Nematode-bacterium symbioses--cooperation and conflict revealed in the "omics" age

Abstract

Nematodes are ubiquitous organisms that have a significant global impact on ecosystems, economies, agriculture, and human health. The applied importance of nematodes and the experimental tractability of many species have promoted their use as models in various research areas, including developmental biology, evolutionary biology, ecology, and animal-bacterium interactions. Nematodes are particularly well suited for the investigation of host associations with bacteria because all nematodes have interacted with bacteria during their evolutionary history and engage in a variety of association types. Interactions between nematodes and bacteria can be positive (mutualistic) or negative (pathogenic/parasitic) and may be transient or stably maintained (symbiotic). Furthermore, since many mechanistic aspects of nematode-bacterium interactions are conserved, their study can provide broader insights into other types of associations, including those relevant to human diseases. Recently, genome-scale studies have been applied to diverse nematode-bacterial interactions and have helped reveal mechanisms of communication and exchange between the associated partners. In addition to providing specific information about the system under investigation, these studies also have helped inform our understanding of genome evolution, mutualism, and innate immunity. In this review we discuss the importance and diversity of nematodes, "omics"' studies in nematode-bacterial systems, and the wider implications of the findings.

Figure 1

Schematic Overview of Model Nematode-Bacterium Symbioses: Symbiont Location and Life Cycle> A: Xenorhabdus and Photorhabdus (green) are located within infective juveniles (environmental stage) of Steinernema and Heterorhabditis nematodes respectively. The bacteria are located in the lumen between intestinal epithelial cells (grey with dark grey nuclei) (insets). B: The infective juveniles of Sterinernema and Heterorhabditis parasitize insect hosts. The nematodes and bacteria kill the insect and reproduce within the insect cadaver. The nematodes then re-associate with their bacterial symbiont and migrate away from the cadaver into the environment to seek new hosts. C: The ecotsymbiont (green) of Laxus oneistus (grey) is located on the outside of all nematode life stages. The bacteria are arranged in a perpendicular fashion to the exterior of the nematode (inset). D. L. oneistus nematodes grow and reproduce in the sediment of the sea floor. Their thiotrophic ectosymbiont profits from nematode migrations in oxygen and sulfide gradients (see text for more details). E. The Wolbachia symbiont (green) of Brugia malayi nematodes (grey) are localized to the hypodermal cells of the lateral chords in all nematode life stages and the reproductive tissues of females. These bacteria are intracellular (inset). F. B. malayi is transmitted to a human host through a mosquito vector. The nematodes undergo reproduction within the human host and produce a larval stage that can be taken up by new mosquitoes. Larval stages grow within the mosquito and can then infect new human hosts when the mosquito takes a blood meal.