Skip to content
1887

Microbial Genomics logo Microbial Genomics

Volume 11, Issue 6

Diverse toxin repertoire but limited metabolic capacities inferred from the draft genome assemblies of three (Citri clade) strains associated with Open Access

Abstract

(class ) is a diverse wall-less bacterial genus whose members are strictly dependent on eukaryotic hosts (mostly arthropods and plants), with which they engage in pathogenic to mutualistic interactions. are generally fastidious to culture , especially those that are vertically transmitted by their hosts, which include flies in the genus . has been invaded by at least three independent clades of : Poulsonii (the best studied, contains reproductive manipulators and defensive mutualists associated with two major clades of and has amongst the highest substitution rates within bacteria), Citri (restricted to the group of ) and Ixodetis. We report the first genome drafts of -associated Citri clade : strain Moj from , strain Ald-Tx from from Texas (newly discovered; also associated with ) and strain Hy2 from (the only species known to naturally also harbour a Poulsonii clade strain, thereby providing an arena for horizontal gene transfer). Compared to their Poulsonii clade counterparts, we infer that the three Citri clade strains have the following: (1) equal or worse DNA repair abilities; (b) more limited metabolic capacities, which may underlie their comparatively lower titres and transmission efficiency; and (c) similar content of toxin domains, including at least one ribosome-inactivating protein, which is implicated in the Poulsonii-conferred defence against natural enemies. As a byproduct of our phylogenomic analyses and exhaustive search for certain toxin domains in public databases, we document the toxin repertoire in close relatives of -associated , and in a very divergent newly discovered lineage (i.e. ‘clade X’). Phylogenies of toxin-encoding genes or domains imply substantial exchanges between closely and distantly related strains. Surprisingly, despite encoding several toxin genes and achieving relatively high prevalences in certain natural populations (Ald-Tx in this study; Moj in prior work), fitness assays of Moj (this study) and Ald-Tx (prior work) in the context of wasp parasitism fail to detect a beneficial effect to their hosts. Thus, how Citri clade strains persist in their host populations remains elusive.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Mycoplasma , phylogeny , symbiosis and vertical transmission
© 2025 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/mgen/10.1099/mgen.0.001408
2025-06-05
2025-06-23
Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/6/mgen001408.html?itemId=/content/journal/mgen/10.1099/mgen.0.001408&mimeType=html&fmt=ahah

References

  1. Duron O, Hurst GD. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol 2013; 11: [View Article]
     [Google Scholar]
  2. Russell JA, Funaro CF, Milton Y, Goldman-Huertas B, Suh D et al. A veritable menagerie of heritable bacteria across the ants, lepidopterans, and beyond. PLoS One 2012; 7: [View Article]
     [Google Scholar]
  3. 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; 7:e38544 [View Article] [PubMed]
     [Google Scholar]
  4. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008; 6:741–751 [View Article]
     [Google Scholar]
  5. Łukasik P, Kolasa MR. With a little help from my friends: the roles of microbial symbionts in insect populations and communities. Philos Trans R Soc Lond B Biol Sci 2024; 379:20230122 [View Article] [PubMed]
     [Google Scholar]
  6. Ross PA, Turelli M, Hoffmann AA. Evolutionary ecology of Wolbachia releases for disease control. Annu Rev Genet 2019; 53:93–116 [View Article] [PubMed]
     [Google Scholar]
  7. Behrmann LV, Meier K, Vollmer J, Chiedu CC, Schiefer A et al. In vitro extracellular replication of Wolbachia endobacteria. Front Microbiol 2024; 15:1405287 [View Article]
     [Google Scholar]
  8. Wang W, Cui W, Yang H. Toward an accurate mechanistic understanding of Wolbachia-induced cytoplasmic incompatibility. Environ Microbiol 2022; 24:4519–4532 [View Article] [PubMed]
     [Google Scholar]
  9. Hochstrasser M. Molecular biology of cytoplasmic incompatibility caused by Wolbachia endosymbionts. Annu Rev Microbiol 2023; 77:299–316 [View Article] [PubMed]
     [Google Scholar]
  10. Porter J, Sullivan W. The cellular lives of Wolbachia. Nat Rev Microbiol 2023; 21:750–766 [View Article] [PubMed]
     [Google Scholar]
  11. Tan Y, Aravind L, Zhang D. Genomic underpinnings of cytoplasmic incompatibility: CIF gene-neighborhood diversification through extensive lateral transfers and recombination in Wolbachia. Genome Biol Evol 2024; 16:evae171 [View Article] [PubMed]
     [Google Scholar]
  12. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009; 325:992–994 [View Article] [PubMed]
     [Google Scholar]
  13. Brandt JW, Chevignon G, Oliver KM, Strand MR. Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids. Proc Biol Sci 2017; 284:20171925 [View Article] [PubMed]
     [Google Scholar]
  14. Patel V, Lynn-Bell N, Chevignon G, Kucuk RA, Higashi CHV et al. Mobile elements create strain-level variation in the services conferred by an aphid symbiont. Environ Microbiol 2023; 25:3333–3348 [View Article] [PubMed]
     [Google Scholar]
  15. Regassa LB. The family Spiroplasmataceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. eds The Prokaryotes: Firmicutes and Tenericutes Berlin, Heidelberg: Springer; 2014 pp 551–67
     [Google Scholar]
  16. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 2008; 6:27 [View Article] [PubMed]
     [Google Scholar]
  17. Williamson DL, Poulson DF. Sex ratio organisms (Spiroplasmas) of Drosophila. Mycoplasmas 1979; 3:175–208
     [Google Scholar]
  18. Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J et al. The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Syst Evol Microbiol 2004; 54:893–918 [View Article] [PubMed]
     [Google Scholar]
  19. Moore LD, Ballinger MJ. The toxins of vertically transmitted Spiroplasma. Front Microbiol 2023; 14:1148263 [View Article]
     [Google Scholar]
  20. Kikuchi Y. Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 2009; 24:195–204 [View Article] [PubMed]
     [Google Scholar]
  21. Masson F, Lemaitre B. Growing ungrowable bacteria: overview and perspectives on insect symbiont culturability. Microbiol Mol Biol Rev 2020; 84:00089–20 [View Article] [PubMed]
     [Google Scholar]
  22. Masson F, Schüpfer F, Jollivet C, Lemaitre B. Transformation of the Drosophila sex-manipulative endosymbiont Spiroplasma poulsonii and persisting hurdles for functional genetic studies. Appl Environ Microbiol 2020; 86:00835–20 [View Article] [PubMed]
     [Google Scholar]
  23. Masson F, Calderon Copete S, Schüpfer F, Garcia-Arraez G, Lemaitre B. In vitro culture of the insect endosymbiont Spiroplasma poulsonii highlights bacterial genes involved in host-symbiont interaction. mBio 2018; 9:e00024-18 [View Article] [PubMed]
     [Google Scholar]
  24. Anbutsu H, Fukatsu T. Spiroplasma as a model insect endosymbiont. Environ Microbiol Rep 2011; 3:144–153 [View Article] [PubMed]
     [Google Scholar]
  25. Hurst GDD, Jiggins FM, Majerus MEN. 12 inherited microorganisms that selectively kill male hosts: the hidden players of insect evolution?. In Insect Symbiosis vol 177 2003 [View Article]
     [Google Scholar]
  26. Jaenike J, Stahlhut JK, Boelio LM, Unckless RL. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism?. Mol Ecol 2010; 19:414–425 [View Article] [PubMed]
     [Google Scholar]
  27. Martinez-Montoya H. Spiroplasma and its interaction with Drosophila: genome sequencing and analysis of potential fitness effects of naturally infected populations [Dissertation]. Texas A&M University; College Station, TX, USA: 2017
     [Google Scholar]
  28. Haselkorn TS. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly 2010; 4:80–87 [View Article]
     [Google Scholar]
  29. Herren JK, Paredes JC, Schüpfer F, Lemaitre B. Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. mBio 2013; 4:e00532-12 [View Article] [PubMed]
     [Google Scholar]
  30. Haselkorn TS, Markow TA, Moran NA. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 2009; 18:1294–1305 [View Article] [PubMed]
     [Google Scholar]
  31. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA et al. Heritable endosymbionts of Drosophila. Genetics 2006; 174:363–376 [View Article] [PubMed]
     [Google Scholar]
  32. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 2007; 3:23–25 [View Article] [PubMed]
     [Google Scholar]
  33. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 2010; 329:212–215 [View Article] [PubMed]
     [Google Scholar]
  34. Xie J, Vilchez I, Mateos M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 2010; 5:e12149 [View Article] [PubMed]
     [Google Scholar]
  35. Hrdina A, Serra Canales M, Arias-Rojas A, Frahm D, Iatsenko I. The endosymbiont Spiroplasma poulsonii increases Drosophila melanogaster resistance to pathogens by enhancing iron sequestration and melanization. mBio 2024; 15:e0093624 [View Article] [PubMed]
     [Google Scholar]
  36. Herren JK, Paredes JC, Schüpfer F, Arafah K, Bulet P et al. Insect endosymbiont proliferation is limited by lipid availability. elife 2014; 3:e02964 [View Article] [PubMed]
     [Google Scholar]
  37. Herren JK, Lemaitre B. Spiroplasma and host immunity: activation of humoral immune responses increases endosymbiont load and susceptibility to certain Gram-negative bacterial pathogens in Drosophila melanogaster. Cell Microbiol 2011; 13:1385–1396 [View Article] [PubMed]
     [Google Scholar]
  38. Haselkorn TS, Watts TD, Markow TA. Density dynamics of diverse Spiroplasma strains naturally infecting different species of Drosophila. Fly 2013; 7:204–210 [View Article] [PubMed]
     [Google Scholar]
  39. Gerth M, Martinez-Montoya H, Ramirez P, Masson F, Griffin JS et al. Rapid molecular evolution of Spiroplasma symbionts of Drosophila. Microb Genom 2021; 7: [View Article]
     [Google Scholar]
  40. Williamson DL, Sakaguchi B, Hackett KJ, Whitcomb RF, Tully JG et al. Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int J Syst Bacteriol 1999; 49 Pt 2:611–618 [View Article] [PubMed]
     [Google Scholar]
  41. Hackett KJ, Lynn DE, Williamson DL, Ginsberg AS, Whitcomb RF. Cultivation of the Drosophila sex-ratio spiroplasma. Science 1986; 232:1253–1255 [View Article] [PubMed]
     [Google Scholar]
  42. Masson F, Rommelaere S, Marra A, Schüpfer F, Lemaitre B. Dual proteomics of Drosophila melanogaster hemolymph infected with the heritable endosymbiont Spiroplasma poulsonii. PLoS One 2021; 16:e0250524 [View Article] [PubMed]
     [Google Scholar]
  43. Hamilton PT, Peng F, Boulanger MJ, Perlman SJ. A ribosome-inactivating protein in a Drosophila defensive symbiont. Proc Natl Acad Sci USA 2016; 113:350–355 [View Article] [PubMed]
     [Google Scholar]
  44. Bentley JK, Veneti Z, Heraty J, Hurst GDD. The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol 2007; 5:9 [View Article] [PubMed]
     [Google Scholar]
  45. Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GDD. A functional dosage compensation complex required for male killing in Drosophila. Science 2005; 307:1461–1463 [View Article] [PubMed]
     [Google Scholar]
  46. Harumoto T. Self-stabilization mechanism encoded by a bacterial toxin facilitates reproductive parasitism. Curr Biol 2023; 33:4021–4029 [View Article] [PubMed]
     [Google Scholar]
  47. Harumoto T, Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature 2018; 557:252–255 [View Article] [PubMed]
     [Google Scholar]
  48. Harumoto T, Anbutsu H, Lemaitre B, Fukatsu T. Male-killing symbiont damages host’s dosage-compensated sex chromosome to induce embryonic apoptosis. Nat Commun 2016; 7:12781 [View Article] [PubMed]
     [Google Scholar]
  49. Harumoto T, Anbutsu H, Fukatsu T. Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog 2014; 10:e1003956 [View Article] [PubMed]
     [Google Scholar]
  50. Masson F, Calderon-Copete S, Schüpfer F, Vigneron A, Rommelaere S et al. Blind killing of both male and female Drosophila embryos by a natural variant of the endosymbiotic bacterium Spiroplasma poulsonii. Cell Microbiol 2020; 22:e13156 [View Article] [PubMed]
     [Google Scholar]
  51. Garcia-Arraez MG, Masson F, Escobar JCP, Lemaitre B. Functional analysis of RIP toxins from the Drosophila endosymbiont Spiroplasma poulsonii. BMC Microbiol 2019; 19:46 [View Article] [PubMed]
     [Google Scholar]
  52. Watts T, Haselkorn TS, Moran NA, Markow TA. Variable incidence of Spiroplasma infections in natural populations of Drosophila species. PLoS One 2009; 4:e5703 [View Article] [PubMed]
     [Google Scholar]
  53. Wasserman M. Cytological evolution in the Drosophila repleta species group. Ecological genetics and evolution: the cactus-yeast-Drosophila model system/edited JSF barker, WT starmer; 1982
  54. Acurio AE. Evidence of a South American origin for the Drosophila repleta group (Diptera: Drosophilidae). Eur J Entomol 2024; 121:124–133 [View Article]
     [Google Scholar]
  55. Osaka R, Watada M, Kageyama D, Nomura M. Population dynamics of a maternally-transmitted Spiroplasma infection in Drosophila hydei. Symbiosis 2010; 52:41–45 [View Article]
     [Google Scholar]
  56. Kageyama D, Anbutsu H, Watada M, Hosokawa T, Shimada M et al. Prevalence of a non-male-killing Spiroplasma in natural populations of Drosophila hydei. Appl Environ Microbiol 2006; 72:6667–6673 [View Article] [PubMed]
     [Google Scholar]
  57. Ota T, Kawabe M, Oishi K, Poulson DF. Non-male-killing spiroplasmas in Drosophila hydei. J Hered 1979; 70:211–213 [View Article]
     [Google Scholar]
  58. Corbin C, Jones JE, Chrostek E, Fenton A, Hurst GDD. Thermal sensitivity of the Spiroplasma-Drosophila hydei protective symbiosis: the best of climes, the worst of climes. Mol Ecol 2021; 30:1336–1344 [View Article] [PubMed]
     [Google Scholar]
  59. Patterson JT. The Drosophilidae of the Southwest The University of Texas Publications; 1943 pp 7–214
     [Google Scholar]
  60. Folmer O, Black MB, Hoeh WR, Lutz RA, Vrijenhoek RC. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994; 3:294–299 [PubMed]
     [Google Scholar]
  61. Gloor GB, Preston CR, Johnson-Schlitz DM, Nassif NA, Phillis RW et al. Type I repressors of P element mobility. Genetics 1993; 135:81–95 [View Article] [PubMed]
     [Google Scholar]
  62. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010
  63. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  64. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  65. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  66. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinf 2009; 10:421 [View Article] [PubMed]
     [Google Scholar]
  67. Harris RS. Improved Pairwise Alignment of Genomic DNA The Pennsylvania State University; 2007
     [Google Scholar]
  68. Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R et al. Human-mouse alignments with BLASTZ. Genome Res 2003; 13:103–107 [View Article] [PubMed]
     [Google Scholar]
  69. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
     [Google Scholar]
  70. 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]
  71. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
     [Google Scholar]
  72. Yan X-H, Pei S-C, Yen H-C, Blanchard A, Sirand-Pugnet P et al. Delineating bacterial genera based on gene content analysis: a case study of the Mycoplasmatales-Entomoplasmatales clade within the class Mollicutes. Microb Genom 2024; 10:001321 [View Article] [PubMed]
     [Google Scholar]
  73. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  74. The Galaxy Community The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2022 update. Nucleic Acids Res 2022; 50:W345-W51 [View Article]
     [Google Scholar]
  75. Jones P, Binns D, Chang H-Y, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article] [PubMed]
     [Google Scholar]
  76. Mulder N, Apweiler R. InterPro and InterProScan: tools for protein sequence classification and comparison. Methods Mol Biol 2007; 396:59–70 [View Article] [PubMed]
     [Google Scholar]
  77. Massey JH, Newton ILG. Diversity and function of arthropod endosymbiont toxins. Trends Microbiol 2022; 30:185–198 [View Article] [PubMed]
     [Google Scholar]
  78. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  79. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
     [Google Scholar]
  80. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. 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]
  81. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article] [PubMed]
     [Google Scholar]
  82. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
     [Google Scholar]
  83. Russel J, Pinilla-Redondo R, Mayo-Muñoz D, Shah SA, Sørensen SJ. CRISPRCasTyper: automated identification, annotation, and classification of CRISPR-Cas loci. CRISPR J 2020; 3:462–469 [View Article] [PubMed]
     [Google Scholar]
  84. Boratyn GM, Schäffer AA, Agarwala R, Altschul SF, Lipman DJ et al. Domain enhanced lookup time accelerated BLAST. Biol Direct 2012; 7:12 [View Article] [PubMed]
     [Google Scholar]
  85. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20:238 [View Article] [PubMed]
     [Google Scholar]
  86. Bruen T, Bruen T. PhiPack: PHI test and other tests of recombination. McGill University, Montreal, Quebec; 2005 pp 1–8
  87. Haselkorn TS, Jaenike J. Macroevolutionary persistence of heritable endosymbionts: acquisition, retention and expression of adaptive phenotypes in Spiroplasma. Mol Ecol 2015; 24:3752–3765 [View Article] [PubMed]
     [Google Scholar]
  88. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD. Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 2005; 14:281–287 [View Article] [PubMed]
     [Google Scholar]
  89. Malogolowkin C. Maternally inherited “sex ratio” conditions in Drosophila willistoni and Drosophila paulistorum. Genetics 1958; 43:274–286 [View Article] [PubMed]
     [Google Scholar]
  90. Ventura IM, Martins AB, Lyra ML, Andrade CAC, Carvalho KA et al. Spiroplasma in Drosophila melanogaster populations: prevalence, male-killing, molecular identification, and no association with Wolbachia. Microb Ecol 2012; 64:794–801 [View Article] [PubMed]
     [Google Scholar]
  91. Xie J, Butler S, Sanchez G, Mateos M. Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 2014; 112:399–408 [View Article] [PubMed]
     [Google Scholar]
  92. Paredes JC, Herren JK, Schüpfer F, Lemaitre B. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio 2016; 7:01006–01016 [View Article] [PubMed]
     [Google Scholar]
  93. Jones JE, Hurst GDD. Symbiont-mediated fly survival is independent of defensive symbiont genotype in the Drosophila melanogaster-Spiroplasma-wasp interaction. J Evol Biol 2020; 33:1625–1633 [View Article] [PubMed]
     [Google Scholar]
  94. Jones JE, Hurst GDD. Symbiont-mediated protection varies with wasp genotype in the Drosophila melanogaster-Spiroplasma interaction. Heredity 2020; 124:592–602 [View Article] [PubMed]
     [Google Scholar]
  95. Lue C-H, Buffington ML, Scheffer S, Lewis M, Elliott TA et al. DROP: molecular voucher database for identification of Drosophila parasitoids. Mol Ecol Resour 2021; 21:2437–2454 [View Article] [PubMed]
     [Google Scholar]
  96. Mateos M, Winter L, Winter C, Higareda-Alvear VM, Martinez-Romero E et al. Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont. Ecol Evol 2016; 6:2679–2687 [View Article] [PubMed]
     [Google Scholar]
  97. Ballinger MJ, Perlman SJ. Generality of toxins in defensive symbiosis: ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathog 2017; 13:e1006431 [View Article] [PubMed]
     [Google Scholar]
  98. Łukasik P, Dawid MA, Ferrari J, Godfray HCJ. The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia 2013; 173:985–996 [View Article] [PubMed]
     [Google Scholar]
  99. Xie J, Tiner B, Vilchez I, Mateos M. Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol Ecol 2011; 53:1065–1079 [View Article] [PubMed]
     [Google Scholar]
  100. Ebbert MA. The interaction phenotype in the Drosophila willistoni-Spiroplasma symbiosis. Evolution 1991; 45:971–988 [View Article] [PubMed]
     [Google Scholar]
  101. Malogolowkin-Cohen C, Rodrigues-Pereira MAQ. Sexual drive of normal and SR flies of Drosophila nebulosa. Evolution 1975; 29:579–580 [View Article] [PubMed]
     [Google Scholar]
  102. Vilchez-Ramirez I. Exploring the persistence of a non-male-killing Spiroplasma infection in Drosophila and the potential host range of Drosophila-infecting Spiroplasmas. Dissertation Texas A&M University; College Station: 2018
     [Google Scholar]
  103. Oliveira DCSG, Almeida FC, O’Grady PM, Armella MA, DeSalle R et al. Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Mol Phylogenet Evol 2012; 64:533–544 [View Article] [PubMed]
     [Google Scholar]
  104. Oliveira DCSG, Leonidas M, Etges WJ, O’grady PM, Desalle R. Species delimitation in the Drosophila aldrichi subcluster (Diptera: Drosophilidae) using DNA sequences. Zootaxa 2008; 1725:37–47 [View Article]
     [Google Scholar]
  105. Beckenbach AT, Heed WB, Etges WJ. A mitochondrial DNA analysis of vicariant speciation in two lineages in the Drosophila mulleri subgroup. Evol Ecol Res 2008; 10:475–492
     [Google Scholar]
  106. Castro Vargas C, Richmond MP, Ramirez Loustalot Laclette M, Markow TA. Early events in speciation: cryptic species of Drosophila aldrichi. Ecol Evol 2017; 7:4220–4228 [View Article] [PubMed]
     [Google Scholar]
  107. Perez-Leanos A, Loustalot-Laclette MR, Nazario-Yepiz N, Markow TA. Ectoparasitic mites and their Drosophila hosts. Fly 2017; 11:10–18
     [Google Scholar]
  108. Osaka R, Watada M, Kageyama D, Nomura M. Detection of Spiroplasma from the mite Macrocheles sp. (Acari; Macrochelidae) ectoparasitic to the fly Drosophila hydei (Diptera; Drosophilidae): a possible route of horizontal transmission?. Symbiosis 2013; 60:79–84 [View Article]
     [Google Scholar]
  109. Gehrer L, Vorburger C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 2012; 8:613–615 [View Article]
     [Google Scholar]
  110. Ahmed MZ, Li S-J, Xue X, Yin X-J, Ren S-X et al. The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 2015; 10:e1004672 [View Article] [PubMed]
     [Google Scholar]
  111. Williamson DL. Studies on the pathogenicity of spiroplasmas for Drosophila pseudoobscura. Annales de l’Institut Pasteur / Microbiologie 1984; 135:157–162 [View Article]
     [Google Scholar]
  112. Ballinger MJ, Gawryluk RMR, Perlman SJ. Toxin and genome evolution in a Drosophila defensive symbiosis. Genome Biol Evol 2019; 11:253–262 [View Article] [PubMed]
     [Google Scholar]
  113. Berner D, Ruffener S, Blattner LA. Chromosome-level assemblies of the Pieris mannii butterfly genome suggest Z-origin and rapid evolution of the W chromosome4o. Genome Biol Evol 2023; 15:evad111 [View Article] [PubMed]
     [Google Scholar]
  114. Filée J, Lopez-Villavicencio M, Debat V, Fourdin R, Salazar C et al. Wild communities of morpho butterflies reveal Spiroplasma endosymbiont with inflated genome size and peculiar evolution. bioRxiv 2024 [View Article]
     [Google Scholar]
  115. Haryono M, Lo WS, Gasparich GE, Kuo CH. Complete genome sequence of Spiroplasma sp. NBRC 100390. Genome Announc 2017; 5: [View Article]
     [Google Scholar]
  116. Lo WS, Haryono M, Gasparich GE, Kuo CH. Complete genome sequence of Spiroplasma sp. TU-14. Genome Announc 2017; 5:01465–16 [View Article] [PubMed]
     [Google Scholar]
  117. Vera-Ponce León A, Dominguez-Mirazo M, Bustamante-Brito R, Higareda-Alvear V, Rosenblueth M et al. Functional genomics of a Spiroplasma associated with the carmine cochineals Dactylopius coccus and Dactylopius opuntiae. BMC Genom 2021; 22:240 [View Article] [PubMed]
     [Google Scholar]
  118. Timmermans M, Prabha H, Kett S. Wolbachia and Spiroplasma endosymbionts in the Anurida maritima (Collembola) species group. Evol J Lin Soc 2023; 2: [View Article]
     [Google Scholar]
  119. Mishra D, Srinivasan R. Catching a walker in the act – DNA partitioning by ParA family of proteins. Front Microbiol 2022; 13:856547 [View Article] [PubMed]
     [Google Scholar]
  120. Ipoutcha T, Tsarmpopoulos I, Talenton V, Gaspin C, Moisan A et al. Multiple origins and specific evolution of CRISPR/Cas9 systems in minimal bacteria (Mollicutes). Front Microbiol 2019; 10:2701 [View Article] [PubMed]
     [Google Scholar]
  121. Ku C, Lo W-S, Chen L-L, Kuo C-H. Complete genomes of two dipteran-associated spiroplasmas provided insights into the origin, dynamics, and impacts of viral invasion in Spiroplasma. Genome Biol Evol 2013; 5:1151–1164 [View Article] [PubMed]
     [Google Scholar]
  122. Knezevic P, Adriaenssens EM, Ictv Report C. ICTV virus taxonomy profile: Plectroviridae. J Gen Virol 2021; 102: [View Article]
     [Google Scholar]
  123. Ramirez P, Leavitt JC, Gill JJ, Mateos M. Preliminary characterization of phage-like particles from the male-killing Mollicute Spiroplasma poulsonii (an endosymbiont of Drosophila). Curr Microbiol 2023; 80: [View Article]
     [Google Scholar]
  124. Catchpowle J, Maynard J, Chang BJ, Payne MS, Beeton ML et al. Miniscule mollicutes: current hurdles to bacteriophage identification. Sustainable Microbiology 2024; 1: [View Article]
     [Google Scholar]
  125. Marais A, Bove JM, Renaudin J. Characterization of the recA gene regions of Spiroplasma citri and Spiroplasma melliferum. J Bacteriol 1996; 178:7003–7009 [View Article] [PubMed]
     [Google Scholar]
  126. Paredes JC, Herren JK, Schüpfer F, Marin R, Claverol S et al. Genome sequence of the Drosophila melanogaster male-killing Spiroplasma strain MSRO endosymbiont. mBio 2015; 6:02437–14 [View Article] [PubMed]
     [Google Scholar]
  127. Tellis MB, Kotkar HM, Joshi RS. Regulation of trehalose metabolism in insects: from genes to the metabolite window. Glycobiology 2023; 33:262–273 [View Article] [PubMed]
     [Google Scholar]
  128. Smith JL. The physiological role of ferritin-like compounds in bacteria. Crit Rev Microbiol 2004; 30:173–185 [View Article] [PubMed]
     [Google Scholar]
  129. Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B et al. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 2009; 5:e1000630 [View Article] [PubMed]
     [Google Scholar]
  130. Marra A, Masson F, Lemaitre B. The iron transporter Transferrin 1 mediates homeostasis of the endosymbiotic relationship between Drosophila melanogaster and Spiroplasma poulsonii. Microlife 2021; 2:uqab008 [View Article] [PubMed]
     [Google Scholar]
  131. Hutchence KJ, Fischer B, Paterson S, Hurst GDD. How do insects react to novel inherited symbionts? A microarray analysis of Drosophila melanogaster response to the presence of natural and introduced Spiroplasma. Mol Ecol 2011; 20:950–958 [View Article] [PubMed]
     [Google Scholar]
  132. Arai H, Legeai F, Kageyama D, Sugio A, Simon J-C. Genomic insights into Spiroplasma endosymbionts that induce male-killing and protective phenotypes in the pea aphid. FEMS Microbiol Lett 2024; 371:fnae027 [View Article] [PubMed]
     [Google Scholar]
  133. Higareda Alvear VM, Mateos M, Cortez D, Tamborindeguy C, Martinez-Romero E. Differential gene expression in a tripartite interaction: Drosophila, Spiroplasma and parasitic wasps. PeerJ 2021; 9: [View Article]
     [Google Scholar]
  134. Mateos M, Silva NO, Ramirez P, Higareda-Alvear VM, Aramayo R et al. Effect of heritable symbionts on maternally-derived embryo transcripts. Sci Rep 2019; 9:8847 [View Article] [PubMed]
     [Google Scholar]
  135. Liu P, Li Y, Ye Y, Chen J, Li R et al. The genome and antigen proteome analysis of Spiroplasma mirum. Front Microbiol 2022; 13:996938 [View Article]
     [Google Scholar]
  136. Walsh MJ, Dodd JE, Hautbergue GM. Ribosome-inactivating proteins: potent poisons and molecular tools. Virulence 2013; 4:774–784 [View Article] [PubMed]
     [Google Scholar]
  137. Stirpe F. Ribosome-inactivating proteins. Toxicon 2004; 44:371–383 [View Article] [PubMed]
     [Google Scholar]
  138. Ruhe ZC, Low DA, Hayes CS. Polymorphic toxins and their immunity proteins: diversity, evolution, and mechanisms of delivery. Annu Rev Microbiol 2020; 74:497–520 [View Article] [PubMed]
     [Google Scholar]
  139. Chen CK-M, Chan N-L, Wang AH-J. The many blades of the β-propeller proteins: conserved but versatile. Trends Biochem Sci 2011; 36:553–561 [View Article] [PubMed]
     [Google Scholar]
  140. Jernigan KK, Bordenstein SR. Ankyrin domains across the tree of life. PeerJ 2014; 2:e264 [View Article] [PubMed]
     [Google Scholar]
  141. Ernst S, Ecker F, Kaspers MS, Ochtrop P, Hedberg C et al. Legionella effector AnkX displaces the switch II region for Rab1b phosphocholination. Sci Adv 2020; 6:eaaz8041 [View Article] [PubMed]
     [Google Scholar]
  142. Cihlova B, Lu Y, Mikoč A, Schuller M, Ahel I. Specificity of DNA ADP-ribosylation reversal by NADARs. Toxins 2024; 16:208 [View Article] [PubMed]
     [Google Scholar]
  143. Simon NC, Aktories K, Barbieri JT. Novel bacterial ADP-ribosylating toxins: structure and function. Nat Rev Microbiol 2014; 12:599–611 [View Article] [PubMed]
     [Google Scholar]
  144. Tremblay O, Thow Z, Merrill AR. Several new putative bacterial adp-ribosyltransferase toxins are revealed from in silico data mining, including the novel toxin vorin, encoded by the fire blight pathogen Erwinia amylovora. Toxins 2020; 12:792 [View Article] [PubMed]
     [Google Scholar]
  145. Brown EM, Arellano-Santoyo H, Temple ER, Costliow ZA, Pichaud M et al. Gut microbiome ADP-ribosyltransferases are widespread phage-encoded fitness factors. Cell Host Microbe 2021; 29:1351–1365 [View Article] [PubMed]
     [Google Scholar]
  146. Aravind L, Zhang D, de Souza RF, Anand S, Iyer LM. The natural history of ADP-ribosyltransferases and the ADP-ribosylation system. Curr Top Microbiol Immunol 2015; 384:3–32 [View Article] [PubMed]
     [Google Scholar]
  147. Killiny N, Castroviejo M, Saillard C. Spiroplasma citri spiralin acts in vitro as a lectin binding to glycoproteins from its insect vector Circulifer haematoceps. Phytopathology 2005; 95:541–548 [View Article] [PubMed]
     [Google Scholar]
  148. Duret S, Berho N, Danet J-L, Garnier M, Renaudin J. Spiralin is not essential for helicity, motility, or pathogenicity but is required for efficient transmission of Spiroplasma citri by its leafhopper vector Circulifer haematoceps. Appl Environ Microbiol 2003; 69:6225–6234 [View Article] [PubMed]
     [Google Scholar]
  149. Masson F, Rommelaere S, Schüpfer F, Boquete J-P, Lemaitre B. Disproportionate investment in Spiralin B production limits in-host growth and favors the vertical transmission of Spiroplasma insect endosymbionts. Proc Natl Acad Sci USA 2022; 119:e2208461119 [View Article] [PubMed]
     [Google Scholar]
  150. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001408
Loading
Diverse toxin repertoire but limited metabolic capacities inferred from the draft genome assemblies of three Spiroplasma (Citri clade) strains associated with Drosophila
M Gen 11, 001408 (2025); https://doi.org/10.1099/mgen.0.001408
/content/journal/mgen/10.1099/mgen.0.001408
/content/journal/mgen/10.1099/mgen.0.001408
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

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