Symbiotic conversations are revealed under genetic interrogation

Abstract

The recent development and application of molecular genetics to the symbionts of invertebrate animal species have advanced our knowledge of the biochemical communication that occurs between the host and its bacterial symbionts. In particular, the ability to manipulate these associations experimentally by introducing genetic variants of the symbionts into naive hosts has allowed the discovery of novel colonization mechanisms and factors. In addition, the role of the symbionts in inducing normal host development has been revealed, and its molecular basis described. In this Review, I discuss many of these developments, focusing on what has been discovered in five well-understood model systems.

Figure 1. Microbial symbioses occur throughout the phylogeny of animals

Experimentally accessible associations, including several that are described in this Review, occur in all the main phylogenetic groups. These associations span the breadth of animal diversity, and are represented in cellular-grade, tissue-grade and organ-grade levels of developmental and morphological complexity.

Figure 2. Classes of symbiosis models

Experimental models of microbial symbioses can be characterized into three types. Gnotobiotic systems (a) have been useful for examining the interactions within the complex consortia that are normally present in vertebrate enteric tracts. In these systems, germ-free host animals are produced, and one or a few bacterial species are introduced to allow an examination of a simplified relationship. An alternative approach is to investigate consortia of invertebrates (b), which are often simpler in species composition. Finally, there are several natural animal models (c) in which only a single bacterial species is present.

Figure 3. Simplified life cycles of five symbioses

In each of the symbioses shown, the animal obtains a specific symbiont (or symbionts), which colonizes the host in a particular location. a | The squid obtains its symbionts from sea-water populations, which colonize the nascent light organ. b | The nematode brings its symbiont into the insect host, where both proliferate. The bacteria then recolonize the nematodes, which escape from the carcass. c | Juvenile leeches obtain symbionts after hatching from their cocoon (perhaps from the cocoon itself). They then take up residence in the crop, where they digest their blood meal. d | The tsetse fly can either pass the symbionts maternally to the eggs or pick up new strains from the environment. e | Specific symbionts on the food of the fruit fly colonize and persist in the enteric tract.

Figure 4. categories of colonization mutants

Microbial symbionts that are passed horizontally must negotiate several stages of the colonization process. Studies of genetically engineered mutant strains have revealed defects that can be placed in one of several classes. In this example, inoculation with a wild-type strain from the environment allows a few symbionts to colonize, which grow to a specific population size that is then stably maintained over time. Three broad classes of defects have been discovered in several symbiotic systems: initiation mutants, which are unable to inoculate the host; accommodation mutants, which fail to reach the usual population size; and persistence mutants, which at first colonize normally, but are unable to maintain themselves.