Opinion
The Nidobiome: A Framework for Understanding Microbiome Assembly in Neonates

https://doi.org/10.1016/j.tree.2020.03.007Get rights and content

Highlights

  • An animal’s associated microbes (its ‘microbiome’) impact its fitness, representing a significant ecological and evolutionary factor. Animals begin life without a developed microbiome, making the first encounter with environmental microbes particularly important.

  • Nests have been increasingly recognized as important drivers of microbiome assembly in neonates.

  • The nidobiome concept integrates parents, nest, and neonates to better understand initial microbiome assembly. This concept identifies the roles of parents, nest, and neonates as microbiome modifiers, emphasizing their interactions and highlighting gaps in our knowledge of microbiome assembly.

  • It also recognizes the particular developmental stages during which microbial interactions can be especially important. Identification of such stages allows for comparison of microbiome assembly across animal species.

The importance of microbial associations to animals’ development, physiology, and fitness is widely recognized. In most animals, these microbial associations must be developed anew with every generation, making microbiome assembly a critical ecological and evolutionary process. To fully understand neonate microbial colonization, we need to study the interacting effects of neonate, parents, nest, and external environment. We propose an integrative approach based on the concept of the ‘nidobiome’, a new unit of microbiome–host interactions, which brings together these key elements. We discuss the contribution of each element on microbial colonization at different stages of host development, and we provide a framework based on key developmental events to compare microbiome assembly across animal species.

Section snippets

The Need for a New Conceptual Approach to Understanding Microbiome Effects on Neonate Fitness

The importance of microbial associations to animals’ lives is widely recognized [1]. Microbes allow hosts to access nutrients [2], help develop functional organs and systems [3], process toxins [4], and resist pathogens [5], among many other fitness benefits [6]. Although microbes may colonize the reproductive tract of parents and can interact with both gametes since before fertilization [7,8], most healthy newborns begin with scarce microbial associations that rapidly increase in abundance and

Nests Are Central to Microbial Colonization of Neonates

Parents select, modify, and construct particular environments (i.e., nests) where their offspring will be born or hatched [27]. Nests represent the immediate built environment faced by newborns before being exposed to external conditions. Animal clades show different degrees of nest construction (Box 1), with complex nesting behaviors including both invertebrate (e.g., social insects) and vertebrate species (e.g., fish, crocodilians, rodents). At first glance, a nest consists of a defined

The Nidobiome across Time: Using Key Developmental Events to Understand Microbial Assembly and Compare Diverse Life Histories

Merging multiple microbial sources in a time-sensitive context presents a great challenge to understanding microbiome development in neonates. Considering environmental exposure and parental transmission independently simplifies experimental design but introduces conceptual limitations, failing to account for the combined effects of the nest, parents, and the environment on initial microbial colonization. An alternative way to simplify experimental design is to partition microbiome assembly

Concluding Remarks

The goal of the nidobiome concept is to provide a flexible yet detailed framework for the study of initial microbiome assembly. The clear differentiation of elements, processes, and key developmental events should make the nidobiome approach a useful tool for hypothesis testing and experimental design. At the same time, it provides a flexible framework for successful comparisons between different clades from the wide diversity of life histories, allowing the integration of model systems and

Acknowledgments

We thank Dr Elizabeth Miller for several discussions that enriched this opinion paper. We appreciate the comments of the editor Dr Andrea E.A. Stephens and two anonymous reviewers that improved our paper. We thank Aslam Narvaez-Parra (www.paisajeaslam.com) for the great illustrations. Financial support was provided by a CONACYT PhD scholarship to F.C-C. from the Mexican Government (No. 231223) and an award to B.J.M.B. from the National Institute of General Medical Sciences (P01GM125576).

Glossary

Built environment
a modified environment that creates particular conditions that differ from the nonmodified environment. In nests, examples of these modifications can be physical, with walls changing thermal and hydric conditions inside the built environment, or chemical, when providing secretions that prevent microbial growth.
Microbiome
the community of microbes associated with a host, including microbes inhabiting its internal organs and its external surface. Although a majority of the animal

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