Introduction

ANIMALS IN A MICROBIAL WORLD

1.1. What Is An Animal?

We can answer this question in two ways. One answer is relatively straightforward and is provided in the following paragraph, and a first attempt at the really interesting answer occupies the rest of this book.

The animals are a monophyletic group of eukaryotes with a multicellular common ancestor that fed holozoically (i.e., on particulate food) and comprised cells that lacked a cell wall and included multiple morphologically and functionally different cell types. These traits set animals apart from the only other major group of ancestrally multicellular eukaryotes, the terrestrial plants, and other eukaryotes with multicellular representatives, e.g., the fungi and red algae, which have saprophytic or photosynthetic lifestyles and are composed of cells enclosed within a cell wall. Early in their diversification, two key innovations evolved in the animals: the gut, permitting exploitation of large food items; and the nervous system, laying the foundation for the complex behavior displayed by many animals. A further defining feature of the animals is that, as a group, they lack key metabolic capabilities common to various other organisms, including the capacity to photosynthesize, fix nitrogen, synthesize many amino acids contributing to protein, and produce various cofactors required for the function of enzymes central to metabolism. In other words, many animals are morphologically complex and some are clever, but all are metabolically impoverished.

This description of animals is not incorrect, but it is incomplete. It omits 1-10% of the biomass and half or more of the cells in the animal body. The missing cells are the microbial communities that live persistently with the animal. Most of these microorganisms are bacteria, but they also include unicellular eukaryotes; and large animals additionally bear multicellular eukaryotes, including mycelial fungi, mites, helminth worms, etc. Traditionally, these inhabitants of animals have been ignored unless they are injurious to the health of their animal host, and because many are difficult to culture, their ubiquity and diversity are grossly underestimated by routine culture-based microbiological methods.

The study of microorganisms associated with animals has been transformed by culture-independent methods to identify and study the function of microorganisms. The key technology has been high throughput DNA sequencing (also known as next generation sequencing), by which all the DNA, expressed genes, or specific genomic regions of interest in a sample can be sequenced simultaneously. It is now possible to determine the taxa in the microbial community and their functional traits, for example from a biopsy taken from the lung or intestine of a human patient, from a single soil microarthropod, or from the gills of a bivalve mollusk brought up from a deep sea hydrothermal vent. These everimproving technologies have supported a decade or more of research on the microbiological natural history of animal bodies. It is now apparent that animals are the habitat for a previously unsuspected diversity and abundance of microbial residents, and this unfolding discovery has empowered experimental science, revealing that these microorganisms are critical to the health and well-being of their animal hosts.

So, what is an animal? It is a multiorganismal entity, comprising animal cells and microbial cells. The phenotype of an animal is not the product of animal genes, proteins, cells, tissues, and organs alone, but the product of the interactions between all of these animal functions with communities of microorganisms, whose composition and function vary with the age, physiological condition, and genotype of their animal host. Following from the growing appreciation of the significance of the microbiology of animals, many aspects of animal biology are being rewritten (McFall-Ngai et al., 2013). The biomedical sciences are increasingly recognizing the pervasive effects of resident microorganisms on human health. These effects extend beyond local impacts, for example of gut microorganisms on gut health and disease, to microbial effects on cardiovascular health, the integrity of the circadian rhythm, and psychiatric health. Many evolutionary biologists are realizing that the response of animals to selection is influenced by the impact of microbial partners on the trait under selection and the heritability of the microorganisms. Applied biologists are appreciating that microbes can shape the capacity of insects, such as mosquitoes, to vector disease agents (e.g., the malaria parasite, dengue virus) and their susceptibility to certain pestcontrol agents. Furthermore, reliable predictions of the impacts of climate change on animal distributions will require consideration of the environmental requirements and dispersal capability of the microbial partners as well as the animal.

But, before we go any further, we need to address some issues of terminology. As with so many scientific disciplines, multiple terms are being used, sometimes interchangeably but often with different shades of meaning that can sow confusion and misunderstanding. Section 1.2 provides a guide to how some terms are used in this book, as well as why some terms are eschewed.

1.2. Terminology: Dismantling the Tower of Babel

Terms are important not only because they communicate agreed concepts within a discipline but also because they can encapsulate an entire conceptual framework. In this respect, the term "microbiome," coined to describe the catalog of microorganisms and their genes (Lederberg and McCray, 2001), is of central importance. The microbiome is a global, all-encompassing term for the microbiology of an animal, and is particularly useful where, as in shot-gun sequencing, individual genes cannot readily be assigned to particular microbial taxa. A related term is "microbiota," which refers specifically to the microbial taxa associated with an animal. The terms microbiome and microbiota are sometimes used interchangeably when referring to taxa. Alternatively, the microbiome can be used exclusively to refer to genes and genomes, with the microbiota as a taxonomic descriptor. It is usually obvious from the context how the term microbiome is being used. In this book, I will use both terms, with microbiome to describe inventories of genes, especially in relation to function, and microbiota when referring to the organisms.

The terms microbiome and microbiota have meaning for a science that is founded on molecular biology and genomics. A major driver of microbiome research over the last decade has been large consortium projects that have generated microbial sequences associated with humans, and their potential biomedical importance. However, microbiome...