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Effect of heritable symbionts on maternally-derived embryo transcripts.
Sci Rep. 2019 06 20; 9(1):8847.SR

Abstract

Maternally-transmitted endosymbiotic bacteria are ubiquitous in insects. Among other influential phenotypes, many heritable symbionts of arthropods are notorious for manipulating host reproduction through one of four reproductive syndromes, which are generally exerted during early developmental stages of the host: male feminization; parthenogenesis induction; male killing; and cytoplasmic incompatibility (CI). Major advances have been achieved in understanding mechanisms and identifying symbiont factors involved in reproductive manipulation, particularly male killing and cytoplasmic incompatibility. Nonetheless, whether cytoplasmically-transmitted bacteria influence the maternally-loaded components of the egg or early embryo has not been examined. In the present study, we investigated whether heritable endosymbionts that cause different reproductive phenotypes in Drosophila melanogaster influence the mRNA transcriptome of early embryos. We used mRNA-seq to evaluate differential expression in Drosophila embryos lacking endosymbionts (control) to those harbouring the male-killing Spiroplasma poulsonii strain MSRO-Br, the CI-inducing Wolbachia strain wMel, or Spiroplasma poulsonii strain Hyd1; a strain that lacks a reproductive phenotype and is naturally associated with Drosophila hydei. We found no consistent evidence of influence of symbiont on mRNA composition of early embryos, suggesting that the reproductive manipulation mechanism does not involve alteration of maternally-loaded transcripts. In addition, we capitalized on several available mRNA-seq datasets derived from Spiroplasma-infected Drosophila melanogaster embryos, to search for signals of depurination of rRNA, consistent with the activity of Ribosome Inactivating Proteins (RIPs) encoded by Spiroplasma poulsonii. We found small but statistically significant signals of depurination of Drosophila rRNA in the Spiroplasma treatments (both strains), but not in the symbiont-free control or Wolbachia treatment, consistent with the action of RIPs. The depurination signal was slightly stronger in the treatment with the male-killing strain. This result supports a recent report that RIP-induced damage contributes to male embryo death.

Authors+Show Affiliations

Department Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA. mmateos@tamu.edu.Department Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA. Department Biology, Texas A&M University, College Station, TX, USA.Department Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA.Centro de Ciencias Genómicas (CCG), Universidad Nacional Autónoma de México (UNAM), Cuernavaca, Morelos, Mexico.Department Biology, Texas A&M University, College Station, TX, USA.Department Biology, Texas A&M University, College Station, TX, USA.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

31222094

Citation

Mateos, Mariana, et al. "Effect of Heritable Symbionts On Maternally-derived Embryo Transcripts." Scientific Reports, vol. 9, no. 1, 2019, p. 8847.
Mateos M, Silva NO, Ramirez P, et al. Effect of heritable symbionts on maternally-derived embryo transcripts. Sci Rep. 2019;9(1):8847.
Mateos, M., Silva, N. O., Ramirez, P., Higareda-Alvear, V. M., Aramayo, R., & Erickson, J. W. (2019). Effect of heritable symbionts on maternally-derived embryo transcripts. Scientific Reports, 9(1), 8847. https://doi.org/10.1038/s41598-019-45371-0
Mateos M, et al. Effect of Heritable Symbionts On Maternally-derived Embryo Transcripts. Sci Rep. 2019 06 20;9(1):8847. PubMed PMID: 31222094.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Effect of heritable symbionts on maternally-derived embryo transcripts. AU - Mateos,Mariana, AU - Silva,Nadisha O, AU - Ramirez,Paulino, AU - Higareda-Alvear,Victor M, AU - Aramayo,Rodolfo, AU - Erickson,James W, Y1 - 2019/06/20/ PY - 2018/10/09/received PY - 2019/05/28/accepted PY - 2019/6/22/entrez PY - 2019/6/22/pubmed PY - 2020/11/6/medline SP - 8847 EP - 8847 JF - Scientific reports JO - Sci Rep VL - 9 IS - 1 N2 - Maternally-transmitted endosymbiotic bacteria are ubiquitous in insects. Among other influential phenotypes, many heritable symbionts of arthropods are notorious for manipulating host reproduction through one of four reproductive syndromes, which are generally exerted during early developmental stages of the host: male feminization; parthenogenesis induction; male killing; and cytoplasmic incompatibility (CI). Major advances have been achieved in understanding mechanisms and identifying symbiont factors involved in reproductive manipulation, particularly male killing and cytoplasmic incompatibility. Nonetheless, whether cytoplasmically-transmitted bacteria influence the maternally-loaded components of the egg or early embryo has not been examined. In the present study, we investigated whether heritable endosymbionts that cause different reproductive phenotypes in Drosophila melanogaster influence the mRNA transcriptome of early embryos. We used mRNA-seq to evaluate differential expression in Drosophila embryos lacking endosymbionts (control) to those harbouring the male-killing Spiroplasma poulsonii strain MSRO-Br, the CI-inducing Wolbachia strain wMel, or Spiroplasma poulsonii strain Hyd1; a strain that lacks a reproductive phenotype and is naturally associated with Drosophila hydei. We found no consistent evidence of influence of symbiont on mRNA composition of early embryos, suggesting that the reproductive manipulation mechanism does not involve alteration of maternally-loaded transcripts. In addition, we capitalized on several available mRNA-seq datasets derived from Spiroplasma-infected Drosophila melanogaster embryos, to search for signals of depurination of rRNA, consistent with the activity of Ribosome Inactivating Proteins (RIPs) encoded by Spiroplasma poulsonii. We found small but statistically significant signals of depurination of Drosophila rRNA in the Spiroplasma treatments (both strains), but not in the symbiont-free control or Wolbachia treatment, consistent with the action of RIPs. The depurination signal was slightly stronger in the treatment with the male-killing strain. This result supports a recent report that RIP-induced damage contributes to male embryo death. SN - 2045-2322 UR - https://www.unboundmedicine.com/medline/citation/31222094/Effect_of_heritable_symbionts_on_maternally_derived_embryo_transcripts_ L2 - https://doi.org/10.1038/s41598-019-45371-0 DB - PRIME DP - Unbound Medicine ER -