Animals in a bacterial world, a new imperative for the life sciences

Abstract

In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other's genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal-bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

Fig. 1.

Animals through time. (A) Upper atmospheric oxygen concentration, as a percent of current levels, plotted against geological time. (B) Phylogenetic history of life on Earth, scaled to match the oxygen timeline. Note that the origin of the eukaryotes and the subsequent diversification of animals both correspond to periods of increasing atmospheric oxygen. (C) (Left) A phylogeny of choanoflagellates and selected animals, annotated to indicate the evolution of characters particularly relevant to interactions with bacteria. (Right) Interactions between bacteria and eukaryotes, corresponding to the phylogeny. Bacteria are prey, sources of metabolites, inducers of development in symbiosis (morphogenesis) and in larval settlement (environmental cues), and activators of immune systems.

Fig. 2.

The ancestry of humans reflected in the genomic signature. A phylogenetic analysis of the human genes reveals the relative percentage of the genome that arose at a series of stages in biological evolution (20).

Fig. 3.

Signaling within and between the animal and its microbiota. Members of the microbiota, such as those in and on the gut, oral cavity, and skin, communicate among themselves and exchange signals with the animal’s organ systems, participating in the body’s homeostasis. Some of the signals promoting this balance are mentioned in the text (green), whereas other representatives are not (black; Tables S1 and S2). The microbiota also influences animal behavior, creating a direct interface with other organisms. AMP, antimicrobial peptides; LPS, lipopolysaccharide; PGN, peptidoglycan; PSA, polysaccharide A; SCFA, short-chain fatty acids; TMA, trimethylamine oxide.

Fig. 4.

Nested ecological interactions of animals and bacteria and their underlying metabolic bases. (A) A forest canopy insect illustrates the cascading effects of animal-bacterial interactions across multiple spatial scales. Bacterial symbionts (Left), residing in the gut (Center Left), are essential to nutritional success of insect species (Center Right) in tropical forest canopies (Right), where they often make up a majority of animal biomass. (B) Diversity of energy metabolism in bacteria and animals. Animals can ferment and aerobically respire but are unable to perform the vast diversity of other, ecologically vital, energy-harvesting processes. Beyond phototrophy, which they share with plants, bacteria can also contribute to primary production by using inorganic energy sources (lithotrophy) to fix CO₂. Animals are directly or indirectly dependent on bacteria for extracting energy and cycling biomolecules, whereas animals actively contribute to bacterial productivity through bioturbation, nutrient provisioning, and as habitats for colonization and shelter.