Spiroplasma poulsonii

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Spiroplasma poulsonii
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Mycoplasmatota
Class: Mollicutes
Order: Mycoplasmatales
Family: Mycoplasmataceae
Genus: Spiroplasma
Species:
S. poulsonii
Binomial name
Spiroplasma poulsonii
Williamson et al. 1999

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.

Contents

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. neotestaceaSpiroplasma 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]

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, 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 any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) 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>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly", "pomace fly", or "banana fly". Starting with Charles W. Woodworth's 1901 proposal of the use of this species as a model organism, D. melanogaster continues to be widely used for biological research in genetics, physiology, microbial pathogenesis, and life history evolution. As of 2017, six Nobel Prizes have been awarded to drosophilists for their work using the insect.

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

Wolbachia is a genus of intracellular bacteria that infects mainly arthropod species, including a high proportion of insects, and also some nematodes. It is one of the most common parasitic microbes, and is possibly the most common reproductive parasite in the biosphere. Its interactions with its hosts are often complex, and in some cases have evolved to be mutualistic rather than parasitic. 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>Spiroplasma</i> Genus of bacteria

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, 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.

<span class="mw-page-title-main">Ribosome-inactivating protein</span> Protein synthesis inhibitor

A ribosome-inactivating protein (RIP) is a protein synthesis inhibitor that acts at the eukaryotic ribosome. This protein family describes a large family of such proteins that work by acting as rRNA N-glycosylase. They inactivate 60S ribosomal subunits by an N-glycosidic cleavage, which releases a specific adenine base from the sugar-phosphate backbone of 28S rRNA. RIPs exist in bacteria and plants.

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.

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

Drosophila hydei (mosca casera) is a species of Diptera, or the order of flies, in the family Drosophilidae. It is a species in the hydei species subgroup, a group in the repleta species group. Bizarrely, it is also known for having approximately 23 mm long sperm, 10 times the length of the male's body. Drosophila hydei are commonly found on compost piles worldwide, and can be rudimentarily identified by eye owing to their large size and variegated pigment pattern on the thorax. The name derives from Dr R. R. Hyde, who first discovered that the species was distinct from Drosophila repleta. D. hydei are one of the more popular flies used as feeders in the pet trade. A few varieties are available, some flightless. They are very similar to Drosophila melanogaster, despite having separated 50 million years ago.

The microbiota are the sum of all symbiotic microorganisms living on or in an organism. The fruit fly Drosophila melanogaster is a model organism and known as one of the most investigated organisms worldwide. The microbiota in flies is less complex than that found in humans. It still has an influence on the fitness of the fly, and it affects different life-history characteristics such as lifespan, resistance against pathogens (immunity) and metabolic processes (digestion). Considering the comprehensive toolkit available for research in Drosophila, analysis of its microbiome could enhance our understanding of similar processes in other types of host-microbiota interactions, including those involving humans. Microbiota plays key roles in the intestinal immune and metabolic responses via their fermentation product, acetate.

<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.

<span class="mw-page-title-main">Diptericin</span>

Diptericin is a 9 kDa antimicrobial peptide (AMP) of flies first isolated from the blowfly Phormia terranova. It is primarily active against Gram-negative bacteria, disrupting bacterial membrane integrity. The structure of this protein includes a proline-rich domain with similarities to the AMPs drosocin, pyrrhocoricin, and abaecin, and a glycine-rich domain with similarity to attacin. Diptericin is an iconic readout of immune system activity in flies, used ubiquitously in studies of Drosophila immunity. Diptericin is named after the insect order Diptera.

<span class="mw-page-title-main">Drosocin</span> Antimicrobial peptide

Drosocin is a 19-residue long antimicrobial peptide (AMP) of flies first isolated in the fruit fly Drosophila melanogaster, and later shown to be conserved throughout the genus Drosophila. Drosocin is regulated by the NF-κB Imd signalling pathway in the fly.

<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">Imd pathway</span> Immune signaling pathway of insects

The Imd pathway is a broadly-conserved NF-κB immune signalling pathway of insects and some arthropods that regulates a potent antibacterial defence response. The pathway is named after the discovery of a mutation causing severe immune deficiency. The Imd pathway was first discovered in 1995 using Drosophila fruit flies by Bruno Lemaitre and colleagues, who also later discovered that the Drosophila Toll gene regulated defence against Gram-positive bacteria and fungi. Together the Toll and Imd pathways have formed a paradigm of insect immune signalling; as of September 2, 2019, these two landmark discovery papers have been cited collectively over 5000 times since publication on Google Scholar.

<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.

<span class="mw-page-title-main">Bruno Lemaitre</span> French immunologist

Bruno Lemaitre is a French immunologist and a professor at the École Polytechnique Fédérale de Lausanne (EPFL). His research focuses on the mechanisms of innate immunity and endosymbiosis in Drosophila. Lemaitre has also authored several books on the topic of narcissism in science. and a book on the philosophy of Michael Polanyi.

References

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