Skip to main content
Log in

Composition and change in the microbiome of Diaphorina citri infected with Candidatus Liberibacter asiaticus in China

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is the primary vector of Candidatus Liberibacter asiaticus (Las), which causes the devastating disease Huanglongbing (HLB) in Asian citrus. To examine the effects of pathogens on the diversity and structure of insect-associated bacterial communities, we carried out a molecular analysis using healthy D.citri and Las-infected D.citri as a vector-pathogen model. 16S rRNA Illumina sequencing analysis of D.citri revealed shifts in its microbial diversity in response to pathogen infection. The phylum Proteobacteria predominated in D.citri representing 89.40 and 91.73% of the bacterial communities, while remaining bacterial sequences were mainly assigned to the phyla Actinobacteria, Firmicutes, Bacteroidetes and Acidobacteria. The relative proportions of different groups of bacteria changed significantly after pathogen infection. The relative abundance of bacterial communities between healthy D.citri and Las-infected D.citri were different, and the relative abundance of most dominant bacteria decreased, such as Oscillospira, Lactobacillus and Rubrobacter. However, the relative abundance of Wolbachia increased from 1.81 to 2.14%, and there was no difference in the abundance of Carsonella. In pairwise comparisons, the clone library from healthy D.citri contained greater 16S rRNA gene diversity, as reflected by the higher Shannon index at 2.937 versus 2.756 for the healthy and Las-infected clone libraries, respectively. These data indicated that Las infection has a profound effect on the structure and composition of the bacterial community associated with D.citri.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria mediated nitrogen fixation in natural populations of the fruit fly Ceratitiscapitata. Mol Ecol 14:2637–2643

    Article  CAS  Google Scholar 

  • Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK (2010) Qiime allows analysis of high-throughput community sequencing data. Nat Methods 7:335–356

    Article  CAS  Google Scholar 

  • Dodson BL, Hughes GL, Paul O, Matacchiero AC, Kramer LD, Rasgon JL (2014) Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. Plos Negl Trop Dis 8(7):e2965

    Article  Google Scholar 

  • Fagen JR, Giongo A, Brown CT, Davis-Richardson AG, Gano KA, Triplett EW (2012) Characterization of the relative abundance of the Citrus pathogen Ca. Liberibacter Asiaticus in the microbiome of its insect vector, Diaphorina citri, using high throughput 16S rRNA sequencing. The Open Microbiology Journal 6:29–33

    Article  CAS  Google Scholar 

  • Gil R, Pérez-Brocal V, Latorre A, Moya A (2006) Minimal genomes required for life. In Prokaryotic diversity Mecanisms and significance edited by: Logan NA, Lappin-Scott HM, Oyston CF. Cambridge University Press, 105–121

  • Hughes GL, Vega-Rodriguez J, Xue P, Rasgon JL (2012) Wolbachia strain wAlbB enhances infection by the rodent malaria parasite Plasmodium berghei in Anopheles gambiae mosquitoes. Semin Liver Dis 13(02):126–135

    Google Scholar 

  • Hussain M, Frentiu FD, Moreira LA, O'Neill SL., Asgari S (2011) Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedesaegypti. Proceedings of the National Academy of Sciences of the United States of America, 108:9250-9255

    Article  CAS  Google Scholar 

  • Inoue H, Ohnishi J, Ito T, Tomimura K, Miyata S, Iwanami T (2009) Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Ann Appl Biol 155:29–36

    Article  Google Scholar 

  • Jagoueix S, Bové JM, Garnier M (1996) PCR detection of the two 'Candidatus' Liberobacter species associated with greening disease of citrus. Mol Cell Probes 10:43–50

    Article  CAS  Google Scholar 

  • Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204

    Article  Google Scholar 

  • Kolora LD, Powell CM, Hunter W, Bextine B, Lauzon CR (2015) Internal extracellular Bacteria of Diaphorina citri, Kuwayama (Hemiptera:Psyllidae), the Asian citrus psyllid. Curr Microbiol 70(5):710–715

    Article  CAS  Google Scholar 

  • Lin XL, Pan QJ, Tian HG, Douglas AE, Liu TX (2015) Bacteria abundance and diversity of different life stages of Plutellaxylostella (Lepidoptera: plutellidae), revealed by bacteria culture-dependent and pcr-dgge methods. Insect Sci 22:375–385

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) Flash: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  Google Scholar 

  • Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterialendosymbiont Carsonella. Science 314:267

    Article  CAS  Google Scholar 

  • Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A, Gurgui M, Oldham NJ, van Echten-Deckert G, Okamura K, Yamamoto K, Inoue H, Ohkuma M, Hongoh Y, Miyagishima SY, Hattori M, Piel J, Fukatsu T (2013) Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol 23(15):1478–1484

    Article  CAS  Google Scholar 

  • O'Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM (1992)16s rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proceedings of the National Academy of Sciences of the United States of America, 89:2699-2702

    Article  CAS  Google Scholar 

  • O'Neill SL, Hoffman AA, Werren JH (1997) Influential passengers: inherited microorganisms and arthropod reproduction. Q Rev Biol 4:143–144

    Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America, 110:6548-6553

    Article  CAS  Google Scholar 

  • Subandiyah S, Nikoh N, Tsuyumu S, Somowiyarjo S, Fukatsu T (2000) Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera : Psylloidea). Zool Sci 17:983–989

    Article  Google Scholar 

  • Surya S, Hunter WB, Justin R et al (2012) Survey of endosymbionts in the Diaphorina citri metagenome and assembly of a Wolbachia wDi draft genome[J]. PLoS One 7(11):e50067

    Article  Google Scholar 

  • Takatsuka J, Kunimi Y (2000) Intestinal bacteria affect growth of Bacillus thuringiensis in larvae of the oriental tea tortrix, Homona magnanima Diakonoff (Lepidoptera: tortricidae). J Invertebr Pathol 76:222–226

    Article  CAS  Google Scholar 

  • Tamames J, Gil R, Latorre A, Peretó J, Silva FJ, Moya A (2007) The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol 7:181

    Article  Google Scholar 

  • Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66:2898–2905

    Article  CAS  Google Scholar 

  • Trivedi P, Duan Y, Wang N (2010) Huanglongbing, a systemic disease, restructures the bacterial community associated with citrus roots. Appl Environ Microbiol 76:3427–3436

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609

    Article  CAS  Google Scholar 

  • Zhou LJ, Gabriel DW, Duan YP, Halbert SE, Dixon WN (2007) First report of dodder transmission of huanglongbing from naturally infected murraya paniculata to citrus. Plant Dis 91:227

    Article  CAS  Google Scholar 

Download references

Funding

This article was supported by the National Key R& D Program of China (2018YFD0201500, 2017YFD0202000), the Public Research and Capacity Building Project of Guangdong (2014B020203003), and the Guangdong Provincial Special Fund of Modern Agricultural Industry Technology Innovation Team (2019KJ108).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ai-tian Peng or Lian-hui Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, Xb., Peng, At., Ling, Jf. et al. Composition and change in the microbiome of Diaphorina citri infected with Candidatus Liberibacter asiaticus in China. Int J Trop Insect Sci 39, 283–290 (2019). https://doi.org/10.1007/s42690-019-00036-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-019-00036-3

Keywords

Navigation