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Spiroplasma

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Spiroplasma
Corn stunt Spiroplasma in phloem cells. Thick section (0.4 micrometers) observed in a TEM. Magnified 75,000X.
Scientific classification
Domain:
Bacteria
Phylum:
Mycoplasmatota
Class:
Mollicutes
Order:
Mycoplasmatales
Family:
Spiroplasmataceae

Skrypal 1974 ex Skrypal 1983
Genus:
Spiroplasma

Saglio et al. 1973
Type species
Spiroplasma citri
Saglio et al. 1973
Species[1]

Spiroplasma is a genus of Mollicutes, a group of small bacteria without cell walls. Spiroplasma shares the simple metabolism, parasitic lifestyle, fried-egg colony morphology and small genome of other Mollicutes, but has a distinctive helical morphology, unlike Mycoplasma. It has a spiral shape and moves in a corkscrew motion. Many Spiroplasma are found either in the gut or haemolymph of insects where they can act to manipulate host reproduction, or defend the host as endosymbionts. Spiroplasma are also disease-causing agents in the phloem of plants. Spiroplasmas are fastidious organisms, which require a rich culture medium. Typically they grow well at 30 °C, but not at 37 °C. A few species, notably Spiroplasma mirum, grow well at 37 °C (human body temperature), and cause cataracts and neurological damage in suckling mice. The best studied species of spiroplasmas are Spiroplasma poulsonii, a reproductive manipulator and defensive insect symbiont, Spiroplasma citri, the causative agent of citrus stubborn disease, and Spiroplasma kunkelii, the causative agent of corn stunt disease.

Human pathogenicity

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There is some disputed evidence for the role of spiroplasmas in the etiology of transmissible spongiform encephalopathies (TSEs), due primarily to the work of Frank Bastian, summarized below. Other researchers have failed to replicate this work, while the prion model for TSEs has gained very wide acceptance.[2] A 2006 study appears to refute the role of spiroplasmas in the best small animal scrapie model (hamsters).[3] Bastian et al. (2007) have responded to this challenge with the isolation of a spiroplasma species from scrapie-infected tissue, grown it in cell-free culture, and demonstrated its infectivity in ruminants.[4]

Insect symbioses

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Many Spiroplasma strains are vertically transmitted endosymbionts of Drosophila species, with a variety of host-altering mechanisms similar to Wolbachia. These strains are from the Spiroplasma poulsonii clade, and can have important effects on host fitness. The S. poulsonii strain of Drosophila neotestacea protects its host against parasitic nematodes. This interaction is an example of defensive symbiosis, where the fitness of the symbiont is intricately tied to the fitness of the host. The D. neotestacea S. poulsonii also defends its fly host from infestation by parasitic wasps.[5][6] The mechanism through which S. poulsonii attacks nematodes and parasitic wasps relies on the presence of toxins called ribosome-inactivating proteins (RIPs), similar to Sarcin or Ricin.[7] 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.[7] Spiroplasma associations highlight a growing movement to consider heritable symbionts as important drivers in patterns of evolution.[8][9]

The S. poulsonii strain of Drosophila melanogaster can also attack parasitoid wasps, but is not regarded as a primarily defensive symbiont. This is because this D. melanogaster Spiroplasma (called MSRO) kills D. melanogaster eggs fertilized by Y-bearing sperm. This mode of reproductive manipulation benefits the symbiont as the female fly has a greater reproductive output than males. The genetic basis of this male-killing was discovered in 2018, solving a decades-old mystery of how the bacteria targeted male-specific cells.[10] In an interview with the Global Health Institute, Dr. Toshiyuki Harumoto said this discovery is the first example of a bacterial effector protein that affects host cellular machinery in a sex-specific manner, and the first endosymbiont factor identified to explain the cause of male-killing. Thus it should have a big impact on the fields of symbiosis, sex determination, and evolution.[11]

Beyond Drosophila, Spiroplasma of the ixodetis, apis, chrysopicola, citri, mirum, and poulsonii clades are found in many insects and arthropods, including ticks, spiders, bees, ants, beetles, and butterflies.[12][13][1][14] Male-killing is also found in the Spiroplasma of the ladybug Harmonia axyridis and the plain tiger butterfly. In the plain tiger butterfly, the consequences have led to speciation.[15]

Plant diseases

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Spiroplasma citri is the causative agent of Citrus stubborn disease, a plant disease affecting species in the genus Citrus.[16] It infects the phloem of the affected plant, causing fruit deformities. Spiroplasma kunkelii is also referred to as Corn Stunt Spiroplasma as it is the causative agent of Corn stunt disease, a disease of corn and other grasses that stunts plant growth. Spiroplasma kunkelii represents a major economic risk, as corn production in the United States is an industry worth over $50 billion.[17] Both Spiroplasma citri and Spiroplasma kunkelii are transmitted by leafhoppers.[18][19]

Phylogeny

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The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN)[20] and National Center for Biotechnology Information (NCBI)[21]

16S rRNA based LTP_08_2023[22][23][24] 120 marker proteins based GTDB 08-RS214[25][26][27]

Metamycoplasmataceae

Mycoplasmoidales

Mycoplasmoidaceae

Spiroplasma

Spiroplasma ixodetis Tully et al. 1995

Spiroplasma platyhelix Williamson et al. 1997

species‑group 3
Mycoplasmatales
Spiroplasma

S. eriocheiris Wang et al. 2011

S. atrichopogonis Koerber et al. 2005

S. mira corrig. Tully et al. 1982

S. chrysopicola Whitcomb et al. 1997

S. syrphidicola Whitcomb et al. 1996

S. insolita corrig. Hackett et al. 1993

S. penaei Nunan et al. 2005

S. leucomae Oduori, Lipa & Gasparich 2005

S. poulsonii Williamson et al. 1999

S. phoenicea corrig. Saillard et al. 1987

S. kunkelii Whitcomb et al. 1986

S. citri Saglio et al. 1973

S. mellifera corrig. Clark et al. 1985

Spiroplasmataceae
Spiroplasma

Spiroplasma alleghenense

Spiroplasma sabaudiense

Spiroplasma lampyridicola

Spiroplasma leptinotarsae

Spiroplasma clarkii

Spiroplasma apis

Spiroplasma montanense

Spiroplasma taiwanense

Spiroplasma monobiae

Spiroplasma cantharicola

Spiroplasma diminutum

Spiroplasma floricola

Spiroplasma diabroticae

Mesoplasma melaleucae

Spiroplasma culicicola

Spiroplasma chinense

Spiroplasma velocicrescens

Spiroplasma litorale

Spiroplasma corruscae

Spiroplasma turonicum

Spiroplasma helicoides

Spiroplasma gladiatoris

Spiroplasma lineolae

Spiroplasma tabanidicola

species‑group 2

"Ca. Spiroplasma holothuricola" He et al. 2018

Mycoplasmoidaceae

VBWQ01
Spiroplasma

Spiroplasma ixodetis

Spiroplasma platyhelix

species‑group 3
Mycoplasmataceae
Spiroplasma

S. eriocheiris

S. mira

S. chrysopicola

S. syrphidicola

S. poulsonii

S. phoenicea

S. citri

S. mellifera

Spiroplasma

Spiroplasma alleghenense

Spiroplasma sabaudiense

Spiroplasma turonica

Spiroplasma corruscae

Spiroplasma litorale

Spiroplasma taiwanense

Spiroplasma cantharicola

Spiroplasma diminuta

Spiroplasma floricola

Spiroplasma monobiae

Spiroplasma apis

Spiroplasma clarkii

Spiroplasma culicicola

Spiroplasma chinense

Spiroplasma helicoides

Spiroplasma gladiatoris

Spiroplasma tabanidicola

species‑group 2

See also

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References

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  1. ^ a b Ballinger, Matthew J.; Moore, Logan D.; Perlman, Steve J.; Stabb, Eric V. (31 January 2018). "Evolution and Diversity of Inherited Spiroplasma Symbionts in Myrmica Ants". Applied and Environmental Microbiology. 84 (4). Bibcode:2018ApEnM..84E2299B. doi:10.1128/AEM.02299-17. PMC 5795062. PMID 29196290.
  2. ^ Leach, R.H.; Matthews, W.B.; Will, R. (June 1983). "Creutzfeldt-Jakob disease". Journal of the Neurological Sciences. 59 (3): 349–353. doi:10.1016/0022-510x(83)90020-5. PMID 6348215. S2CID 3558955.
  3. ^ Alexeeva, I.; Elliott, E. J.; Rollins, S.; Gasparich, G. E.; Lazar, J.; Rohwer, R. G. (3 January 2006). "Absence of Spiroplasma or Other Bacterial 16S rRNA Genes in Brain Tissue of Hamsters with Scrapie". Journal of Clinical Microbiology. 44 (1): 91–97. doi:10.1128/JCM.44.1.91-97.2006. PMC 1351941. PMID 16390954.
  4. ^ Bastian, Frank O.; Sanders, Dearl E.; Forbes, Will A.; Hagius, Sue D.; Walker, Joel V.; Henk, William G.; Enright, Fred M.; Elzer, Philip H. (1 September 2007). "Spiroplasma spp. from transmissible spongiform encephalopathy brains or ticks induce spongiform encephalopathy in ruminants". Journal of Medical Microbiology. 56 (9): 1235–1242. doi:10.1099/jmm.0.47159-0. PMID 17761489.
  5. ^ Jaenike, J.; Unckless, R.; Cockburn, S. N.; Boelio, L. M.; Perlman, S. J. (8 July 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.
  6. ^ Haselkorn, Tamara S.; Jaenike, John (July 2015). "Macroevolutionary persistence of heritable endosymbionts: acquisition, retention and expression of adaptive phenotypes in". Molecular Ecology. 24 (14): 3752–3765. doi:10.1111/mec.13261. PMID 26053523. S2CID 206182327.
  7. ^ a b Ballinger, Matthew J.; Perlman, Steve J.; Hurst, Greg (6 July 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.
  8. ^ Jaenike, John; Stahlhut, Julie K.; Boelio, Lisa M.; Uncless, Robert L. (January 2010). "Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism?". Molecular Ecology. 19 (2): 414–425. Bibcode:2010MolEc..19..414J. doi:10.1111/j.1365-294X.2009.04448.x. PMID 20002580. S2CID 46063874.
  9. ^ Koch, Hauke; Schmid-Hempel, Paul (29 November 2011). "Socially transmitted gut microbiota protect bumble bees against an intestinal parasite". Proceedings of the National Academy of Sciences of the United States of America. 108 (48): 19288–19292. Bibcode:2011PNAS..10819288K. doi:10.1073/pnas.1110474108. PMC 3228419. PMID 22084077.
  10. ^ Harumoto, Toshiyuki; Lemaitre, Bruno (May 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.
  11. ^ Papageorgiou, Nik (5 July 2018). "Mystery solved: The bacterial protein that kills male fruit flies".
  12. ^ Duron, Olivier; Bouchon, Didier; Boutin, Sébastien; Bellamy, Lawrence; Zhou, Liqin; Engelstädter, Jan; Hurst, Gregory D. (24 June 2008). "The diversity of reproductive parasites among arthropods: Wolbachiado not walk alone". BMC Biology. 6 (1): 27. doi:10.1186/1741-7007-6-27. PMC 2492848. PMID 18577218.
  13. ^ Binetruy, Florian; Bailly, Xavier; Chevillon, Christine; Martin, Oliver Y.; Bernasconi, Marco V.; Duron, Olivier (1 April 2019). "Phylogenetics of the Spiroplasma ixodetis endosymbiont reveals past transfers between ticks and other arthropods". Ticks and Tick-borne Diseases. 10 (3): 575–584. doi:10.1016/j.ttbdis.2019.02.001. PMID 30744948.
  14. ^ Tsushima, Yusuke; Nakamura, Kayo; Tagami, Yohsuke; Miura, Kazuki (April 2015). "Mating rates and the prevalence of male-killing Spiroplasma in Harmonia axyridis (Coleoptera: Coccinellidae)". Entomological Science. 18 (2): 217–220. doi:10.1111/ens.12113. S2CID 83582284.
  15. ^ Jiggins, F. M.; Hurst, G. D. D.; Jiggins, C. D.; Schulenburg, J. H. G. v d; Majerus, M. E. N. (2000). "The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium". Parasitology. 120 (5): 439–446. doi:10.1017/S0031182099005867. PMID 10840973. S2CID 34436795.
  16. ^ Yokomi, Raymond K.; Mello, Alexandre F. S.; Saponari, Maria; Fletcher, Jacqueline (February 2008). "Polymerase Chain Reaction-Based Detection of Spiroplasma citri Associated with Citrus Stubborn Disease". Plant Disease. 92 (2): 253–260. doi:10.1094/PDIS-92-2-0253. PMID 30769379.
  17. ^ "Use of Spectral Vegetation Indices for Detection of European Corn Borer Infestation in Iowa Corn Plots | Science Inventory | US EPA". Cfpub.epa.gov. Retrieved 2019-02-12.
  18. ^ Bové, Joseph M.; Renaudin, Joël; Saillard, Colette; Foissac, Xavier; Garnier, Monique (2003). "Spiroplasma citri, a Plant Pathogenic Mollicute: Relationships with Its Two Hosts, the Plant and the Leafhopper Vector". Annual Review of Phytopathology. 41 (1): 483–500. doi:10.1146/annurev.phyto.41.052102.104034. ISSN 0066-4286. PMID 12730387.
  19. ^ Özbek, Elvan; Miller, Sally A; Meulia, Tea; Hogenhout, Saskia A (2003-03-01). "Infection and replication sites of Spiroplasma kunkelii (Class: Mollicutes) in midgut and Malpighian tubules of the leafhopper Dalbulus maidis". Journal of Invertebrate Pathology. 82 (3): 167–175. doi:10.1016/S0022-2011(03)00031-4. ISSN 0022-2011. PMID 12676553.
  20. ^ A.C. Parte; et al. "Spiroplasmataceae". List of Prokaryotic names with Standing in Nomenclature (LPSN). Retrieved 2022-09-09.
  21. ^ Sayers; et al. "Spiroplasmataceae". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2022-09-09.
  22. ^ "The LTP". Retrieved 20 November 2023.
  23. ^ "LTP_all tree in newick format". Retrieved 20 November 2023.
  24. ^ "LTP_08_2023 Release Notes" (PDF). Retrieved 20 November 2023.
  25. ^ "GTDB release 08-RS214". Genome Taxonomy Database. Retrieved 10 May 2023.
  26. ^ "bac120_r214.sp_label". Genome Taxonomy Database. Retrieved 10 May 2023.
  27. ^ "Taxon History". Genome Taxonomy Database. Retrieved 10 May 2023.
  28. ^ Ramírez, A. S.; Rosas, A.; Hernández-Beriain, J. A.; Orengo, J. C.; Saavedra, P.; de la Fe, C.; Fernández, A.; Poveda, J. B. (July 2005). "Relationship between rheumatoid arthritis and Mycoplasma pneumoniae: a case–control study". Rheumatology. 44 (7): 912–914. doi:10.1093/rheumatology/keh630. PMID 15814575.
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