Reductive genome evolution, host–symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies

Hosokawa, Takahiro; Nikoh, Naruo; Koga, Ryuichi; Satô, Masahiko; Tanahashi, Masahiko; Meng, Xian Ying; Fukatsu, Takema

doi:10.1038/ismej.2011.125

Cited by 79 publications

(106 citation statements)

References 51 publications

(69 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…S6). In the bat fly, the louse fly, the grasshopper, and the termites, the F Wolbachia infections are not fixed in the host populations, suggesting facultative nature of these host-symbiont associations (32)(33)(34)(35). These observations suggest that (i) the bedbug-wCle nutritional mutualism evolved independently of the nematodeWolbachia mutualism within the Wolbachia F supergroup, (ii) the origin of the bedbug-wCle mutualistic association is more recent than the origin of the nematode-Wolbachia mutualistic association, (iii) plausibly, an ancestor of the cimicid bugs acquired wCle from an unrelated arthropod host, (iv) in the donor arthropod, wCle was likely a facultative endosymbiotic associate, and (v) the establishment of the bedbug-wCle association presumably entailed an evolutionary transition from facultative symbiosis to obligate nutritional mutualism for the symbiont side.…”

Section: Conserved Biotin Operon Inserted In the Wolbachia Genomementioning

confidence: 99%

Evolutionary origin of insect– Wolbachia nutritional mutualism

Nikoh

Hosokawa

Moriyama

et al. 2014

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

Self Cite

348

407

View full text Add to dashboard Cite

Obligate insect-bacterium nutritional mutualism is among the most sophisticated forms of symbiosis, wherein the host and the symbiont are integrated into a coherent biological entity and unable to survive without the partnership. Originally, however, such obligate symbiotic bacteria must have been derived from free-living bacteria. How highly specialized obligate mutualisms have arisen from less specialized associations is of interest. Here we address this evolutionary issue by focusing on an exceptional insect-Wolbachia nutritional mutualism. Although Wolbachia endosymbionts are ubiquitously found in diverse insects and generally regarded as facultative/parasitic associates for their insect hosts, a Wolbachia strain associated with the bedbug Cimex lectularius, designated as wCle, was shown to be essential for host's growth and reproduction via provisioning of B vitamins. We determined the 1,250,060-bp genome of wCle, which was generally similar to the genomes of insect-associated facultative Wolbachia strains, except for the presence of an operon encoding the complete biotin synthetic pathway that was acquired via lateral gene transfer presumably from a coinfecting endosymbiont Cardinium or Rickettsia. Nutritional and physiological experiments, in which wCle-infected and wCle-cured bedbugs of the same genetic background were fed on B-vitaminmanipulated blood meals via an artificial feeding system, demonstrated that wCle certainly synthesizes biotin, and the wCleprovisioned biotin significantly contributes to the host fitness. These findings strongly suggest that acquisition of a single gene cluster consisting of biotin synthesis genes underlies the bedbug-Wolbachia nutritional mutualism, uncovering an evolutionary transition from facultative symbiosis to obligate mutualism facilitated by lateral gene transfer in an endosymbiont lineage.

show abstract

Section: Conserved Biotin Operon Inserted In the Wolbachia Genomementioning

confidence: 99%

Evolutionary origin of insect– Wolbachia nutritional mutualism

Nikoh

Hosokawa

Moriyama

et al. 2014

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

Self Cite

348

407

View full text Add to dashboard Cite

show abstract

“…Long-term host-symbiont relationships often lead to a complete interdependence of both partners over evolutionary time [13][14][15][16]. Once established within the host, endosymbionts generally experience severe genome size reduction due to relaxed evolutionary pressures on genes that are redundant with host functions [17][18][19] or become unnecessary for the new association [20].…”

Section: Introductionmentioning

confidence: 99%

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

Masson¹,

Zaidman-Rémy²,

Heddi³

2016

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Many insects sustain long-term relationships with intracellular symbiotic bacteria that provide them with essential nutrients. Such endosymbiotic relationships likely emerged from ancestral infections of the host by free-living bacteria, the genomes of which experience drastic gene losses and rearrangements during the host-symbiont coevolution. While it is well documented that endosymbiont genome shrinkage results in the loss of bacterial virulence genes, whether and how the host immune system evolves towards the tolerance and control of bacterial partners remains elusive. Remarkably, many insects rely on a 'compartmentalization strategy' that consists in secluding endosymbionts within specialized host cells, the bacteriocytes, thus preventing direct symbiont contact with the host systemic immune system. In this review, we compile recent advances in the understanding of the bacteriocyte immune and cellular regulators involved in endosymbiont maintenance and control. We focus on the cereal weevils Sitophilus spp., in which bacteriocytes form bacteriome organs that strikingly evolve in structure and number according to insect development and physiological needs. We discuss how weevils track endosymbiont dynamics through at least two mechanisms: (i) a bacteriome local antimicrobial peptide synthesis that regulates endosymbiont cell cytokinesis and helps to maintain a homeostatic state within bacteriocytes and (ii) some cellular processes such as apoptosis and autophagy which adjust endosymbiont load to the host developmental requirements, hence ensuring a fine-tuned integration of symbiosis costs and benefits.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

show abstract

“…This "pupiparity" makes horizontal transfer of symbionts unlikely, as there is no feeding stage outside the body of the maternal parent. Hosokawa et al (20) observed symbiont infection in the maternal milk gland in several members of the Nycteribiinae, suggesting uterine transmission of bacteria to the larvae through milk gland secretions, which also has been documented for tsetse flies (26).…”

mentioning

confidence: 99%

“…Although similar in 16S rRNA gene sequences to Arsenophonus, they were ultimately assigned to a distinct lineage that is sister to "Candidatus Riesia pediculicola," an endosymbiont found in primate lice. Based on phylogenetic characteristics, Hosokawa et al (20) proposed a new name, "Candidatus Aschnera chinzeii," for this clade. The presence of vertical transmission and an overall evolutionary concordance between host and symbiont suggest an obligate association with its host (20).…”

mentioning

confidence: 99%

“…Based on phylogenetic characteristics, Hosokawa et al (20) proposed a new name, "Candidatus Aschnera chinzeii," for this clade. The presence of vertical transmission and an overall evolutionary concordance between host and symbiont suggest an obligate association with its host (20). Although the specific function of "Candidatus Aschnera chinzeii" is unknown, the closely related "Candidatus Riesia pediculicola" is essential for the survival of its louse host, providing B complex vitamins that are lacking in the host's blood diet (21).…”

mentioning

confidence: 99%

See 1 more Smart Citation