Literature DB >> 29563258

Common and unique strategies of male killing evolved in two distinct Drosophila symbionts.

Toshiyuki Harumoto1, Takema Fukatsu2, Bruno Lemaitre3.   

Abstract

Male killing is a selfish reproductive manipulation caused by symbiotic bacteria, where male offspring of infected hosts are selectively killed. The underlying mechanisms and the process of their evolution are of great interest not only in terms of fundamental biology, but also their potential applications. The two bacterial Drosophila symbionts, Wolbachia and Spiroplasma, have independently evolved male-killing ability. This raises the question whether the underlying mechanisms share some similarities or are specific to each bacterial species. Here, we analyse pathogenic phenotypes of D. bifasciata infected with its natural male-killing Wolbachia strain and compare them with those of D. melanogaster infected with male-killing Spiroplasma We show that male progeny infected with the Wolbachia strain die during embryogenesis with abnormal apoptosis. Interestingly, male-killing Wolbachia infection induces DNA damage and segregation defects in the dosage-compensated chromosome in male embryos, which are reminiscent of the phenotypes caused by male-killing Spiroplasma in D. melanogaster By contrast, host neural development seems to proceed normally unlike male-killing Spiroplasma infection. Our results demonstrate that the dosage-compensated chromosome is a common target of two distinct male killers, yet Spiroplasma uniquely evolved the ability to damage neural tissue of male embryos.
© 2018 The Authors.

Entities:  

Keywords:  Drosophila; Spiroplasma; Wolbachia; male killing; symbiosis

Mesh:

Year:  2018        PMID: 29563258      PMCID: PMC5897628          DOI: 10.1098/rspb.2017.2167

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  53 in total

1.  Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp.

Authors:  F Dedeine; F Vavre; F Fleury; B Loppin; M E Hochberg; M Bouletreau
Journal:  Proc Natl Acad Sci U S A       Date:  2001-05-15       Impact factor: 11.205

2.  Sex-ratio; a non-Mendelian character in Drosophila bifasciata.

Authors:  G E MAGNI
Journal:  Nature       Date:  1953-07-11       Impact factor: 49.962

3.  Male-Killing Spiroplasma Alters Behavior of the Dosage Compensation Complex during Drosophila melanogaster Embryogenesis.

Authors:  Becky Cheng; Nitin Kuppanda; John C Aldrich; Omar S Akbari; Patrick M Ferree
Journal:  Curr Biol       Date:  2016-05-05       Impact factor: 10.834

Review 4.  Reproductive parasitism: maternally inherited symbionts in a biparental world.

Authors:  Gregory D D Hurst; Crystal L Frost
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-05-01       Impact factor: 10.005

5.  The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes.

Authors:  I Marín; A Franke; G J Bashaw; B S Baker
Journal:  Nature       Date:  1996-09-12       Impact factor: 49.962

6.  Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development.

Authors:  S Robinow; K White
Journal:  J Neurobiol       Date:  1991-07

7.  Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y.

Authors:  Antonio Bernardo Carvalho; Andrew G Clark
Journal:  Science       Date:  2004-11-04       Impact factor: 47.728

8.  A host parasite interaction rescues Drosophila oogenesis defects.

Authors:  Diana J Starr; Thomas W Cline
Journal:  Nature       Date:  2002-07-04       Impact factor: 49.962

Review 9.  Are all sex chromosomes created equal?

Authors:  Doris Bachtrog; Mark Kirkpatrick; Judith E Mank; Stuart F McDaniel; J Chris Pires; William Rice; Nicole Valenzuela
Journal:  Trends Genet       Date:  2011-09       Impact factor: 11.639

10.  Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo.

Authors:  Jennifer Martin; Trisha Chong; Patrick M Ferree
Journal:  PLoS One       Date:  2013-11-13       Impact factor: 3.240

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  8 in total

Review 1.  Genetic innovations in animal-microbe symbioses.

Authors:  Julie Perreau; Nancy A Moran
Journal:  Nat Rev Genet       Date:  2021-08-13       Impact factor: 59.581

Review 2.  Sex determination systems as the interface between male-killing bacteria and their hosts.

Authors:  Emily A Hornett; Daisuke Kageyama; Gregory D D Hurst
Journal:  Proc Biol Sci       Date:  2022-04-13       Impact factor: 5.530

Review 3.  The effect of the endosymbiont Wolbachia on the behavior of insect hosts.

Authors:  Jie Bi; Yu-Feng Wang
Journal:  Insect Sci       Date:  2019-11-11       Impact factor: 3.262

4.  A Tangled Web: Origins of Reproductive Parasitism.

Authors:  Joseph J Gillespie; Timothy P Driscoll; Victoria I Verhoeve; Mohammed Sayeedur Rahman; Kevin R Macaluso; Abdu F Azad
Journal:  Genome Biol Evol       Date:  2018-09-01       Impact factor: 3.416

5.  Spiroplasma Infection among Ixodid Ticks Exhibits Species Dependence and Suggests a Vertical Pattern of Transmission.

Authors:  Shohei Ogata; Wessam Mohamed Ahmed Mohamed; Kodai Kusakisako; May June Thu; Yongjin Qiu; Mohamed Abdallah Mohamed Moustafa; Keita Matsuno; Ken Katakura; Nariaki Nonaka; Ryo Nakao
Journal:  Microorganisms       Date:  2021-02-08

6.  A single synonymous nucleotide change impacts the male-killing phenotype of prophage WO gene wmk.

Authors:  Jessamyn I Perlmutter; Jane E Meyers; Seth R Bordenstein
Journal:  Elife       Date:  2021-10-22       Impact factor: 8.140

7.  The phage gene wmk is a candidate for male killing by a bacterial endosymbiont.

Authors:  Jessamyn I Perlmutter; Sarah R Bordenstein; Robert L Unckless; Daniel P LePage; Jason A Metcalf; Tom Hill; Julien Martinez; Francis M Jiggins; Seth R Bordenstein
Journal:  PLoS Pathog       Date:  2019-09-10       Impact factor: 6.823

8.  Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis.

Authors:  Jae Hak Son; Brian L Weiss; Daniela I Schneider; Kiswend-Sida M Dera; Fabian Gstöttenmayer; Robert Opiro; Richard Echodu; Norah P Saarman; Geoffrey M Attardo; Maria Onyango; Adly M M Abd-Alla; Serap Aksoy
Journal:  PLoS Pathog       Date:  2021-09-16       Impact factor: 6.823

  8 in total

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