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Abstract Maternal transmission of microbes occurs across the animal kingdom and is vital for offspring development and long-term health. The mechanisms of this transfer are most well-studied in humans and other mammals but are less well-understood in egg-laying animals, especially those with no parental care. Here, we investigate the transfer of maternal microbes in the oviparous phrynosomatid lizard, Sceloporus virgatus. We compared the microbiota of three maternal tissues—oviduct, cloaca, and intestine—to three offspring sample types: egg contents and eggshells on the day of oviposition, and hatchling intestinal tissue on the day of hatching. We found that maternal identity is an important factor in hatchling microbiome composition, indicating that maternal transmission is occurring. The maternal cloacal and oviductal communities contribute to offspring microbiota in all three sample types, with minimal microbes sourced from maternal intestines. This indicates that the maternal reproductive microbiome is more important for microbial inheritance than the gut microbiome, and the tissue-level variation of the adult S. virgatus microbiota must develop as the hatchling matures. Despite differences between adult and hatchling communities, offspring microbiota were primarily members of the Enterobacteriaceae and Yersiniaceae families (Phylum Proteobacteria), consistent with this and past studies of adult S. virgatus microbiomes.
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Recovered microbiome of an oviparous lizard differs across gut and reproductive tissues, cloacal swabs, and faeces
Microbial diversity and community function are related, and can be highly specialized in different gut regions. The cloacal microbiome of Sceloporus virgatus females provides antifungal protection to eggshells, a specialized function that suggests a specialized microbiome. Here, we describe the cloacal, intestinal, and oviductal microbiome from S. virgatus gravid females, adding to growing evidence of microbiome localization in reptiles and other taxa. We further assessed whether common methods for sampling gastrointestinal (GI) microbes – cloacal swabs and feces – provide accurate representations of these microbial communities. We found that different regions of the gut had unique microbial communities. The cloacal microbiome showed extreme specialization averaging 99% Proteobacteria (Phylum) and 83% Enterobacteriacaea (Family). Enterobacteriacaea decreased up the GI and reproductive tracts. Cloacal swabs recovered communities similar to that of lower intestine and cloacal tissues. In contrast, fecal samples had much higher diversity and a distinct composition (common Phyla: 62% Firmicutes, 18% Bacteroidetes, 10% Proteobacteria; common Families: 39% Lachnospiraceae, 11% Ruminococcaceae, 11% Bacteroidaceae) relative to all gut regions. The common families in fecal samples made up < 1% of cloacal tissue samples, increasing to 43% at the upper intestine. Similarly, the common families in gut tissue (Enterobacteriaceae and Helicobacteraceae) made up < 1% of the fecal microbiome. Further, we found that cloacal swabs taken shortly after defecation may be contaminated with fecal matter. Our results serve as a caution against using feces as a proxy for GI microbes, and may help explain high between-sample variation seen in some studies using cloacal swabs.
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- Award ID(s):
- 1755408
- PAR ID:
- 10316551
- Date Published:
- Journal Name:
- Molecular Ecology Resources
- ISSN:
- 1755-098X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/1755-0998.13573
