Paternal transmission of symbiotic bacteria in malaria vectors

Damiani, Claudia; Ricci, Irene; Crotti, Elena; Rossi, Paolo; Rizzi, Aurora; Scuppa, Patrizia; Esposito, Fulvio; Bandi, Claudio; Daffonchio, Daniele; Favia, Guido

doi:10.1016/j.cub.2008.10.040

Cited by 130 publications

(136 citation statements)

References 7 publications

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“…However, Wolbachia, also present in C. obscurior, could exert effects on host reproduction as well. In contrast to some other intracellular symbionts (Moran and Dunbar, 2006;Damiani et al, 2008;Watanabe et al, 2014), paternal transmission of Westeberhardia is unlikely as we did not detect Westeberhardia DNA in transferred sperm and/or seminal fluids stored in the spermatheca of uninfected queens mated to infected males.…”

Section: Transmission Of Westeberhardiacontrasting

confidence: 78%

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

et al. 2015

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The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior, 'Candidatus Westeberhardia cardiocondylae'. Upon metamorphosis, Westeberhardia is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain Westeberhardia in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of Westeberhardia (533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of Westeberhardia during pupal stage, this suggests a contribution of Westeberhardia to cuticle formation. Despite a widespread occurrence of Westeberhardia across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of C. obscurior.

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Section: Transmission Of Westeberhardiacontrasting

confidence: 78%

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

et al. 2015

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“…Asaia bacteria naturally infect the Anopheles germ line and are vertically transmitted (39,40), and thus may conflict with other maternally transmitted bacteria. This, together with the observed significant and large decrease in frequency of this taxon upon antibiotic treatment in both mosquito species, led us to investigate Asaia as a candidate bacteria involved in the interference of Wolbachia transmission.…”

Section: Microbiota-wolbachia Interactions Kill Mosquitoes After a Bloodmentioning

confidence: 99%

Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes

Hughes¹,

Dodson²,

Johnson

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

225

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Significance Factors influencing Wolbachia transfer into new species remain poorly understood. This is important as Wolbachia can influence speciation and is being developed as a novel arthropod-borne disease control approach. We show the native microbiota of Anopheles impede vertical transmission of Wolbachia . Antibiotic microbiome perturbation enables Wolbachia transmission in two Anopheles species. Mosquitoes with altered microbiomes do not exhibit blood meal-induced mortality associated with Wolbachia infection, suggesting that mosquitoes are killed by interactions between Wolbachia and other bacteria present in the mosquito. We identified Asaia as the bacterium responsible for inhibiting Wolbachia transmission, and partially responsible for blood meal-induced mortality. These results suggest that microbial interactions profoundly affect the host, and that microbiome incompatibility may influence distribution of Wolbachia in arthropods.

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“…Namely, the symbionts are transmitted vertically to the next host generation via infection to eggs in the maternal body, but not via infection to sperms (8,9). Exceptional reports of paternal symbiont transmission are venereal transmission cases of several symbiotic bacteria (10,11) and biparental transmission cases of some symbiotic viruses (12). Oocytes accumulate a large quantity of cytoplasm that provide a room for symbiont infection, whereas sperms discard their cytoplasm (together with inhabiting symbiotic bacteria) during spermatogenesis and transform into a streamlined shape with the small head consisting of condensed nucleus and the slender tail made of microtubule bundles for motility (13,14).…”

mentioning

confidence: 99%

Intrasperm vertical symbiont transmission

Watanabe

Yukuhiro

Matsuura

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Symbiotic bacteria are commonly associated with cells and tissues of diverse animals and other organisms, which affect hosts' biology in a variety of ways. Most of these symbionts are present in the cytoplasm of host cells and maternally transmitted through host generations. The paucity of paternal symbiont transmission is likely relevant to the extremely streamlined sperm structure: the head consisting of condensed nucleus and the tail made of microtubule bundles, without the symbiont-harboring cytoplasm that is discarded in the process of spermatogenesis. Here, we report a previously unknown mechanism of paternal symbiont transmission via an intrasperm passage. In the leafhopper Nephotettix cincticeps, a facultative Rickettsia symbiont was found not only in the cytoplasm but also in the nucleus of host cells. In male insects, strikingly, most sperm heads contained multiple intranuclear Rickettsia cells. The Rickettsia infection scarcely affected the host fitness including normal sperm functioning. Mating experiments revealed both maternal and paternal transmission of the Rickettsia symbiont through host generations. When cultured with mosquito and silkworm cell lines, the Rickettsia symbiont was preferentially localized within the insect cell nuclei, indicating that the Rickettsia symbiont itself must have a mechanism for targeting nucleus. The mechanisms underlying the sperm head infection without disturbing sperm functioning are, although currently unknown, of both basic and applied interest.

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Paternal transmission of symbiotic bacteria in malaria vectors

Cited by 130 publications

References 7 publications

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla obscurior

Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes

Intrasperm vertical symbiont transmission

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