YH, Ahmed MZ, Li SJ, Lv N, Shi PQ, Chen XS, Qiu BL (2017a) Plant mediated horizontal transmission of Rickettsia endosymbiont between different whitefly species. FEMS Microbiol Ecol 93(12).
  29. Li SJ, Ahmed MZ, LV N, Shi PQ, Wang XM, Huang JL, Qiu BL (2017b) Plant mediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–1028. CrossRefPubMedGoogle Scholar
  30. Liu YH, Kang ZW, Guo Y, Zhu GS, Shah MMR, Song Y, Fan YL, Jing X, Liu TX (2016) Nitrogen hurdle of host alternation for a polyphagous aphid and the associated changes of endosymbionts. Sci Rep 6:24781. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mereghetti V, Chouaia B, Montagna M (2017) New insights into the microbiota of moth pests. Int J Mol Sci 18(11):2450. CrossRefPubMedCentralGoogle Scholar
  32. Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilkening J, Edwards RA (2008) The metagenomics RAST server –a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 19(9):386. CrossRefGoogle Scholar
  33. MycKenzie CL, Osborne L (2017) Bemisia tabaci MED (Q biotype) is on the move in Florida to residential landscapes and may impact open field agriculture. Fla Entomol 100:481–485. CrossRefGoogle Scholar
  34. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2014) Vegan: community ecology package. R package version 2.2-0.
  35. Pan H, Li X, Ge D, Wang S, Wu Q, Xie W, Jiao X, Chu D, Liu B, Xu B, Zhang Y (2012) Factors affecting population dynamics of maternally transmitted endosymbionts in Bemisia tabaci. PLoS One 7(2):e30760. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pan H, Su Q, Jiao X, Zhou L, Liu B, Xie W, Wang S, Wu Q, Xu B, Zhang Y (2013) Relative amount of symbionts in Bemisia tabaci (Gennadius) Q changes with host plant and establishing the method of analyzing free amino acid in B. tabaci. Commun Integr Biol 6:e23397. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Randle-Boggis RJ, Helgason T, Sapp M, Ashton PD (2016) Evaluating techniques for metagenome annotation using simulated sequence data. FEMS Microbiol Ecol 92(7):fiw095. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Rosell RC, Lichty JE, Brown JK (1995) Ultrastructure of the mouthparts of adult sweetpotato whitefly, Bemisia tabaci Gennadius (Homoptera:Aleyrodidae). Int J Insect Morphol Embryol 24:297–306CrossRefGoogle Scholar
  39. Schuster DJ, Rajinder SM, Toapanta M, Cordero R, Thompson S, Cyman S, Shurtleff A, Morris RF (2010) Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Manag Sci 66:186–195. CrossRefPubMedGoogle Scholar
  40. Shatters RG, Powell C, Boykin LM, Liansheng H, McKenzie CL (2009) Improved DNA barcoding method for Bemisia tabaci and related Aleyrodidae:development of universal and Bemisia tabaci biotype specific mitochondrial cytochrome c oxidase I polymerase chain reaction primers. J Econ Entomol 102:750–758. CrossRefPubMedGoogle Scholar
  41. Smith HA, Nagle CA, MacVean CA, McKenzie CL (2016) Susceptibility of Bemisia tabaci MEAM1 (Hemiptera:Aleyrodidae) to imidacloprid, thiamethoxam, dinotefuran and flupyradifurone in south Florida. Insects 7(4):57. CrossRefPubMedCentralGoogle Scholar
  42. Su Q, Pan H, Liu B, Chu D, Xie W, Wu Q, Wang S, Xu B, Zhang Y (2013) Insect symbiont facilitates vector acquisition, retention, and transmission of plant virus. Sci Rep 3:1367. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Su Q, Xie W, Wang S, Wu Q, Liu B, Fang Y, Zhang Y (2014) The endosymbiont Hamiltonella increases the growth rate of its host Bemisia tabaci during periods of nutritional stress. PloS one 9(2):e89002.
  44. Su Q, Oliver KM, Xie W, Wu Q, Wang S, Zhang Y (2015) The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct Ecol 29:1007–1018. CrossRefGoogle Scholar
  45. Su MM, Guo L, Tao YL, Zhang YJ, Wan FH, Chu D (2016) Effect of host plant factor on the bacterial communities associated with two whitefly sibling species. PLoS One 11:e0152183. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Upadhyay SK, Sharma S, Singh H, Dixit S, Kumar J, Verma PC, Chandrashekar K (2015) Whitefly genome expression reveals host-symbiont interaction in amino acid biosynthesis. PLoS One 10(5):e0126751. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Vijayakumar MM, More RP, Rangasamy A, Gandhi GR, Muthugounder M, Thiruvengadam V, Samaddar S, Jalali S, Sa T (2018) Gut bacterial diversity of insecticide-susceptible and resistant nymphs of the brown planthopper Nilaparvata lugens stal (Hemiptera:Delphacidae) and the elucidation of their putative functional roles. J Microbiol Biotechnol 28:976–986. CrossRefPubMedGoogle Scholar
  48. Weiss B, Aksoy S (2011) Microbiome influences on insect host vector competence. Trends Parasitol 27(11):514–522. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Werren JH (2012) Symbionts provide pesticide detoxification. Proc Natl Acad Sci U S A 109:8364–8365. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Xia X, Sun B, Gurr GM, Vasseur L, Xue M, You M (2018) Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front Microbiol 9:25. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Zhang YC, Cao WJ, Zhong LR, Godfray HCJ, Liu XD (2016) Host plant determines the population size of an obligate symbiont (Buchenera aphidicola) in aphids. Appl Environ Microbiol 82:2336–2346. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhao Y, Zhang S, Luo JY, Wang CY, Lv LM, Cui JJ (2016) Bacterial communities of the cotton aphid Aphis gossypii associated with BT cotton in northern China. Sci Rep 6:22958. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zhu YX, Song YL, Zhang YK, Hoffmann AA, Zhou JC, Sun JT, Hong XY (2018) Incidence of facultative bacterial endosymbionts in spider mites associated with local environments and host plants. Appl Environ Microbiol 84(6):e02546–e02517. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Università degli studi di Milano 2019

Authors and Affiliations

  1. 1.CONACYT-Centro de Investigaciones Biológicas del Noroeste SCInstituto Politécnico Nacional 195La PazMexico
  2. 2.Centro de Investigaciones Biológicas del Noroeste, SCInstituto Politécnico Nacional 195La PazMexico
  3. 3.Instituto Tecnológico de La PazLa PazMexico
  4. 4.Facultad de Química, Unidad SisalUniversidad Nacional Autónoma de MéxicoSisalMexico

Personalised recommendations