Spiroplasma

Last updated

Spiroplasma
Spiro.jpg
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.

Contents

Human pathogenicity

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

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. neotestaceaS. 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] . Protection against wasp attack can be thermally sensitive, ablated at lower environmental temperatures [10] [11] .

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. melanogasterSpiroplasma (called MSRO) kills D. melanogaster eggs fertilized by Y-bearing sperm [12] . This mode of reproductive manipulation benefits the symbiont as the female fly has a greater reproductive output than males. Work by Veneti and colleagues [13] demonstrated that male-killing was ablated by loss of function of any gene in the dosage compensation complex (DCC), leading to the hypothesis that the target of male-killing was the single X chromosome of males, and enabled by the DCC binding to this chromosome. Work in D. nebulosa demonstrated male death was associated with widespread apoptosis in male embryos during mid/late embryogenesis [14] . The genetic basis of this male-killing was discovered in 2018, solving a decades-old mystery of how the bacteria targeted male-specific cells. [15] 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. [16]

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. [17] [18] [1] [19] Male-killing is also found in the Spiroplasma of the ladybird beetles Adalia bipunctata [20] and Harmonia axyridis [21] , the plain tiger butterfly, the lacewing Mallada desjadinisi [22] , and the pea aphid Acyrthosiphum pisum. In the plain tiger butterfly, the consequences have led to speciation. [23]

Plant diseases

Spiroplasma citri is the causative agent of Citrus stubborn disease, a plant disease affecting species in the genus Citrus . [24] 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. [25] Both Spiroplasma citri and Spiroplasma kunkelii are transmitted by leafhoppers. [26] [27]

Genetics and Molecular evolution

Spiroplasma, like other mollicutes, have a distinct genetic code, with two rather than three stop codons [28] . Molecular evolution studies, using Spiroplasma passaged vertically in Drosophila, indicate a very fast rate of molecular evolution [29] . Spiroplasma genomes are commonly extremely AT rich, can contain a variety of prophage (viral) elements, and also plasmids.CRISPR defences are found in some members of the genus [30] . Genome sizes are generally between 0.7 and 2.2 Mb.

Phylogeny

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN) [31] and National Center for Biotechnology Information (NCBI) [32]

16S rRNA based LTP_08_2023 [33] [34] [35] 120 marker proteins based GTDB 08-RS214 [36] [37] [38]

Metamycoplasmataceae

Mycoplasmoidales

Mycoplasmoidaceae

Spiroplasma

Spiroplasma ixodetisTully et al. 1995

Spiroplasma platyhelixWilliamson et al. 1997

species‑group 3
Mycoplasmatales
Spiroplasma

S. eriocheirisWang et al. 2011

S. atrichopogonisKoerber et al. 2005

S. mira corrig. Tully et al. 1982

S. chrysopicolaWhitcomb et al. 1997

S. syrphidicolaWhitcomb et al. 1996

S. insolitacorrig. Hackett et al. 1993

S. penaeiNunan et al. 2005

S. leucomaeOduori, Lipa & Gasparich 2005

S. poulsonii Williamson et al. 1999

S. phoeniceacorrig. Saillard et al. 1987

S. kunkelii Whitcomb et al. 1986

S. citri Saglio et al. 1973

S. melliferacorrig. 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

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of fly, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals, and bacterial endosymbionts that provide essential nutrients to insects.

<i>Wolbachia</i> Genus of bacteria in the Alphaproteobacteria class

Wolbachia is a genus of gram-negative bacteria infecting many species of arthropods and filarial nematodes. The symbiotic relationship ranges from parasitism to obligate mutualism. It is one of the most common parasitic microbes of arthropods, and is possibly the most widespread reproductive parasite bacterium in the biosphere. Its interactions with hosts are complex and highly diverse across different host species. Some host species cannot reproduce, or even survive, without Wolbachia colonisation. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus, and as many as 25 to 70% of all insect species are estimated to be potential hosts.

<i>Adalia bipunctata</i> Species of beetle

Adalia bipunctata, the two-spot ladybird, two-spotted ladybug or two-spotted lady beetle, is a carnivorous beetle of the family Coccinellidae that is found throughout the holarctic region. It is very common in western and central Europe. It is also native to North America but it has heavily declined in many states and provinces. It is commonly introduced and imported as a biological control agent.

Cytoplasmic incompatibility (CI) is a mating incompatibility reported in many arthropod species that is caused by intracellular parasites such as Wolbachia. These bacteria reside in the cytoplasm of the host cells and modify their hosts' sperm in a way that leads to embryo death unless this modification is 'rescued' by the same bacteria in the eggs. CI has been reported in many insect species, as well as in mites and woodlice. Aside from Wolbachia, CI can be induced by the bacteria Cardinium,Rickettsiella, Candidatus Mesenet longicola and Spiroplasma. CI is currently being exploited as a mechanism for Wolbachia-mediated disease control in mosquitoes.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts.

Arsenophonus nasoniae is a species of bacterium which was previously isolated from Nasonia vitripennis, a species of parasitoid wasp. These wasps are generalists which afflict the larvae of parasitic carrion flies such as blowflies, houseflies and flesh flies. A. nasoniae belongs to the phylum Pseudomonadota and family Morganellaceae. The genus Arsenophonus, has a close relationship to the Proteus (bacterium) rather than to that of Salmonella and Escherichia. The genus is composed of gammaproteobacterial, secondary-endosymbionts which are gram-negative. Cells are non-flagellated, non-motile, non-spore forming and form long to highly filamentous rods. Cellular division is exhibited through septation. The name 'Arsenophonus nasoniae gen. nov., sp. nov.' was therefore proposed for the discovered bacterium due to its characteristics and its microbial interaction with N. vitripennis. The type strain of A. nasoniae is Strain SKI4.

Spiroplasma citri is a bacterium species and the causative agent of Citrus stubborn disease.

<i>Spiroplasma phage 1-R8A2B</i> Species of virus

Spiroplasma phage 1-R8A2B is a filamentous bacteriophage in the genus Vespertiliovirus of the family Plectroviridae, part of the group of single-stranded DNA viruses. The virus has many synonyms, such as SpV1-R8A2 B, Spiroplasma phage 1, and Spiroplasma virus 1, SpV1. SpV1-R8A2 B infects Spiroplasma citri. Its host itself is a prokaryotic pathogen for citrus plants, causing Citrus stubborn disease.

Arsenophonus is a genus of Morganellaceae, of the Gammaproteobacteria. Members of the Arsenophonus genus are increasingly discovered bacterial symbionts of arthropods that are estimated to infect over 5% of arthropod species globally 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 and the rice pest Nilaparvata lugens.

<i>Howardula aoronymphium</i> Species of roundworm

Howardula aoronymphium is a species of nematode that infects specialist mushroom-feeding fruit flies such as Drosophila falleni and Drosophila neotestacea. Mated female nematodes pierce the fly larva cuticle and take up residence in the hemolymph where they mature alongside the fly. When the adult fly ecloses, the nematode motherworm has reached full size and sheds juvenile nematodes into the hemolymph which are eventually excreted by either the fly anus or ovipositor. Howardula nematodes can severely impact fly egg development, as infection can effectively sterilize some species.

<i>Drosophila neotestacea</i> Species of fly

Drosophila neotestacea is a member of the testacea species group of Drosophila. Testacea species are specialist fruit flies that breed on the fruiting bodies of mushrooms. These flies will choose to breed on psychoactive mushrooms such as the Fly Agaric Amanita muscaria. Drosophila neotestacea can be found in temperate regions of North America, ranging from the north eastern United States to western Canada.

<i>Drosophila testacea</i> species group Species group of the subgenus Drosophila

The Drosophila testacea species group belongs to the Immigrans-tripunctata radiation of the subgenus Drosophila, and contains 4 species: Drosophila putrida, Drosophila neotestacea, Drosophila testacea, and Drosophila orientacea. Testacea species are specialist mushroom-feeding flies, and can metabolize toxic compounds in Amanita mushrooms. The Testacea species group is studied for its specialist ecology, population genetics, and bacterial endosymbionts. The North American species Drosophila neotestacea is perhaps the best-studied of the group for its interactions with parasitic wasps and nematodes, bacterial endosymbionts, and trypanosomatid parasites. Of note, selfish X chromosomes have been discovered in three of the four Testacea group species.

Spiroplasma poulsonii are bacteria of the genus Spiroplasma that are commonly endosymbionts of flies. These bacteria live in the hemolymph of the flies, where they can act as reproductive manipulators or defensive symbionts.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

<i>Drosophila innubila</i> Species of fly

Drosophila innubila is a species of vinegar fly restricted to high-elevation woodlands in the mountains of the southern USA and Mexico, which it likely colonized during the last glacial period. Drosophila innubila is a kind of mushroom-breeding Drosophila, and member of the Drosophila quinaria species group. Drosophila innubila is best known for its association with a strain of male-killing Wolbachia bacteria. These bacteria are parasitic, as they drain resources from the host and cause half the infected female's eggs to abort. However Wolbachia may offer benefits to the fly's fitness in certain circumstances. The D. innubila genome was sequenced in 2019.

John Jaenike is an ecologist and evolutionary biologist, and currently a professor at the University of Rochester New York. Jaenike was an early proponent of the Red Queen hypothesis, using the idea to explain the maintenance of sex. Jaenike is also known for his extensive work on mushroom-feeding Drosophila and the evolution of their inherited bacterial symbionts Wolbachia and Spiroplasma poulsonii.

<span class="mw-page-title-main">Morganellaceae</span> Family of bacteria

The Morganellaceae are a family of Gram-negative bacteria that include some important human pathogens formerly classified as Enterobacteriaceae. This family is a member of the order Enterobacterales in the class Gammaproteobacteria of the phylum Pseudomonadota. Genera in this family include the type genus Morganella, along with Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia and Xenorhabdus.

Candidatus Arsenophonus arthropodicus is a Gram-negative and intracellular secondary (S) endosymbiont that belongs to the genus Arsenophonus. This bacterium is found in the Hippoboscid louse fly, Pseudolynchia canariensis. S-endosymbionts are commonly found in distinct tissues. Strains of recovered Arsenophonus found in arthropods share 99% sequence identification in the 16S rRNA gene across all species. Arsenophonus-host interactions involve parasitism and mutualism, including a popular mechanism of "male-killing" found commonly in a related species, Arsenophonus nasoniae. This species is considered "Ca. A. arthropodicus" due it being as of yet uncultured.

<i>Spiroplasma kunkelii</i> Species of bacteria

Spiroplasma kunkelii is a species of Mollicutes, which are small bacteria that all share a common cell wall-less feature. They are characterized by helical and spherical morphology, they actually have the ability to be spherical or helical depending on the circumstances. The cells movement is bound by a membrane. The cell size ranges from 0.15 to 0.20 micrometers.

References

  1. 1 2 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. 1 2 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. ↑ Corbin, Chris; Jones, Jordan E.; Chrostek, Ewa; Fenton, Andy; Hurst, Gregory D. D. (2021). "Thermal sensitivity of the Spiroplasma–Drosophila hydei protective symbiosis: The best of climes, the worst of climes". Molecular Ecology. 30 (5): 1336–1344. Bibcode:2021MolEc..30.1336C. doi:10.1111/mec.15799. ISSN   1365-294X. PMID   33428287.
  11. ↑ Jones, Jordan E.; Hurst, Gregory D. D. (2023). "History matters: Thermal environment before but not during wasp attack determines the efficiency of symbiont-mediated protection". Molecular Ecology. 32 (12): 3340–3351. Bibcode:2023MolEc..32.3340J. doi:10.1111/mec.16935. ISSN   1365-294X.
  12. ↑ Montenegro, H.; Solferini, V. N.; Klaczko, L. B.; Hurst, G. D. D. (2005). "Male-killing Spiroplasma naturally infecting Drosophila melanogaster". Insect Molecular Biology. 14 (3): 281–287. doi:10.1111/j.1365-2583.2005.00558.x. ISSN   1365-2583. PMID   15926897.
  13. ↑ Veneti, Zoe; Bentley, Joanna K.; Koana, Takao; Braig, Henk R.; Hurst, Gregory D. D. (2005-03-04). "A Functional Dosage Compensation Complex Required for Male Killing in Drosophila". Science. 307 (5714): 1461–1463. Bibcode:2005Sci...307.1461V. doi:10.1126/science.1107182. PMID   15746426.
  14. ↑ Bentley, Joanna K.; Veneti, Zoe; Heraty, Joseph; Hurst, Gregory DD (2007-03-15). "The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa". BMC Biology. 5 (1): 9. doi: 10.1186/1741-7007-5-9 . ISSN   1741-7007. PMC   1832177 . PMID   17362512.
  15. ↑ 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.
  16. ↑ Papageorgiou, Nik (5 July 2018). "Mystery solved: The bacterial protein that kills male fruit flies".
  17. ↑ 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.
  18. ↑ 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.
  19. ↑ 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.
  20. ↑ Hurst, G. D. D.; von der Schulenburg, J. H. Graf; Majerus, T. M. O.; Bertrand, D.; Zakharov, I. A.; Baungaard, J.; Völkl, W.; Stouthamer, R.; Majerus, M. E. N. (1999). "Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria". Insect Molecular Biology. 8 (1): 133–139. doi:10.1046/j.1365-2583.1999.810133.x. ISSN   1365-2583. PMID   9927182.
  21. ↑ Majerus, T. M. O.; Von Der Schulenburg, J. H. Graf; Majerus, M. E. N.; Hurst, G. D. D. (November 1999). "Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae)". Insect Molecular Biology. 8 (4): 551–555. doi:10.1046/j.1365-2583.1999.00151.x. ISSN   0962-1075. PMID   10634973.
  22. ↑ Hayashi, Masayuki; Watanabe, Masaya; Yukuhiro, Fumiko; Nomura, Masashi; Kageyama, Daisuke (2016-06-15). Bourtzis, Kostas (ed.). "A Nightmare for Males? A Maternally Transmitted Male-Killing Bacterium and Strong Female Bias in a Green Lacewing Population". PLOS ONE. 11 (6): e0155794. Bibcode:2016PLoSO..1155794H. doi: 10.1371/journal.pone.0155794 . ISSN   1932-6203. PMC   4909225 . PMID   27304213.
  23. ↑ 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.
  24. ↑ 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.
  25. ↑ "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.
  26. ↑ 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.
  27. ↑ 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. Bibcode:2003JInvP..82..167O. doi:10.1016/S0022-2011(03)00031-4. ISSN   0022-2011. PMID   12676553.
  28. ↑ Renbaum, Paul; Abrahamove, Dan; Fainsod, Abraham; Wilson, Geoffrey G.; Rottem, Shlomo; Razin, Aharon (1990-03-11). "Cloning, characterization, and expression in Escherichia coli of the gene coding for the CpG DNA methylase from Spiroplasma sp. strain MQ1(M Sssl)". Nucleic Acids Research. 18 (5): 1145–1152. doi:10.1093/nar/18.5.1145. ISSN   0305-1048. PMC   330428 . PMID   2181400.
  29. ↑ Gerth, Michael; Martinez-Montoya, Humberto; Ramirez, Paulino; Masson, Florent; Griffin, Joanne S.; Aramayo, Rodolfo; Siozios, Stefanos; Lemaitre, Bruno; Mateos, Mariana; Hurst, Gregory D. D. (2021). "Rapid molecular evolution of Spiroplasma symbionts of Drosophila". Microbial Genomics. 7 (2): 000503. doi: 10.1099/mgen.0.000503 . ISSN   2057-5858. PMC   8208695 . PMID   33591248.
  30. ↑ Ipoutcha, Thomas; Tsarmpopoulos, Iason; Talenton, Vincent; Gaspin, Christine; Moisan, Annick; Walker, Caray A.; Brownlie, Joe; Blanchard, Alain; Thebault, Patricia; Sirand-Pugnet, Pascal (2019-11-21). "Multiple Origins and Specific Evolution of CRISPR/Cas9 Systems in Minimal Bacteria (Mollicutes)". Frontiers in Microbiology. 10: 2701. doi: 10.3389/fmicb.2019.02701 . ISSN   1664-302X. PMC   6882279 . PMID   31824468.
  31. ↑ A.C. Parte; et al. "Spiroplasmataceae". List of Prokaryotic names with Standing in Nomenclature (LPSN). Retrieved 2022-09-09.
  32. ↑ Sayers; et al. "Spiroplasmataceae". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2022-09-09.
  33. ↑ "The LTP" . Retrieved 20 November 2023.
  34. ↑ "LTP_all tree in newick format" . Retrieved 20 November 2023.
  35. ↑ "LTP_08_2023 Release Notes" (PDF). Retrieved 20 November 2023.
  36. ↑ "GTDB release 08-RS214". Genome Taxonomy Database . Retrieved 10 May 2023.
  37. ↑ "bac120_r214.sp_label". Genome Taxonomy Database . Retrieved 10 May 2023.
  38. ↑ "Taxon History". Genome Taxonomy Database . Retrieved 10 May 2023.
  39. ↑ 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.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.