22-BBSRC/NSF-BIO Hidden costs of infection: mechanisms by which parasites disrupt host-microbe symbioses and alter development

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The field of host-microbe interactions is undergoing a paradigm shift. Historically, pairwise interactions between hosts and their parasites, pathogens, and symbionts were primarily studied as isolated pairwise interactions. Now, there is increasing recognition that hosts are ecosystems. An individual plant or animal houses hundreds or even thousands of species of microorganisms that compete with or facilitate each other, either directly or indirectly via their shared host. As a result, consensus is emerging that an ecological framework is critical to understand the assembly and function of host-associated communities. Microorganisms that share the same host affect each other's colonization success. These patterns scale up to entire host-associated microbial communities. Microbiome manipulations show that parasites alter microbiome composition, and that the microbiome in turn can affect a host's parasite load or the colonization success of microbial symbionts. Crosstalk between co-colonizing microorganisms often manifests as a priority effect, in which an early encounter with one microorganism impacts the host's response to later colonizers. Plants that are primed by an encounter with a parasite or pathogen exhibit stronger and more rapid responses. Priority effects are ubiquitous in host-associated communities. Yet, relative to multiparasite or multi-symbiont systems, priority effects between co-colonizing symbionts and parasites remain understudied. The Wood lab recently found that in the legume Medicago, early arriving parasitic nematodes inhibit nodulation by later-arriving nitrogen-fixing rhizobia, while early arriving rhizobia facilitate gall formation. In other words, in co-colonized hosts, the parasite inhibits symbiosis, while the symbiont increases susceptibility to parasite infection. This result is biologically significant because it is almost certainly maladaptive for the host.The Medicago-rhizobia-nematode system is a tractable experimental system in which to discriminate between the relative contribution of resource- and defence-based mechanisms to competition in host-associated communities. Controlled inoculations onto aposymbiotic hosts is straightforward because both rhizobia and nematodes are horizontally transmitted. We will use split-root culture system, in which a plant's root system is split into two pots that are independently manipulated, to disentangle local and systemic responses. Thus, in this proposal we will use genetic, physiological and cell biological approaches to test the hypotheses that priority effects are mediated by host defence responses or alternatively by host resource allocation.