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Vertically transmitted microbiome protects eggs from fungal infection and egg failure

BACKGROUND: Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of thes...

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Autores principales: Bunker, M. E., Elliott, G., Heyer-Gray, H., Martin, M. O., Arnold, A. E., Weiss, S. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8207602/
https://www.ncbi.nlm.nih.gov/pubmed/34134779
http://dx.doi.org/10.1186/s42523-021-00104-5
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author Bunker, M. E.
Elliott, G.
Heyer-Gray, H.
Martin, M. O.
Arnold, A. E.
Weiss, S. L.
author_facet Bunker, M. E.
Elliott, G.
Heyer-Gray, H.
Martin, M. O.
Arnold, A. E.
Weiss, S. L.
author_sort Bunker, M. E.
collection PubMed
description BACKGROUND: Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of these egg-protective bacteria may be facilitated through behavioral mechanisms such as egg-tending, but many species do not provide parental care. Thus, an important mechanism of vertical transfer may be the passage of the egg through the maternal cloaca during oviposition itself. In this study, we examined how oviposition affects eggshell microbial communities, fungal attachment, hatch success, and offspring phenotype in the striped plateau lizard, Sceloporus virgatus, a species with no post-oviposition parental care. RESULTS: Relative to dissected eggs that did not pass through the cloaca, oviposited eggs had more bacteria and fewer fungal hyphae when examined with a scanning electron microscope. Using high throughput Illumina sequencing, we also found a difference in the bacterial communities of eggshells that did and did not pass through the cloaca, and the diversity of eggshell communities tended to correlate with maternal cloacal diversity only for oviposited eggs, and not for dissected eggs, indicating that vertical transmission of microbes is occurring. Further, we found that oviposited eggs had greater hatch success and led to larger offspring than those that were dissected. CONCLUSIONS: Overall, our results indicate that female S. virgatus lizards transfer beneficial microbes from their cloaca onto their eggs during oviposition, and that these microbes reduce fungal colonization and infection of eggs during incubation and increase female fitness. Cloacal transfer of egg-protective bacteria may be common among oviparous species, and may be especially advantageous to species that lack parental care. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00104-5.
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spelling pubmed-82076022021-06-16 Vertically transmitted microbiome protects eggs from fungal infection and egg failure Bunker, M. E. Elliott, G. Heyer-Gray, H. Martin, M. O. Arnold, A. E. Weiss, S. L. Anim Microbiome Research Article BACKGROUND: Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of these egg-protective bacteria may be facilitated through behavioral mechanisms such as egg-tending, but many species do not provide parental care. Thus, an important mechanism of vertical transfer may be the passage of the egg through the maternal cloaca during oviposition itself. In this study, we examined how oviposition affects eggshell microbial communities, fungal attachment, hatch success, and offspring phenotype in the striped plateau lizard, Sceloporus virgatus, a species with no post-oviposition parental care. RESULTS: Relative to dissected eggs that did not pass through the cloaca, oviposited eggs had more bacteria and fewer fungal hyphae when examined with a scanning electron microscope. Using high throughput Illumina sequencing, we also found a difference in the bacterial communities of eggshells that did and did not pass through the cloaca, and the diversity of eggshell communities tended to correlate with maternal cloacal diversity only for oviposited eggs, and not for dissected eggs, indicating that vertical transmission of microbes is occurring. Further, we found that oviposited eggs had greater hatch success and led to larger offspring than those that were dissected. CONCLUSIONS: Overall, our results indicate that female S. virgatus lizards transfer beneficial microbes from their cloaca onto their eggs during oviposition, and that these microbes reduce fungal colonization and infection of eggs during incubation and increase female fitness. Cloacal transfer of egg-protective bacteria may be common among oviparous species, and may be especially advantageous to species that lack parental care. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00104-5. BioMed Central 2021-06-16 /pmc/articles/PMC8207602/ /pubmed/34134779 http://dx.doi.org/10.1186/s42523-021-00104-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Bunker, M. E.
Elliott, G.
Heyer-Gray, H.
Martin, M. O.
Arnold, A. E.
Weiss, S. L.
Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title_full Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title_fullStr Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title_full_unstemmed Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title_short Vertically transmitted microbiome protects eggs from fungal infection and egg failure
title_sort vertically transmitted microbiome protects eggs from fungal infection and egg failure
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8207602/
https://www.ncbi.nlm.nih.gov/pubmed/34134779
http://dx.doi.org/10.1186/s42523-021-00104-5
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