Microorganisms in the reproductive tissues of arthropods

Perlmutter, Jessamyn I.; Bordenstein, Seth R.

doi:10.1038/s41579-019-0309-z

Cited by 77 publications

(64 citation statements)

References 208 publications

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“…IM18, Dro, and Listericin), indicating that exposure to microbiota during courtship or copulation stimulates an additional up-regulation of these immune gene transcripts. There is increasing attention for the role of reproductive tract microbiota in reproductive success 62,92 , and a femaleand male-specific reproductive tract microbiome has been characterized in Anopheles mosquitos, but whether D. melanogaster have reproductive-tract specific microbiomes that can influence the post-mating up-regulation of immune transcripts is not yet known.…”

Section: Discussionmentioning

confidence: 99%

Interactions between the microbiome and mating influence the female’s transcriptional profile in Drosophila melanogaster

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Ahmed-Braimah

Wolfner

et al. 2020

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Drosophila melanogaster females undergo a variety of post-mating changes that influence their activity, feeding behavior, metabolism, egg production and gene expression. These changes are induced either by mating itself or by sperm or seminal fluid proteins. In addition, studies have shown that axenic females—those lacking a microbiome—have altered fecundity compared to females with a microbiome, and that the microbiome of the female’s mate can influence reproductive success. However, the extent to which post-mating changes in transcript abundance are affected by microbiome state is not well-characterized. Here we investigated fecundity and the post-mating transcript abundance profile of axenic or control females after mating with either axenic or control males. We observed interactions between the female’s microbiome and her mating status: transcripts of genes involved in reproduction and genes with neuronal functions were differentially abundant depending on the females’ microbiome status, but only in mated females. In addition, immunity genes showed varied responses to either the microbiome, mating, or a combination of those two factors. We further observed that the male’s microbiome status influences the fecundity of both control and axenic females, while only influencing the transcriptional profile of axenic females. Our results indicate that the microbiome plays a vital role in the post-mating switch of the female’s transcriptome.

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Section: Discussionmentioning

confidence: 99%

Interactions between the microbiome and mating influence the female’s transcriptional profile in Drosophila melanogaster

Delbare

Ahmed-Braimah

Wolfner

et al. 2020

Sci Rep

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“…Host niches may thus impact possibilities of Wolbachia host shifts, but the bacteria may also, reciprocally, affect host niches. Many mutualistic endosymbionts can limit their host's niche (Corbin et al, 2017;Perlmutter & Bordenstein, 2020), e.g. by reducing thermal tolerance, as has been reported in Buchnera endosymbionts in aphids (Zhang et al, 2019)).…”

Section: (4) the Role Of Ecologymentioning

confidence: 91%

Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences

2020

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Wolbachia is one of the most abundant endosymbionts on earth, with a wide distribution especially in arthropods. Effective maternal transmission and the induction of various phenotypes in their hosts are two key features of this bacterium. Here, we review our current understanding of another central aspect of Wolbachia's success: their ability to switch from one host species to another. We build on the proposal that Wolbachia host shifts occur in four main steps: (i) physical transfer to a new species; (ii) proliferation within that host; (iii) successful maternal transmission; and (iv) spread within the host species. Host shift can fail at each of these steps, and the likelihood of ultimate success is influenced by many factors. Some stem from traits of Wolbachia (different strains have different abilities for host switching), others on host features such as genetic resemblance (e.g. host shifting is likely to be easier between closely related species), ecological connections (the donor and recipient host need to interact), or the resident microbiota. Host shifts have enabled Wolbachia to reach its enormous current incidence and global distribution among arthropods in an epidemiological process shaped by loss and acquisition events across host species. The ability of Wolbachia to transfer between species also forms the basis of ongoing endeavours to control pests and disease vectors, following artificial introduction into uninfected hosts such as mosquitoes. Throughout, we emphasise the many knowledge gaps in our understanding of Wolbachia host shifts, and question the effectiveness of current methodology to detect these events. We conclude by discussing an apparent paradox: how can Wolbachia maintain its ability to undergo host shifts given that its biology seems dominated by vertical transmission?

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“…These reproductive parasites hijack host cellular processes and alter host reproduction to facilitate their spread. They include a variety of maternally inherited bacterial, fungal, and viral endosymbionts that infect a large number of arthropod hosts, including all major groups of insects and arachnids (2). Among these microbes, the most common are of the genus Wolbachia, which are obligate intracellular bacteria that manipulate host reproduction in a variety of ways (3,4).…”

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Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

2020

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Endosymbiotic bacteria in the genus Wolbachia remarkably infect nearly half of all arthropod species. They spread in part because of manipulations of host sexual reproduction that enhance the maternal transmission of the bacteria, including male killing (death of infected males) and unidirectional cytoplasmic incompatibility (CI; death of offspring from infected fathers and uninfected mothers). Recent discoveries identified several genes in prophage WO of Wolbachia (wmk, cifA, and cifB) that fully or partially recapitulate male killing or CI when transgenically expressed in Drosophila melanogaster. However, it is not yet fully resolved if other gene candidates contribute to these phenotypes. Here, we transgenically tested 10 additional gene candidates for their involvement in male killing and/or CI. The results show that despite sequence and protein architecture similarities or comparative associations with reproductive parasitism, transgenic expression of the candidates does not recapitulate male killing or CI. Sequence analysis across Wmk and its closest relatives reveals amino acids that may be important to its function. In addition, evidence is presented to propose new hypotheses regarding the relationship between wmk transcript length and its ability to kill a given host, as well as copy number of wmk homologs within a bacterial strain, which may be predictive of host resistance. Together, these analyses continue to build the evidence for identification of wmk, cifA, and cifB as the major genes that have thus far been shown to cause reproductive parasitism in Wolbachia, and the transgenic resources provide a basis for further functional study of phage WO genes. IMPORTANCE Wolbachia are widespread bacterial endosymbionts that manipulate the reproduction of diverse arthropods to spread through a population and can substantially shape host evolution. Recently, reports identified three prophage WO genes (wmk, cifA, and cifB) that transgenically recapitulate many aspects of reproductive manipulation in Drosophila melanogaster. Here, we transgenically tested 10 additional gene candidates for CI and/or male killing in flies. The results yield no evidence for the involvement of these gene candidates in reproductive parasitism, bolstering the evidence for identification of the cif and wmk genes as the major factors involved in their phenotypes. In addition, evidence supports new hypotheses for prediction of male-killing phenotypes or lack thereof based on wmk transcript length and copy number. These experiments inform efforts to understand the full basis of reproductive parasitism for basic and applied purposes and lay the foundation for future work on the function of an interesting group of Wolbachia and phage WO genes.

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Microorganisms in the reproductive tissues of arthropods

Cited by 77 publications

References 208 publications

Interactions between the microbiome and mating influence the female’s transcriptional profile in Drosophila melanogaster

Interactions between the microbiome and mating influence the female’s transcriptional profile in Drosophila melanogaster

Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

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