1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 11

Kirkpatrickella diaphorinae gen. nov., sp. nov., an uncultured endosymbiont identified in a population of from Hawaii Open Access

Abstract

is the hemipteran pest and vector of a devastating bacterial pathogen of citrus worldwide. In addition to the two core bacterial endosymbionts of , Carsonella ruddii and Profftella armatura, the genome of a novel endosymbiont and as of yet undescribed microbe was discovered in a Hawaiian population through deep sequencing of multiple populations. Found to be closely related to the genus in the family by 16S rRNA gene sequence analysis, it forms a sister clade along with other insect-associated 16S rRNA gene sequences from uncultured bacterium found associated with and . Multilocus sequence analysis confirmed the phylogenetic placement sister to the clade. Despite the culturable clade being the closest phylogenetic neighbour, attempts to culture this newly identified bacterial endosymbiont were unsuccessful. On the basis of these distinct genetic differences, the novel endosymbiont is proposed to be classified into a candidate genus and species ‘ Kirkpatrickella diaphorinae’. The full genome was deposited in GenBank (accession number CP107052; prokaryotic 16S rRNA OP600170).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial symbiont , Diaphorina citri and endosymbiont
Funding
This study was supported by the:
  • National Institute of Food and Agriculture (Award 2015-70016-23011)
    • Principle Award Recipient: Yen-WenKuo
  • National Institute of Food and Agriculture (Award 2020-70029-33200)
    • Principle Award Recipient: Yen-WenKuo
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006111
2023-11-06
2024-05-08
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/73/11/ijsem006111.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.006111&mimeType=html&fmt=ahah

References

  1. Marutani-Hert M, Hunter WB, Morgan JK. Associated bacteria of Asian citrus psyllid (Hemiptera: Psyllidae: Diaphorina citri). Southwestern Entomologist 2011; 36:323–330 [View Article]
     [Google Scholar]
  2. Fagen JR, Giongo A, Brown CT, Davis-Richardson AG, Gano KA et al. 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. Open Microbiol J 2012; 6:29–33 [View Article] [PubMed]
     [Google Scholar]
  3. Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A et al. Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol 2013; 23:1478–1484 [View Article] [PubMed]
     [Google Scholar]
  4. Huang J, Dai Z, Zheng Z, da Silvia PA, Kumagai L et al. Bacteriomic analyses of Asian citrus psyllid and citrus samples infected with “Candidatus Liberibacter asiaticus” in Southern California and Huanglongbing management implications. Front Microbiol 2021; 12:683481 [View Article] [PubMed]
     [Google Scholar]
  5. Saha S, Hunter WB, Reese J, Morgan JK, Marutani-Hert M et al. Survey of endosymbionts in the Diaphorina citri metagenome and assembly of a Wolbachia wDi draft genome. PLoS ONE 2012; 7:e50067 [View Article]
     [Google Scholar]
  6. Nakabachi A, Malenovský I, Gjonov I, Hirose Y. 16S rRNA sequencing detected Profftella, Liberibacter, Wolbachia, and Diplorickettsia from relatives of the Asian citrus psyllid. Microb Ecol 2020; 80:410–422 [View Article] [PubMed]
     [Google Scholar]
  7. Nakabachi A, Piel J, Malenovský I, Hirose Y. Comparative genomics underlines multiple roles of Profftella, an obligate symbiont of Psyllids: providing toxins, vitamins, and carotenoids. Genome Biol Evol 2020; 12:1975–1987 [View Article] [PubMed]
     [Google Scholar]
  8. Dan H, Ikeda N, Fujikami M, Nakabachi A. Behavior of bacteriome symbionts during transovarial transmission and development of the Asian citrus psyllid. PLoS One 2017; 12:e0189779 [View Article] [PubMed]
     [Google Scholar]
  9. Alba-Alejandre I, Alba-Tercedor J, Hunter WB. Anatomical study of the female reproductive system and bacteriome of Diaphorina citri Kuwayama, (Insecta: Hemiptera, Liviidae) using micro-computed tomography. Sci Rep 2020; 10:7161 [View Article] [PubMed]
     [Google Scholar]
  10. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE et al. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 2006; 314:267 [View Article] [PubMed]
     [Google Scholar]
  11. Carlson CR, Ter Horst AM, Johnston JS, Henry E, Falk BW et al. High-quality, chromosome-scale genome assemblies: comparisons of three Diaphorina citri (Asian citrus psyllid) geographic populations. DNA Res 2022; 29:dsac027 [View Article] [PubMed]
     [Google Scholar]
  12. Chen Q, Godfrey K, Liu J, Mao Q, Kuo Y-W et al. A nonstructural protein responsible for viral spread of a novel insect reovirus provides a safe channel for biparental virus transmission to progeny. J Virol 2019; 93:e00702-19 [View Article] [PubMed]
     [Google Scholar]
  13. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R et al. The PATRIC bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res 2020; 48:D606–D612 [View Article] [PubMed]
     [Google Scholar]
  14. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
     [Google Scholar]
  15. Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res 2017; 27:824–834 [View Article] [PubMed]
     [Google Scholar]
  16. Li H, Birol I. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article]
     [Google Scholar]
  17. Kolmogorov M, Bickhart DM, Behsaz B, Gurevich A, Rayko M et al. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods 2020; 17:1103–1110 [View Article] [PubMed]
     [Google Scholar]
  18. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
     [Google Scholar]
  19. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
     [Google Scholar]
  20. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009; 19:1639–1645 [View Article] [PubMed]
     [Google Scholar]
  21. Nawrocki EP. Structural RNA Homology Search and Alignment using Covariance Models. Ph.D. thesis Washington University in Saint Louis, School of Medicine; 2009
     [Google Scholar]
  22. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. Corrigendum to: IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  23. Madeira F, Pearce M, Tivey ARN, Basutkar P, Lee J et al. Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res 2022; 50:W276–W279 [View Article] [PubMed]
     [Google Scholar]
  24. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article] [PubMed]
     [Google Scholar]
  25. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
     [Google Scholar]
  26. Yamada Y, Katsura K, Kawasaki H, Widyastuti Y, Saono S et al. Asaia bogorensis gen. nov., sp. nov., an unusual acetic acid bacterium in the alpha-Proteobacteria. Int J Syst Evol Microbiol 2000; 50 Pt 2:823–829 [View Article] [PubMed]
     [Google Scholar]
  27. Chouaia B, Gaiarsa S, Crotti E, Comandatore F, Degli Esposti M et al. Acetic acid bacteria genomes reveal functional traits for adaptation to life in insect guts. Genome Biol Evol 2014; 6:912–920 [View Article] [PubMed]
     [Google Scholar]
  28. Favia G, Ricci I, Damiani C, Raddadi N, Crotti E et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 2007; 104:9047–9051 [View Article] [PubMed]
     [Google Scholar]
  29. Chylinski K, Makarova KS, Charpentier E, Koonin EV. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res 2014; 42:6091–6105 [View Article] [PubMed]
     [Google Scholar]
  30. Alonso DP, Mancini MV, Damiani C, Cappelli A, Ricci I et al. Genome reduction in the mosquito symbiont Asaia. Genome Biol Evol 2019; 11:1–10 [View Article] [PubMed]
     [Google Scholar]
  31. Chen S, Yu T, Terrapon N, Henrissat B, Walker ED. Genome features of Asaia sp. W12 isolated from the mosquito Anopheles stephensi reveal symbiotic traits. Genes 2021; 12:752 [View Article]
     [Google Scholar]
  32. Kawai M, Higashiura N, Hayasaki K, Okamoto N, Takami A et al. Complete genome and gene expression analyses of Asaia bogorensis reveal unique responses to culture with mammalian cells as a potential opportunistic human pathogen. DNA Res 2015; 22:357–366 [View Article] [PubMed]
     [Google Scholar]
  33. Li F, Li P, Hua H, Hou M, Wang F. Diversity, tissue localization, and infection pattern of bacterial symbionts of the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Microb Ecol 2020; 79:720–730 [View Article] [PubMed]
     [Google Scholar]
  34. Kautz S, Rubin BER, Moreau CS. Bacterial infections across the ants: frequency and prevalence of Wolbachia, Spiroplasma, and Asaia. Psyche J Entomol 2013; 2013:1–11 [View Article]
     [Google Scholar]
  35. Mancini MV, Damiani C, Short SM, Cappelli A, Ulissi U et al. Inhibition of Asaia in adult mosquitoes causes male-specific mortality and diverse transcriptome changes. Pathogens 2020; 9:380 [View Article]
     [Google Scholar]
  36. Mitraka E, Stathopoulos S, Siden-Kiamos I, Christophides GK, Louis C. Asaia accelerates larval development of Anopheles gambiae. Pathog Glob Health 2013; 107:305–311 [View Article] [PubMed]
     [Google Scholar]
  37. Chouaia B, Rossi P, Epis S, Mosca M, Ricci I et al. Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts. BMC Microbiol 2012; 12 Suppl 1:S2 [View Article] [PubMed]
     [Google Scholar]
  38. Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A et al. Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol 2008; 18:R1087–8 [View Article] [PubMed]
     [Google Scholar]
  39. Bongio NJ, Lampe DJ. Inhibition of Plasmodium berghei development in mosquitoes by effector proteins secreted from Asaia sp. bacteria using a novel native secretion signal. PLoS One 2015; 10:e0143541 [View Article] [PubMed]
     [Google Scholar]
  40. Loganathan P, Nair S. Swaminathania salitolerans gen. nov., sp. nov., a salt-tolerant, nitrogen-fixing and phosphate-solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int J Syst Evol Microbiol 2004; 54:1185–1190 [View Article] [PubMed]
     [Google Scholar]
  41. Alfano N, Tagliapietra V, Rosso F, Manica M, Arnoldi D et al. Changes in microbiota across developmental stages of Aedes koreicus, an invasive mosquito vector in Europe: indications for microbiota-based control strategies. Front Microbiol 2019; 10:2832 [View Article] [PubMed]
     [Google Scholar]
  42. Masson F, Lemaitre B. Growing ungrowable bacteria: overview and perspectives on insect symbiont culturability. Microbiol Mol Biol Rev 2020; 84:e00089–20 [View Article]
     [Google Scholar]
  43. Toft C, Fares MA. The evolution of the flagellar assembly pathway in endosymbiotic bacterial genomes. Mol Biol Evol 2008; 25:2069–2076 [View Article] [PubMed]
     [Google Scholar]
  44. Husnik F, McCutcheon JP. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc Natl Acad Sci USA 2016; 113: [View Article] [PubMed]
     [Google Scholar]
  45. Conord C, Despres L, Vallier A, Balmand S, Miquel C et al. Long-term evolutionary stability of bacterial endosymbiosis in curculionoidea: additional evidence of symbiont replacement in the dryophthoridae family. Mol Biol Evol 2008; 25:859–868 [View Article] [PubMed]
     [Google Scholar]
  46. Matsuura Y, Moriyama M, Łukasik P, Vanderpool D, Tanahashi M et al. Recurrent symbiont recruitment from fungal parasites in cicadas. Proc Natl Acad Sci USA 2018; 115:E5970–E5979 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006111
Loading
Candidatus Kirkpatrickella diaphorinae gen. nov., sp. nov., an uncultured endosymbiont identified in a population of Diaphorina citri from Hawaii
Int J Syst Evol Microbiol 73, 006111 (2023); https://doi.org/10.1099/ijsem.0.006111
/content/journal/ijsem/10.1099/ijsem.0.006111
/content/journal/ijsem/10.1099/ijsem.0.006111
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error