Abstract

This paper reviews current research on the microbial life that surrounds vertebrate embryos. Several clades are believed to develop inside sterile—or near-sterile—embryonic microhabitats, while others thrive within a veritable zoo of microbial life. The occurrence of embryo-associated microbes in some groups, but not others, is an under-appreciated transition (possibly transitions) in vertebrate evolution. A lack of comparable studies makes it currently impossible to correlate embryo-associated microbiomes with other aspects of vertebrate evolution. However, there are embryonic features that should instruct a more targeted survey. This paper concludes with a hypothesis for the role of multiciliated surface cells in amphibian and some fish embryos, which may contribute to managing embryo-associated microbial consortia. These cells are known to exist in some species that harbor in ovo microbes or have relatively porous egg capsules, although most have not been assayed for embryo-associated microbiota. Whether the currents generated within these extraembryonic microhabitats contribute to culturing consistent microbial communities remains to be seen.

Highlights

  • Since the beginning of the 21st century, the life sciences have experienced a revolution in our understanding of microbial interactions with multicellular life

  • This review proposes that comparative studies of microbial interactions with vertebrate embryos offer similar opportunities to interrogate these rules of engagement

  • There has been a strong emphasis on the potential implications of embryo-associated microbiomes in the recent literature [1,2,6,189,190]

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Summary

Introduction

Since the beginning of the 21st century, the life sciences have experienced a revolution in our understanding of microbial interactions with multicellular life. The revelation that we are “animals in a bacterial world” [1,2] has largely been driven by new culture-free microbial identification techniques. These include rDNA metabarcoding [3] as well as the sequencing of entire microbial communities, or metagenomics [4]. Parallel lines of research have identified organisms that do not require a (primarily gut) microbiome [5]. These apparent outliers indicate potential constraints on otherwise common host-microbiota interactions. By reviewing the evidence at hand, this paper aims to identify gaps in our understanding in order to prioritize future efforts in vertebrate embryo-microbe research

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