Vertically transmitted microbiome protects eggs from fungal infection and egg failure

Abstract 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...

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Main Authors: M. E. Bunker, G. Elliott, H. Heyer-Gray, M. O. Martin, A. E. Arnold, S. L. Weiss
Format: Article
Language:English
Published: BMC 2021-06-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-021-00104-5
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spelling doaj-36892c8ccf884f139eb0f09e8be705ff2021-06-20T11:26:47ZengBMCAnimal Microbiome2524-46712021-06-013111310.1186/s42523-021-00104-5Vertically transmitted microbiome protects eggs from fungal infection and egg failureM. E. Bunker0G. Elliott1H. Heyer-Gray2M. O. Martin3A. E. Arnold4S. L. Weiss5Department of Biology, University of Puget SoundDepartment of Biology, University of Puget SoundDepartment of Biology, University of Puget SoundDepartment of Biology, University of Puget SoundSchool of Plant Sciences and Department of Ecology and Evolutionary Biology, University of ArizonaDepartment of Biology, University of Puget SoundAbstract 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.https://doi.org/10.1186/s42523-021-00104-5Antifungal bacteriaCloacaEggshellFitnessIlluminaLizard
collection DOAJ
language English
format Article
sources DOAJ
author M. E. Bunker
G. Elliott
H. Heyer-Gray
M. O. Martin
A. E. Arnold
S. L. Weiss
spellingShingle M. E. Bunker
G. Elliott
H. Heyer-Gray
M. O. Martin
A. E. Arnold
S. L. Weiss
Vertically transmitted microbiome protects eggs from fungal infection and egg failure
Animal Microbiome
Antifungal bacteria
Cloaca
Eggshell
Fitness
Illumina
Lizard
author_facet M. E. Bunker
G. Elliott
H. Heyer-Gray
M. O. Martin
A. E. Arnold
S. L. Weiss
author_sort M. E. Bunker
title 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_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_sort vertically transmitted microbiome protects eggs from fungal infection and egg failure
publisher BMC
series Animal Microbiome
issn 2524-4671
publishDate 2021-06-01
description Abstract 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.
topic Antifungal bacteria
Cloaca
Eggshell
Fitness
Illumina
Lizard
url https://doi.org/10.1186/s42523-021-00104-5
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