Skip to content
1887

Abstract

The genus has been traditionally considered to comprise heritable bacterial symbionts of arthropods. Recent work has reported a microbe related to the type species as infecting the honey bee, . The association was unusual for members of the genus in that the microbe–host interaction arose through environmental and social exposure rather than vertical transmission. In this study, we describe the culture of ArsBeeUS, a strain of this microbe isolated from in the USA. The 16S rRNA sequence of the isolated strain indicates it falls within the genus . Biolog analysis indicates the bacterium has a restricted range of nutrients that support growth. experiments demonstrate the strain proliferates rapidly on injection into hosts. We further report the closed genome sequence for the strain. The genome is 3.3 Mb and the G+C content is 37.6 mol%, which is smaller than but larger than the genomes reported for non-culturable symbionts. The genome is complex, with six extrachromosomal elements and 11 predicted intact phage elements, but notably less complex than . Strain ArsBeeUS is clearly distinct from the type species on the basis of genome sequence, with 92 % average nucleotide identity. Based on our results, we propose sp. nov., with the type strain ArsBeeUS (CECT 30499=DSM113403=LMG 32504).

  • 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.0.005469
2022-08-05
2025-03-21
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/72/8/ijsem005469.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.005469&mimeType=html&fmt=ahah

References

  1. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 2013; 110:3229–3236 [View Article] [PubMed]
    [Google Scholar]
  2. Bright M, Bulgheresi S. A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 2010; 8:218–230 [View Article] [PubMed]
    [Google Scholar]
  3. Perlmutter JI, Bordenstein SR. Microorganisms in the reproductive tissues of arthropods. Nat Rev Microbiol 2020; 18:97–111 [View Article] [PubMed]
    [Google Scholar]
  4. Leeks A, Dos Santos M, West SA. Transmission, relatedness, and the evolution of cooperative symbionts. J Evol Biol 2019; 32:1036–1045 [View Article] [PubMed]
    [Google Scholar]
  5. Werren JH, Skinner SW, Huger AM. Male-killing bacteria in a parasitic wasp. Science 1986; 231:990–992 [View Article] [PubMed]
    [Google Scholar]
  6. Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR et al. Notes: Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol 1991; 41:563–565 [View Article]
    [Google Scholar]
  7. Nadal-Jimenez P, Griffin JS, Davies L, Frost CL, Marcello M et al. Genetic manipulation allows in vivo tracking of the life cycle of the son-killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology. Environ Microbiol 2019; 21:3172–3182 [View Article] [PubMed]
    [Google Scholar]
  8. Skinner SW. Son-killer: a third extrachromosomal factor affecting the sex ratio in the parasitoid wasp, Nasonia (=Mormoniella) vitripennis. Genetics 1985; 109:745–759 [View Article] [PubMed]
    [Google Scholar]
  9. Parratt SR, Frost CL, Schenkel MA, Rice A, Hurst GDD et al. Superparasitism drives heritable symbiont epidemiology and host sex ratio in a wasp. PLoS Pathog 2016; 12:e1005629 [View Article] [PubMed]
    [Google Scholar]
  10. Frost CL, Siozios S, Nadal-Jimenez P, Brockhurst MA, King KC et al. The hypercomplex genome of an insect reproductive parasite highlights the importance of lateral gene transfer in symbiont biology. mBio 2020; 11:e02590-19 [View Article] [PubMed]
    [Google Scholar]
  11. Hypsa V, Dale C. In vitro culture and phylogenetic analysis of “Candidatus Arsenophonus triatominarum,” an intracellular bacterium from the triatomine bug, Triatoma infestans. Int J Syst Bacteriol 1997; 47:1140–1144 [View Article] [PubMed]
    [Google Scholar]
  12. Dale C, Beeton M, Harbison C, Jones T, Pontes M. Isolation, pure culture, and characterization of “Candidatus Arsenophonus arthropodicus,” an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 2006; 72:2997–3004 [View Article] [PubMed]
    [Google Scholar]
  13. Allen JM, Reed DL, Perotti MA, Braig HR. Evolutionary relationships of “Candidatus Riesia spp.,” endosymbiotic enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol 2007; 73:1659–1664 [View Article] [PubMed]
    [Google Scholar]
  14. Zreik L, Bové JM, Garnier M. Phylogenetic characterization of the bacterium-like organism associated with marginal chlorosis of strawberry and proposition of a Candidatus taxon for the organism, “Candidatus Phlomobacter fragariae.”. Int J Syst Bacteriol 1998; 48 Pt 1:257–261 [View Article]
    [Google Scholar]
  15. Danet J-L, Foissac X, Zreik L, Salar P, Verdin E et al. Candidatus Phlomobacter fragariae” is the prevalent agent of marginal chlorosis of strawberry in Is the Prevalent Agent of Marginal Chlorosis of Strawberry in French production fields and is transmitted by the planthopperProduction Fields and Is Transmitted by the Planthopper Cixius wagneri (China). Phytopathology 2003; 93:644–649 [View Article]
    [Google Scholar]
  16. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol 2007; 59:600–610 [View Article] [PubMed]
    [Google Scholar]
  17. Aizenberg-Gershtein Y, Izhaki I, Halpern M. Do honeybees shape the bacterial community composition in floral nectar?. PLOS ONE 2013; 8:e67556 [View Article] [PubMed]
    [Google Scholar]
  18. Corby-Harris V, Maes P, Anderson KE. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLOS ONE 2014; 9:e95056 [View Article] [PubMed]
    [Google Scholar]
  19. Yañez O, Gauthier L, Chantawannakul P, Neumann P. Endosymbiotic bacteria in honey bees: Arsenophonus spp. are not transmitted transovarially. FEMS Microbiol Lett 2016; 363:fnw147 [View Article] [PubMed]
    [Google Scholar]
  20. Drew GC, Budge GE, Frost CL, Neumann P, Siozios S et al. Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts. ISME J 2021; 15:2956–2968 [View Article] [PubMed]
    [Google Scholar]
  21. Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D et al. Pathogen webs in collapsing honey bee colonies. PLOS ONE 2012; 7:e43562 [View Article] [PubMed]
    [Google Scholar]
  22. Budge GE, Adams I, Thwaites R, Pietravalle S, Drew GC et al. Identifying bacterial predictors of honey bee health. J Invertebr Pathol 2016; 141:41–44 [View Article] [PubMed]
    [Google Scholar]
  23. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article] [PubMed]
    [Google Scholar]
  24. Stackebrandt E, Liesack W. Nucleic acids and classification. In Goodfellow M, O’Donnell A. eds Handbook of New Bacterial Systematics London, England: Academic Press; 1993 pp 152–189
    [Google Scholar]
  25. Nawrocki EP. Structural RNA Homology Search and Alignment using Covariance Models [PhD] Washington University in Saint Louis; 2009
    [Google Scholar]
  26. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. 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]
  29. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007; 23:127–128 [View Article] [PubMed]
    [Google Scholar]
  30. Gómez-Gómez J-M, Manfredi C, Alonso J-C, Blázquez J. A novel role for RecA under non-stress: promotion of swarming motility in Escherichia coli K-12. BMC Biol 2007; 5:14 [View Article] [PubMed]
    [Google Scholar]
  31. Basset A, Tzou P, Lemaitre B, Boccard F. A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep 2003; 4:205–209 [View Article]
    [Google Scholar]
  32. Quick JJ. Ultra-long read sequencing protocol for RAD004; 2018 https://dx.doi.org/10.17504/protocols.io.mrxc57n
  33. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  34. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLOS ONE 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  35. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI Prokaryotic Genome Annotation Pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  36. Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 2000; 28:27–30 [View Article] [PubMed]
    [Google Scholar]
  37. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–21 [View Article] [PubMed]
    [Google Scholar]
  38. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 2015; 16:157 [View Article] [PubMed]
    [Google Scholar]
  39. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016 [View Article]
    [Google Scholar]
  40. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  41. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019; 36:1925–1927 [View Article] [PubMed]
    [Google Scholar]
  42. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article] [PubMed]
    [Google Scholar]
  43. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: The United States Department of Energy Systems Biology Knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article] [PubMed]
    [Google Scholar]
  44. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  45. Hirschmann M, Grundmann F, Bode HB. Identification and occurrence of the hydroxamate siderophores aerobactin, putrebactin, avaroferrin and ochrobactin C as virulence factors from entomopathogenic bacteria. Environ Microbiol 2017; 19:4080–4090 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.005469
Loading
/content/journal/ijsem/10.1099/ijsem.0.005469
Loading

Data & Media loading...

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