Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

Abstract

ABSTRACT The maternal transmission of microbiota during embryonic development of vertebrates is still poorly understood. Here, we used high-throughput sequencing of the 16S rRNA bacterial genes to determine the bacterial communities in the gastrointestinal tract and amniotic environment, i.e., the amniotic fluid, amniotic membrane and extraembryonic yolk, of embryos at the last stage of development of the viviparous lizard Sceloporus grammicus Wiegmann, 1828. We compared these communities to those found in the maternal intestine, mouth, cloaca, and the aseptic ventral skin as a control of the aseptic technique. Our results showed that bacterial 16S rRNA genes were present in the embryos of S. grammicus. Their diversity was lower and more similar in composition between individuals than those found in the maternal tissues. This suggests that a strong control exists on the transmission of bacteria from the mother to the embryos. We found 78% of the embryonic amplicon sequence variants (ASVs) in the maternal bacterial microbiota, suggesting that the transmission of bacteria from the mother to the embryos is a continuous process and some bacteria may have been transferred during early embryonic stages. The embryonic bacteria were found to overlap mostly with those found in the mouth and aseptic ventral skin of the mother, although it is difficult to conclude that the shared ASVs originated from these maternal tissues. Our study provides evidence of microbiota vertical transfer during embryonic development in the animal kingdom. It also highlights that this maternal transmission could be included in the maternal effects that impact the offspring. IMPORTANCE We investigated the presence and diversity of bacteria in the embryos of the viviparous lizard Sceloporus grammicus and their amniotic environment. We compared this diversity to that found in the maternal intestine, mouth, and cloaca. We detected bacterial DNA in the embryos, albeit with a lower bacterial species diversity than found in maternal tissues. Most of the bacterial species detected in the embryos were also found in the mother, although not all of them. Interestingly, we detected a high similarity in the composition of bacterial species among embryos from different mothers. These findings suggest that there may be a mechanism controlling the transmission of bacteria from the mother to the embryo. Our results highlight the possibility that the interaction between maternal bacteria and the embryo may affect the development of the lizards.

Keywords

• early life microbiome
• Is microbiome inherited from the mother?
• maternal effects
• maternal microbiome
• microbial transmission
• reptile microbiome