Literature DB >> 28878066

Cytological analysis of cytoplasmic incompatibility induced by Cardinium suggests convergent evolution with its distant cousin Wolbachia.

Marco Gebiola1,2, Massimo Giorgini2, Suzanne E Kelly3, Matthew R Doremus3,4, Patrick M Ferree5, Martha S Hunter3.   

Abstract

Cytoplasmic incompatibility (CI) is a conditional sterility in numerous arthropods that is caused by inherited, intracellular bacteria such as Wolbachia Matings between males carrying CI-inducing Wolbachia and uninfected females, or between males and females infected with different Wolbachia strains, result in progeny that die during very early embryogenesis. Multiple studies in diploid (Drosophila) and haplodiploid (Nasonia) insects have shown that CI-Wolbachia cause a failure of the paternally derived chromatin from resolving into distinct chromosomes. This leads to the formation of chromatin bridges and other mitotic defects as early as the first mitotic division, and to early mitotic arrest. It is currently unknown if CI-inducing symbionts other than Wolbachia affect similar cellular processes. Here, we investigated CI caused by an unrelated bacterium, Cardinium, which naturally infects a parasitic wasp, Encarsia suzannae CI crosses in this host-symbiont system resulted in early mitotic defects including asynchrony of paternal and maternal chromosome sets as they enter mitosis, chromatin bridges and improper chromosome segregation that spanned across multiple mitotic divisions, triggering embryonic death through accumulated aneuploidy. We highlight small differences with CI-Wolbachia, which could be due to the underlying CI mechanism or host-specific effects. Our results suggest a convergence of CI-related cellular phenotypes between these two unrelated symbionts.
© 2017 The Author(s).

Entities:  

Keywords:  bacterial endosymbionts; embryonic death; mitotic defects; parasitoid; reproductive manipulators

Mesh:

Year:  2017        PMID: 28878066      PMCID: PMC5597839          DOI: 10.1098/rspb.2017.1433

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


  34 in total

1.  Within-species diversity of Wolbachia-induced cytoplasmic incompatibility in haplodiploid insects.

Authors:  F Vavre; F Dedeine; M Quillon; P Fouillet; F Fleury; M Bouletreau
Journal:  Evolution       Date:  2001-08       Impact factor: 3.694

2.  Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences.

Authors:  F Vavre; F Fleury; J Varaldi; P Fouillet; M Boulétreau
Journal:  Evolution       Date:  2000-02       Impact factor: 3.694

3.  Biology of Wolbachia.

Authors:  J H Werren
Journal:  Annu Rev Entomol       Date:  1997       Impact factor: 19.686

4.  Bidirectional incompatibility between conspecific populations of Drosophila simulans.

Authors:  S L O'Neill; T L Karr
Journal:  Nature       Date:  1990-11-08       Impact factor: 49.962

5.  Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans.

Authors:  C W Lassy; T L Karr
Journal:  Mech Dev       Date:  1996-06       Impact factor: 1.882

6.  Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii'.

Authors:  Einat Zchori-Fein; Steve J Perlman; Suzanne E Kelly; Nurit Katzir; Martha S Hunter
Journal:  Int J Syst Evol Microbiol       Date:  2004-05       Impact factor: 2.747

7.  Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia.

Authors:  Seth R Bordenstein; Julieanne J Uy; John H Werren
Journal:  Genetics       Date:  2003-05       Impact factor: 4.562

8.  Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron: disentangling the roles of Cardinium and Wolbachia symbionts.

Authors:  J A White; S E Kelly; S J Perlman; M S Hunter
Journal:  Heredity (Edinb)       Date:  2009-02-18       Impact factor: 3.821

Review 9.  A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review.

Authors:  Jacob A Russell; Colin F Funaro; Ysabel M Giraldo; Benjamin Goldman-Huertas; David Suh; Daniel J C Kronauer; Corrie S Moreau; Naomi E Pierce
Journal:  PLoS One       Date:  2012-12-20       Impact factor: 3.240

10.  Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus.

Authors:  Frédéric Landmann; Guillermo A Orsi; Benjamin Loppin; William Sullivan
Journal:  PLoS Pathog       Date:  2009-03-20       Impact factor: 6.823

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  11 in total

Review 1.  The evolution of caste-biasing symbionts in the social hymenoptera.

Authors:  D Treanor; T Pamminger; W O H Hughes
Journal:  Insectes Soc       Date:  2018-06-29       Impact factor: 1.643

2.  Transcriptome Sequencing Reveals Novel Candidate Genes for Cardinium hertigii-Caused Cytoplasmic Incompatibility and Host-Cell Interaction.

Authors:  Evelyne Mann; Corinne M Stouthamer; Suzanne E Kelly; Monika Dzieciol; Martha S Hunter; Stephan Schmitz-Esser
Journal:  mSystems       Date:  2017-11-21       Impact factor: 6.496

3.  Co-infection of Wolbachia and Spiroplasma in spider mite Tetranychus truncatus increases male fitness.

Authors:  Kang Xie; Yi-Jia Lu; Kun Yang; Shi-Mei Huo; Xiao-Yue Hong
Journal:  Insect Sci       Date:  2019-06-28       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.  The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity.

Authors:  Manon Bonneau; Frédéric Landmann; Pierrick Labbé; Fabienne Justy; Mylène Weill; Mathieu Sicard
Journal:  PLoS Pathog       Date:  2018-10-15       Impact factor: 6.823

6.  Reproductive isolation due to prezygotic isolation and postzygotic cytoplasmic incompatibility in parasitoid wasps.

Authors:  Kerstin König; Petra Zundel; Elena Krimmer; Christian König; Marie Pollmann; Yuval Gottlieb; Johannes L M Steidle
Journal:  Ecol Evol       Date:  2019-08-20       Impact factor: 2.912

7.  Exposure to opposing temperature extremes causes comparable effects on Cardinium density but contrasting effects on Cardinium-induced cytoplasmic incompatibility.

Authors:  Matthew R Doremus; Suzanne E Kelly; Martha S Hunter
Journal:  PLoS Pathog       Date:  2019-08-19       Impact factor: 6.823

8.  Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas.

Authors:  Timothy P Driscoll; Victoria I Verhoeve; Cassia Brockway; Darin L Shrewsberry; Mariah Plumer; Spiridon E Sevdalis; John F Beckmann; Laura M Krueger; Kevin R Macaluso; Abdu F Azad; Joseph J Gillespie
Journal:  PeerJ       Date:  2020-12-17       Impact factor: 2.984

9.  Comparative Genomics of Wolbachia-Cardinium Dual Endosymbiosis in a Plant-Parasitic Nematode.

Authors:  Amanda M V Brown; Sulochana K Wasala; Dana K Howe; Amy B Peetz; Inga A Zasada; Dee R Denver
Journal:  Front Microbiol       Date:  2018-10-16       Impact factor: 5.640

10.  Symbiont-mediated cytoplasmic incompatibility: what have we learned in 50 years?

Authors:  J Dylan Shropshire; Brittany Leigh; Seth R Bordenstein
Journal:  Elife       Date:  2020-09-25       Impact factor: 8.140

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