Biology:Arsenophonus

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Arsenophonus is a genus of Morganellaceae, of the Gammaproteobacteria.[1] Members of the Arsenophonus genus are increasingly discovered bacterial symbionts of arthropods that are estimated to infect over 5% of arthropod species globally [2] and form a variety of relationships with hosts across the mutualism parasitism continuum. Arsenophonus bacteria have been identified in a diversity of insect taxa, including economically important species such as the Western honey bee[3][4] and the rice pest Nilaparvata lugens.[5]

The majority of work on Arsenophonus has been done on the type species Arsenophonus nasoniae for which genetic manipulation has been successful in achieving in vivo tracking of the bacterium.[6] Arsenophonus nasoniae infects Nasonia parasitic wasps,[7][8] is vertically transmitted, passed from a female wasp to the fly host during parasitisation, and then acquired by her hatching larvae feeding on the microbe.[9] It has a male-killing phenotype. Infection with Arsenophonus nasoniae triggers the death of approximately 80% of the wasps male offspring.[10][11] Killing male offspring is thought to facilitate the spread of Arsenophonus through the host population as it releases more resources to female offspring, and it is the female line that Arsenophonus is transmitted through.[12][13] However, horizontal transmission during superparasitism of a single fly pupae by multiple wasp females is required for symbiont spread.[14]

Within the genus a number of Arsenophonus strains have known roles as mutualistic endosymbionts.[15] In both Pediculus humanus[16] and Lipoptena cervi [17] Arsenophonus symbionts are essential to host functioning and are involved in vitamin synthesis, and are vertically transmitted across host generations. In other hosts Arsenophonus is suspected to be parasitic and infection acquired through the environment. In the Western honey bee Arsenophonus can be horizontally transmitted via social behaviour,[4] and the presence of Arsenophonus in a colony has been linked to poor bee health.[18][19] This species has been formally described as Arsenophonus apicola.[20] Arsenophonus apicola can also infect Galleria mellonella waxworms both through injection and orally, indicating it can also develop associations with honey bee associated taxa.[21] The majority of associations between Arsenophonus and host taxa remain uncharacterized.

The diversity of interactions between Arsenophonus and insects has led to the genus being adopted, alongside Sodalis, as one where it is possible to investigate the genetic and evolutionary changes associated with different types of symbiosis. Siozios et al[22] demonstrated early stages of transition to vertical (parent-offspring) transmission were associated with increases in Arsenophonus genome size, associated with proliferation of prophage. This was considered a consequence of loss of CRISPR-Cas defences, hypothesized to be driven by reduce phage predation rates in strongly host associated endosymbionts. Indeed, Arsenophonus nasoniae has one of the more complex microbial genomes, carrying over 50 prophage elements and 17 plasmids.[23]

References

  1. ↑ Gherna, Robert L. (1991). "NOTES: Arsenophonus nasoniae gen. nov., sp. nov., the Causative Agent of the Son-Killer Trait in the Parasitic Wasp Nasonia vitripennis". International Journal of Systematic Bacteriology 41 (4): 563–565. doi:10.1099/00207713-41-4-563. 
  2. ↑ Duron, Olivier; Bouchon, Didier; Boutin, Sébastien; Bellamy, Lawrence; Zhou, Liqin; Engelstädter, Jan; Hurst, Gregory D. (2008-06-24). "The diversity of reproductive parasites among arthropods: Wolbachiado not walk alone". BMC Biology 6 (1): 27. doi:10.1186/1741-7007-6-27. ISSN 1741-7007. PMID 18577218. 
  3. ↑ Yañez, Orlando (2016). "Endosymbiotic bacteria in honey bees: Arsenophonus spp. are not transmitted transovarially". FEMS Microbiology Letters 363 (14). doi:10.1093/femsle/fnw147. PMID 27279628. PMC 4941583. https://academic.oup.com/femsle/article/363/14/fnw147/2570324. 
  4. ↑ 4.0 4.1 Drew, Georgia C.; Budge, Giles E.; Frost, Crystal L.; Neumann, Peter; Siozios, Stefanos; Yañez, Orlando; Hurst, Gregory D. D. (October 2021). "Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts" (in en). The ISME Journal 15 (10): 2956–2968. doi:10.1038/s41396-021-00977-z. ISSN 1751-7370. PMID 33941888. Bibcode: 2021ISMEJ..15.2956D. 
  5. ↑ Fan, Hai-Wei; Lu, Jia-Bao; Ye, Yu-Xuan; Yu, Xiao-Ping; Zhang, Chuan-Xi (2016). "Characteristics of the draft genome of "Candidatus Arsenophonus nilaparvatae", a facultative endosymbiont of Nilaparvata lugens" (in en). Insect Science 23 (3): 478–486. doi:10.1111/1744-7917.12318. ISSN 1744-7917. PMID 26792263. Bibcode: 2016InsSc..23..478F. https://onlinelibrary.wiley.com/doi/abs/10.1111/1744-7917.12318. 
  6. ↑ Nadal-Jimenez, Pol; Griffin, Joanne S.; Davies, Lianne; Frost, Crystal L.; Marcello, Marco; Hurst, Gregory D. D. (2019). "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" (in en). Environmental Microbiology 21 (8): 3172–3182. doi:10.1111/1462-2920.14724. ISSN 1462-2920. PMID 31237728. Bibcode: 2019EnvMi..21.3172N. 
  7. ↑ Huger, AM; Skinner, SW; Werren, JH (1985). "Bacterial infections associated with the son-killer trait in the parasitoid wasp Nasonia (= Mormoniella) vitripennis (Hymenoptera: Pteromalidae)". Journal of Invertebrate Pathology 46 (3): 272–80. doi:10.1016/0022-2011(85)90069-2. PMID 4067323. Bibcode: 1985JInvP..46..272H. 
  8. ↑ Cite error: Invalid <ref> tag; no text was provided for refs named Arsenophonus
  9. ↑ Nadal-Jimenez, Pol; Griffin, Joanne S.; Davies, Lianne; Frost, Crystal L.; Marcello, Marco; Hurst, Gregory D. D. (August 2019). "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". Environmental Microbiology 21 (8): 3172–3182. doi:10.1111/1462-2920.14724. PMID 31237728. Bibcode: 2019EnvMi..21.3172N. 
  10. ↑ Werren, J. H.; Skinner, S. W.; Huger, A. M. (1986-02-28). "Male-killing bacteria in a parasitic wasp". Science 231 (4741): 990–992. doi:10.1126/science.3945814. ISSN 0036-8075. PMID 3945814. Bibcode: 1986Sci...231..990W. 
  11. ↑ Ferree, Patrick M.; Avery, Amanda; Azpurua, Jorge; Wilkes, Timothy; Werren, John H. (2008-09-23). "A Bacterium Targets Maternally Inherited Centrosomes to Kill Males in Nasonia". Current Biology 18 (18): 1409–1414. doi:10.1016/j.cub.2008.07.093. ISSN 0960-9822. PMID 18804376. Bibcode: 2008CBio...18.1409F. 
  12. ↑ Engelstädter, Jan; Hurst, Gregory D. D. (January 2007). "The Impact of Male-Killing Bacteria on Host Evolutionary Processes". Genetics 175 (1): 245–254. doi:10.1534/genetics.106.060921. ISSN 0016-6731. PMID 17151259. 
  13. ↑ Hurst, Gregory D. D.; Majerus, Michael E. N. (July 1993). "Why do maternally inherited microorganisms kill males?" (in en). Heredity 71 (1): 81–95. doi:10.1038/hdy.1993.110. ISSN 1365-2540. 
  14. ↑ Parratt, Steven R.; Frost, Crystal L.; Schenkel, Martijn A.; Rice, Annabel; Hurst, Gregory D. D.; King, Kayla C. (20 June 2016). "Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp". PLOS Pathogens 12 (6). doi:10.1371/journal.ppat.1005629. PMID 27322651. 
  15. ↑ Nováková, E.; Hypša, V.; Moran, A. (2009). "Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution". BMC Microbiology 9: 143. doi:10.1186/1471-2180-9-143. PMID 19619300. 
  16. ↑ Perotti, M. Alejandra; Allen, Julie M.; Reed, David L.; Braig, Henk R. (April 2007). "Host-symbiont interactions of the primary endosymbiont of human head and body lice". FASEB Journal 21 (4): 1058–1066. doi:10.1096/fj.06-6808com. ISSN 1530-6860. PMID 17227954. 
  17. ↑ Nováková, Eva; Hypša, Václav; Nguyen, Petr; Husník, Filip; Darby, Alistair C. (2016-09-17). "Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae)". Standards in Genomic Sciences 11 (1): 72. doi:10.1186/s40793-016-0195-1. ISSN 1944-3277. PMID 27660670. Bibcode: 2016SGenS..11...72N. 
  18. ↑ Budge, Giles E.; Adams, Ian; Thwaites, Richard; Pietravalle, Stéphane; Drew, Georgia C.; Hurst, Gregory D. D.; Tomkies, Victoria; Boonham, Neil et al. (November 2016). "Identifying bacterial predictors of honey bee health". Journal of Invertebrate Pathology 141: 41–44. doi:10.1016/j.jip.2016.11.003. ISSN 1096-0805. PMID 27818181. Bibcode: 2016JInvP.141...41B. https://eprint.ncl.ac.uk/fulltext.aspx?url=231506/C74DA6E5-0C59-4065-B8D7-4B02E7333EE6.pdf&pub_id=231506. 
  19. ↑ Cornman, R. Scott; Tarpy, David R.; Chen, Yanping; Jeffreys, Lacey; Lopez, Dawn; Pettis, Jeffery S.; vanEngelsdorp, Dennis; Evans, Jay D. (2012-08-21). "Pathogen Webs in Collapsing Honey Bee Colonies" (in en). PLOS ONE 7 (8). doi:10.1371/journal.pone.0043562. ISSN 1932-6203. PMID 22927991. Bibcode: 2012PLoSO...743562C. 
  20. ↑ Nadal-Jimenez, Pol; Siozios, Stefanos; Frost, Crystal L.; Court, Rebecca; Chrostek, Ewa; Drew, Georgia C.; Evans, Jay D.; Hawthorne, David J. et al. (2022-08-03). "Arsenophonus apicola sp. nov., isolated from the honeybee Apis mellifera" (in en). International Journal of Systematic and Evolutionary Microbiology 72 (8). doi:10.1099/ijsem.0.005469. ISSN 1466-5026. PMID 35930469. 
  21. ↑ Simmons, Trefor; Nadal-Jimenez, Pol; Hurst, Gregory D. D. (2025). "The Honeybee Associate Galleria mellonella Can Acquire Arsenophonus apicola Through Oral and Parenteral Infection Routes" (in en). Environmental Microbiology 27 (4). doi:10.1111/1462-2920.70088. ISSN 1462-2920. 
  22. ↑ Siozios, Stefanos; Nadal-Jimenez, Pol; Azagi, Tal; Sprong, Hein; Frost, Crystal L.; Parratt, Steven R.; Taylor, Graeme; Brettell, Laura et al. (2024-12-16). "Genome dynamics across the evolutionary transition to endosymbiosis" (in English). Current Biology 34 (24): 5659–5670.e7. doi:10.1016/j.cub.2024.10.044. ISSN 0960-9822. PMID 39549700. Bibcode: 2024CBio...34.5659S. 
  23. ↑ Frost, Crystal L.; Siozios, Stefanos; Nadal-Jimenez, Pol; Brockhurst, Michael A.; King, Kayla C.; Darby, Alistair C.; Hurst, Gregory D. D. (2020-03-24). "The Hypercomplex Genome of an Insect Reproductive Parasite Highlights the Importance of Lateral Gene Transfer in Symbiont Biology". mBio 11 (2): 10.1128/mbio.02590–19. doi:10.1128/mbio.02590-19. PMID 32209690. 

Further reading

Wikidata ☰ Q16530186 entry



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