Spiroplasma poulsonii

Spiroplasma poulsonii are bacteria of the genus Spiroplasma that are commonly endosymbionts of flies.[1] These bacteria live in the hemolymph (insect blood) of the flies, where they can act as reproductive manipulators or defensive symbionts.

Spiroplasma poulsonii
Scientific classification
Domain: Bacteria
Phylum: Mycoplasmatota
Class: Mollicutes
Order: Mycoplasmatales
Family: Mycoplasmataceae
Genus: Spiroplasma
Species:
S. poulsonii
Binomial name
Spiroplasma poulsonii
Williamson et al. 1999

Biology

Spiroplasma poulsonii is a maternally transmitted symbiont, meaning it is primarily inherited through the female germ line. This involves the co-option of the fly yolk proteins, which allow the symbiont to enter the developing ovary.[2] In the fly hemolymph, S. poulsonii feeds on lipids as its primary food source.[3]

Male-killing

The Drosophila melanogaster S. poulsonii strain MSRO kills D. melanogaster eggs fertilized by Y-bearing sperm.[4] This mode of reproductive manipulation benefits the symbiont as the female fly has a greater reproductive output than males. Thus, by increasing the number of daughters the fly mother produces, the symbiont increases its ability to spread through the increased reproductive output of female flies. Male-killing requires the presence of a functional dosage compensation process in its fly host.[5] The genetic basis of this male-killing was discovered in 2018, and the gene named "SpAID" for "Spiroplasma poulsonii AndrocIDin," in line with previous studies that referred to the then-unknown factor as the S. poulsonii androcidin. SpAID takes advantage of host dosage compensation machinery causing DNA damage to the male X chromosome, leading to a failure of the male X chromosome to organize and model its chromatin structure.[6]

The discovery of SpAID solved a mystery dating back to the 1950s of how the bacteria targeted male-specific cells. In an interview with the Global Health Institute, Dr. Toshiyuki Harumoto said: "To our knowledge, Spaid is the first bacterial effector protein identified to date that affects host cellular machinery in a sex-specific manner...”[6]

Defensive symbiosis

A dissected mushroom-feeding Drosophila infected with Howardula nematodes

The S. poulsonii strain of Drosophila neotestacea can defend its host from attack by nematodes and parasitic wasps.[7] This defence is important enough that S. poulsonii has spread westward across North America due to the selective pressure imposed by the sterilizing nematode parasite Howardula aoronymphium.[8]

The mechanism through which S. poulsonii protects flies from nematodes and parasitic wasps relies on the presence of toxins called ribosome-inactivating proteins (RIPs), similar to sarcin or ricin. These toxins depurinate a conserved adenine site in eukaryotic 28s ribosomal RNA called the Sarcin-Ricin loop by cleaving the N-glycosidic bond between the rRNA backbone and the adenine,[9][10] leaving a signature of RIP attack in nematode and wasp RNA. Spiroplasma poulsonii likely avoids damaging its host fly by carrying parasite-specific complements of RIP toxins encoded on bacterial plasmids. This allows genes for RIP toxins to readily move between species by horizontal gene transfer, as D. neotestacea Spiroplasma RIPs are shared by Spiroplasma of other mushroom-feeding flies, such as Megaselia nigra.[11] The S. poulsonii strain of Drosophila melanogaster can also attack parasitoid wasps, but its impact on survival of the host fly itself is variable, and dependent on wasp species and strain.[12][13]

References

  1. Williamson, D.L. et al, Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly (1999) https://doi.org/10.1099/00207713-49-2-611
  2. Herren, J. K.; Paredes, J. C.; Schupfer, F.; Lemaitre, B. (2013). "Vertical Transmission of a Drosophila Endosymbiont Via Cooption of the Yolk Transport and Internalization Machinery". mBio. 4 (2). doi:10.1128/mBio.00532-12. PMC 3585447. PMID 23462112.
  3. Herren, Jeremy K.; Paredes, Juan C.; Schüpfer, Fanny; Arafah, Karim; Bulet, Philippe; Lemaitre, Bruno (2014). "Insect endosymbiont proliferation is limited by lipid availability". eLife. 3: e02964. doi:10.7554/eLife.02964. PMC 4123717. PMID 25027439.
  4. Montenegro,H et al. Male‐killing Spiroplasma naturally infecting Drosophila melanogaster (2005) https://doi.org/10.1111/j.1365-2583.2005.00558.x}
  5. Veneti, Z et al. A functional dosage compensation complex required for male killing in Drosophila (2005) 10.1126/science.1107182
  6. Harumoto, Toshiyuki; Lemaitre, Bruno (2018). "Male-killing toxin in a bacterial symbiont of Drosophila". Nature. 557 (7704): 252–255. Bibcode:2018Natur.557..252H. doi:10.1038/s41586-018-0086-2. PMC 5969570. PMID 29720654.
  7. Haselkorn, Tamara S.; Jaenike, John (2015). "Macroevolutionary persistence of heritable endosymbionts: Acquisition, retention and expression of adaptive phenotypes in Spiroplasma". Molecular Ecology. 24 (14): 3752–3765. doi:10.1111/mec.13261. PMID 26053523. S2CID 206182327.
  8. Jaenike, J.; Unckless, R.; Cockburn, S. N.; Boelio, L. M.; Perlman, S. J. (2010). "Adaptation via Symbiosis: Recent Spread of a Drosophila Defensive Symbiont". Science. 329 (5988): 212–215. Bibcode:2010Sci...329..212J. doi:10.1126/science.1188235. PMID 20616278. S2CID 206526012.
  9. Hamilton, Phineas T.; Peng, Fangni; Boulanger, Martin J.; Perlman, Steve J. (2016). "A ribosome-inactivating protein in a Drosophiladefensive symbiont". Proceedings of the National Academy of Sciences. 113 (2): 350–355. Bibcode:2016PNAS..113..350H. doi:10.1073/pnas.1518648113. PMC 4720295. PMID 26712000.
  10. Ballinger, Matthew J.; Perlman, Steve J. (2017). "Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila". PLOS Pathogens. 13 (7): e1006431. doi:10.1371/journal.ppat.1006431. PMC 5500355. PMID 28683136.
  11. Ballinger, Matthew J.; Gawryluk, Ryan M R.; Perlman, Steve J. (2018). "Toxin and genome evolution in a Drosophila defensive symbiosis". Genome Biology and Evolution. 11 (1): 253–262. doi:10.1093/gbe/evy272. PMC 6349354. PMID 30576446.
  12. Jones, J.E. & Hurst, G.D.D. Symbiont-mediated protection varies with wasp genotype in the Drosophila melanogaster–Spiroplasma interaction (2015) https://doi.org/10.1038/s41437-019-0291-2
  13. Xie, J.; Butler, S.; Sanchez, G.; Mateos, M. (2014). "Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps". Heredity. 112 (4): 399–408. doi:10.1038/hdy.2013.118. PMC 3966124. PMID 24281548.
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