Microbiome profiling of the onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae)


Autoři: Suresh J. Gawande aff001;  Sivalingam Anandhan aff001;  Ashish Ingle aff001;  Praveen Roylawar aff001;  Kiran Khandagale aff001;  Tushar Gawai aff001;  Alana Jacobson aff002;  Ramasamy Asokan aff003;  Major Singh aff001
Působiště autorů: ICAR-Directorate of Onion and Garlic Research, Rajgurunagar, Pune, India aff001;  Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama, United States of America aff002;  ICAR-Indian Institute of Horticultural Research, Hessarghatta Lake, Bengaluru, India aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223281

Souhrn

The gut microbial community structure of adult Thrips tabaci collected from 10 different agro-climatically diverse locations of India was characterized by using the Illumina MiSeq platform to amplify the V3 region of the 16S rRNA gene of bacteria present in the sampled insects. Analyses were performed to study the bacterial communities associated with Thrips tabaci in India. The complete bacterial metagenome of T. tabaci was comprised of 1662 OTUs of which 62.25% belong to known and 37.7% of unidentified/unknown bacteria. These OTUs constituted 21 bacterial phyla of 276 identified genera. Phylum Proteobacteria was predominant, followed by Actinobacteria, Firmicutes, Bacteroidetes and Cyanobacteria. Additionally, the occurrence of the reproductive endosymbiont, Wolbachia was detected at two locations (0.56%) of the total known OTUs. There is high variation in diversity and species richness among the different locations. Alpha-diversity metrics indicated the higher gut bacterial diversity at Bangalore and lowest at Rahuri whereas higher bacterial species richness at T. tabaci samples from Imphal and lowest at Jhalawar. Beta diversity analyses comparing bacterial communities between the samples showed distinct differences in bacterial community composition of T. tabaci samples from different locations. This paper also constitutes the first record of detailed bacterial communities associated with T. tabaci. The location-wise variation in microbial metagenome profile of T. tabaci suggests that bacterial diversity might be governed by its population genetic structure, environment and habitat.

Klíčová slova:

Actinobacteria – Bacteria – India – Microbiome – Ribosomal RNA – Sequence databases – Species diversity – Wolbachia


Zdroje

1. Duron O, Hurst GD. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. Bmc Biology. 2013 Dec;11(1):45.

2. Hansen AK, Moran NA. Aphid genome expression reveals host–symbiont cooperation in the production of amino acids. Proceedings of the National Academy of Sciences. 2011 Feb 15;108(7):2849–54.

3. Douglas AE. The ecology of symbiotic micro-organisms. In Advances in Ecological Research 1995 Jan 1 (Vol. 26, pp. 69–103). Academic Press.

4. Dillon RJ, Vennard CT, Charnley AK. Pheromones: exploitation of gut bacteria in the locust. Nature. 2000 Feb;403(6772):851.

5. Houk EA, Griffiths GW. Intracellular symbiotes of the Homoptera. Annual review of entomology. 1980 Jan;25(1):161–87.

6. Lee FJ, Miller KI, McKinlay JB, Newton IL. Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS microbiology ecology. 2018 Jun 6;94(8):fiy113.

7. Vorburger C. Symbiont-conferred resistance to parasitoids in aphids–challenges for biological control. Biological Control. 2018 Jan 1;116:17–26.

8. Su Q, Pan H, Liu B, Chu D, Xie W, Wu Q, Wang S, Xu B, Zhang Y. Insect symbiont facilitates vector acquisition, retention, and transmission of plant virus. Scientific Reports. 2013 Mar 4;3:1367.

9. Xia X, Sun B, Gurr GM, Vasseur L, Xue M, You M. Gut microbiota mediate insecticide resistance in the Diamondback moth, Plutella xylostella (L.). Frontiers in microbiology. 2018 Jan 23;9:25. doi: 10.3389/fmicb.2018.00025 29410659

10. Itoh H, Tago K, Hayatsu M, Kikuchi Y. Detoxifying symbiosis: microbe-mediated detoxification of phytotoxins and pesticides in insects. Natural product reports. 2018;35(5):434–54. doi: 10.1039/c7np00051k 29644346

11. Breeuwer JA. Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity. 1997 Jul;79(1):41.

12. Vala F, Weeks A, Claessen D, Breeuwer JA, Sabelis MW. Within‐and between‐population variation for Wolbachia‐induced reproductive incompatibility in a haplodiploid mite. Evolution. 2002 Jul;56(7):1331–9. doi: 10.1111/j.0014-3820.2002.tb01447.x 12206235

13. Cao Y., Fanning S., Proos S., Jordan K. & Srikumar S. A Review on the Applications of Next Generation Sequencing Technologies as Applied to Food-Related Microbiome Studies. Front. Microbiol. 8, 1829; doi: 10.3389/fmicb.2017.01829 29033905

14. Zhao Y, Zhang S, Luo JY, Wang CY, Lv LM, Cui JJ. Bacterial communities of the cotton aphid Aphis gossypii associated with Bt cotton in northern China. Scientific reports. 2016 Apr 15;6:22958. doi: 10.1038/srep22958 27079679

15. Lv ZH, Wei XY, Tao YL, Chu D. Differential susceptibility of whitefly-associated bacteria to antibiotic as revealed by metagenomics analysis. Infection, Genetics and Evolution. 2018 Sep 1;63:24–9. doi: 10.1016/j.meegid.2018.04.024 29702243

16. Dickey AM, Trease AJ, Jara-Cavieres A, Kumar V, Christenson MK, Potluri LP, Morgan JK, Shatters RG Jr, Mckenzie CL, Davis PH, Osborne LS. Estimating bacterial diversity in Scirtothrips dorsalis (Thysanoptera: Thripidae) via next generation sequencing. The Florida entomologist. 2014 Jun;97(2):362. 25382863

17. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. science. 2011 Apr 8;332(6026):254–6. doi: 10.1126/science.1199410 21474763

18. Ferrari J, Scarborough CL, Godfray HC. Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia. 2007 Aug 1;153(2):323–9. doi: 10.1007/s00442-007-0730-2 17415589

19. Douglas AE. Symbiotic microorganisms: untapped resources for insect pest control. TRENDS in Biotechnology. 2007 Aug 1;25(8):338–42. doi: 10.1016/j.tibtech.2007.06.003 17576018

20. Lewis T. Thrips as crop pests. Cab International; 1997.

21. Diaz-Montano J, Fuchs M, Nault BA, Fail J, Shelton AM. Onion thrips (Thysanoptera: Thripidae): a global pest of increasing concern in onion. Journal of Economic Entomology. 2011 Feb 1;104(1):1–3. doi: 10.1603/ec10269 21404832

22. Gent DH, du Toit LJ, Fichtner SF, Mohan SK, Pappu HR, Schwartz HF. Iris yellow spot virus: an emerging threat to onion bulb and seed production. Plant Disease. 2006 Dec;90(12):1468–80. doi: 10.1094/PD-90-1468 30780964

23. Rotenberg D, Jacobson AL, Schneweis DJ, Whitfield AE. Thrips transmission of tospoviruses. Current Opinion in Virology. 2015 Dec 1;15:80–9. doi: 10.1016/j.coviro.2015.08.003 26340723

24. Riley DG, Joseph SV, Srinivasan R, Diffie S. Thrips vectors of tospoviruses. Journal of Integrated Pest Management. 2011 Apr 1;2(1):I1–0.

25. Nault BA, Shelton AM, Gangloff-Kaufmann JL, Clark ME, Werren JL, Cabrera-la Rosa JC, Kennedy GG. Reproductive modes in onion thrips (Thysanoptera: Thripidae) populations from New York onion fields. Environmental Entomology. 2006 Oct 1;35(5):1264–71.

26. Jacobson AL, Kennedy GG. Specific insect-virus interactions are responsible for variation in competency of different Thrips tabaci isolines to transmit different Tomato spotted wilt virus isolates. PLoS One. 2013 Jan 24;8(1):e54567. doi: 10.1371/journal.pone.0054567 23358707

27. Gawande SJ, Anandhan S, Ingle AA, Jacobson A, Asokan R. Heteroplasmy due to coexistence of mtCOI haplotypes from different lineages of the Thrips tabaci cryptic species group. Bulletin of entomological research. 2017 Aug;107(4):534–42. doi: 10.1017/S0007485317000025 28137324

28. Koivisto RK, Braig HR. Microorganisms and parthenogenesis. Biological Journal of the Linnean Society. 2003 May 1;79(1):43–58.

29. Kumm S, Moritz G. First detection of Wolbachia in arrhenotokous populations of thrips species (Thysanoptera: Thripidae and Phlaeothripidae) and its role in reproduction. Environmental Entomology. 2008 Dec 1;37(6):1422–8. doi: 10.1603/0046-225x-37.6.1422 19161685

30. De Vries EJ, Van der Wurff AW, Jacobs G, Breeuwer JA. Onion thrips, Thrips tabaci, have gut bacteria that are closely related to the symbionts of the western flower thrips, Frankliniella occidentalis. Journal of Insect Science. 2008 Jan 1;8(1):23.

31. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. Cold spring harbor laboratory press; 1989.

32. Bolyen E, Jai Ram R, Matthew RD, Nicholas AB, Christian CA, Gabriel A, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. (2019): 1.

33. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA., Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nature methods. 2016 Jul;13(7):581. doi: 10.1038/nmeth.3869 27214047

34. Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018 Dec;6(1):90. doi: 10.1186/s40168-018-0470-z 29773078

35. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013 Jan 16;30(4):772–80. doi: 10.1093/molbev/mst010 23329690

36. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PloS one. 2010 Mar 10;5(3):e9490. doi: 10.1371/journal.pone.0009490 20224823

37. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 2005 Dec 1;71(12):8228–35. doi: 10.1128/AEM.71.12.8228-8235.2005 16332807

38. Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience. 2013 Dec;2(1):16. doi: 10.1186/2047-217X-2-16 24280061

39. Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R, Peddada SD. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microbial ecology in health and disease. 2015 Dec 1;26(1):27663.

40. Engel P, Moran NA. The gut microbiota of insects–diversity in structure and function. FEMS microbiology reviews. 2013 Sep 1;37(5):699–735. doi: 10.1111/1574-6976.12025 23692388

41. Powell CM, Montiel AL, Beddingfield B, Hanson JD, Bextine BR. Comparison of Bacterial Communities of Flower Thrips (Frankliniella tritici 1) and Potato Psyllid (Bactericera cockerelli 2). Southwestern Entomologist. 2015 Dec;40(4):765–74.

42. Kaczmarczyk A, Kucharczyk H, Kucharczyk M, Kapusta P, Sell J, Zielińska S. First insight into microbiome profile of fungivorous thrips Hoplothrips carpathicus (Insecta: Thysanoptera) at different developmental stages: molecular evidence of Wolbachia endosymbiosis. Scientific reports. 2018 Sep 26;8(1):14376 doi: 10.1038/s41598-018-32747-x 30258200

43. Jones RT, Sanchez LG, Fierer N. A cross-taxon analysis of insect-associated bacterial diversity. PLoS one. 2013 Apr 16;8(4):e61218. doi: 10.1371/journal.pone.0061218 23613815

44. Yun JH, Roh SW, Whon TW, Jung MJ, Kim MS, Park DS, Yoon C, Nam YD, Kim YJ, Choi JH, Kim JY. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl. Environ. Microbiol. 2014 Sep 1;80(17):5254–64. doi: 10.1128/AEM.01226-14 24928884

45. Kim JM, Choi MY, Kim JW, Lee SA, Ahn JH, Song J, Kim SH, Weon HY. Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera). Journal of Microbiology. 2017 Jan 1;55(1):21–30.

46. McKenzie VJ, Bowers RM, Fierer N, Knight R, Lauber CL. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. The ISME journal. 2012 Mar;6(3):588. doi: 10.1038/ismej.2011.129 21955991

47. Delalibera I Jr, Handelsman JO, Raffa KF. Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Environmental Entomology. 2005 Jun 1;34(3):541–7.

48. McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proceedings of the National Academy of Sciences. 2007 Dec 4;104(49):19392–7.

49. Cheng D, Guo Z, Riegler M, Xi Z, Liang G, Xu Y. Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome. 2017 Dec;5(1):13. doi: 10.1186/s40168-017-0236-z 28143582

50. Pasti MB, Belli ML. Cellulolytic activity of actinomycetes isolated from termites (Termitidae) gut. FEMS microbiology letters. 1985 Jan 1;26(1):107–12.

51. Schäfer A, Konrad R, Kuhnigk T, Kämpfer P, Hertel H, König H. Hemicellulose‐degrading bacteria and yeasts from the termite gut. Journal of Applied Bacteriology. 1996 May;80(5):471–8. doi: 10.1111/j.1365-2672.1996.tb03245.x 9072518

52. Kaltenpoth M. Actinobacteria as mutualists: general healthcare for insects?. Trends in microbiology. 2009 Dec 1;17(12):529–35. doi: 10.1016/j.tim.2009.09.006 19853457

53. Auer L, Lazuka A, Sillam-Dussès D, Miambi E, O'Donohue M, Hernandez-Raquet G. Uncovering the potential of termite gut microbiome for lignocellulose bioconversion in anaerobic batch bioreactors. Frontiers in microbiology. 2017 Dec 22;8:2623. doi: 10.3389/fmicb.2017.02623 29312279

54. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology. 2011 Feb;20(3):619–28. doi: 10.1111/j.1365-294X.2010.04959.x 21175905

55. Chen B, Teh BS, Sun C, Hu S, Lu X, Boland W, Shao Y. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Scientific reports. 2016 Jul 8;6:29505. doi: 10.1038/srep29505 27389097

56. Brown SD, Lamed R, Morag E, Borovok I, Shoham Y, Klingeman DM, Johnson CM, Yang Z, Land ML, Utturkar SM, Keller M. Draft genome sequences for Clostridium thermocellum wild-type strain YS and derived cellulose adhesion-defective mutant strain AD2. 2012: 3290–3291 doi: 10.1128/JB.00473-12 22628515

57. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Reviews Microbiology. 2008 Feb;6(2):121. doi: 10.1038/nrmicro1817 18180751

58. Dai X, Zhu Y, Luo Y, Song L, Liu D, Liu L, Chen F, Wang M, Li J, Zeng X, Dong Z. Metagenomic insights into the fibrolytic microbiome in yak rumen. PloS one. 2012 Jul 13;7(7):e40430. doi: 10.1371/journal.pone.0040430 22808161

59. Krivosheina MG. On insect feeding on cyanobacteria. Paleontological Journal. 2008 Oct 1;42(6):596–9.

60. Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS one. 2012 Jun 7;7(6):e38544. doi: 10.1371/journal.pone.0038544 22685581

61. Zug R, Hammerstein P. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews. 2015 Feb;90(1):89–111. doi: 10.1111/brv.12098 24618033

62. Beukeboom LW, Perrin N. The evolution of sex determination. Oxford University Press, USA; 2014.

63. Saurav GK, Daimei G, Rana VS, Popli S, Rajagopal R. Detection and Localization of Wolbachia in Thrips palmi Karny (Thysanoptera: Thripidae). Indian journal of microbiology. 2016 Jun 1;56(2):167–71. doi: 10.1007/s12088-016-0567-7 27570308

64. Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R. Host plant induced variation in gut bacteria of Helicoverpa armigera. PloS one. 2012 Jan 26;7(1):e30768. doi: 10.1371/journal.pone.0030768 22292034

65. Lòpez-Fernàndez S, Mazzoni V, Pedrazzoli F, Pertot I, Campisano A. A phloem-feeding insect transfers bacterial endophytic communities between grapevine plants. Frontiers in microbiology. 2017 May 15;8:834. doi: 10.3389/fmicb.2017.00834 28555131

66. De Vries EJ, Jacobs G, Sabelis MW, Menken SB, Breeuwer JA. Diet–dependent effects of gut bacteria on their insect host: the symbiosis of Erwinia sp. and western flower thrips. Proceedings of the Royal Society of London. Series B: Biological Sciences. 2004 Oct 22;271(1553):2171–8.

67. Chanbusarakum L, Ullman D. Characterization of bacterial symbionts in Frankliniella occidentalis (Pergande), Western flower thrips. Journal of invertebrate pathology. 2008 Nov 1;99(3):318–25. doi: 10.1016/j.jip.2008.09.001 18809409

68. Ranjith MT, Harish ER, Girija D, Nazeem PA. Bacterial communities associated with the gut of tomato fruit borer, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) based on Illumina Next-Generation Sequencing. Journal of Asia-Pacific Entomology. 2016 Jun 1;19(2):333–40.

69. Pan H, Li X, Ge D, Wang S, Wu Q, Xie W, Jiao X, Chu D, Liu B, Xu B, Zhang Y. Factors affecting population dynamics of maternally transmitted endosymbionts in Bemisia tabaci. PloS one. 2012 Feb 23;7(2):e30760. doi: 10.1371/journal.pone.0030760 22383972


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