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Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata

The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multip...

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Autores principales: Jennings, Emily C., Korthauer, Matthew W., Hamilton, Trinity L., Benoit, Joshua B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787804/
https://www.ncbi.nlm.nih.gov/pubmed/31624569
http://dx.doi.org/10.1002/ece3.5580
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author Jennings, Emily C.
Korthauer, Matthew W.
Hamilton, Trinity L.
Benoit, Joshua B.
author_facet Jennings, Emily C.
Korthauer, Matthew W.
Hamilton, Trinity L.
Benoit, Joshua B.
author_sort Jennings, Emily C.
collection PubMed
description The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live‐bearing cockroach, Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole‐body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non‐Blattabacteria species are not able to colonize newborn D. punctata until melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk‐like secretions, and mother–offspring interactions during pregnancy.
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spelling pubmed-67878042019-10-17 Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata Jennings, Emily C. Korthauer, Matthew W. Hamilton, Trinity L. Benoit, Joshua B. Ecol Evol Original Research The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live‐bearing cockroach, Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole‐body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non‐Blattabacteria species are not able to colonize newborn D. punctata until melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk‐like secretions, and mother–offspring interactions during pregnancy. John Wiley and Sons Inc. 2019-08-22 /pmc/articles/PMC6787804/ /pubmed/31624569 http://dx.doi.org/10.1002/ece3.5580 Text en © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Jennings, Emily C.
Korthauer, Matthew W.
Hamilton, Trinity L.
Benoit, Joshua B.
Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title_full Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title_fullStr Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title_full_unstemmed Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title_short Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata
title_sort matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, diploptera punctata
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6787804/
https://www.ncbi.nlm.nih.gov/pubmed/31624569
http://dx.doi.org/10.1002/ece3.5580
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