22-BBSRC/NSF-BIO Hidden costs of infection: mechanisms by which parasites disrupt host-microbe symbioses and alter development
Lead Research Organisation:
John Innes Centre
Department Name: Cell and Develop Biology
Abstract
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.
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.
Technical Summary
Crosstalk between co-colonizing parasites and mutualistic microbes is a critical understudied feature of host-associated communities. Our past worked showed that nematodes inhibit rhizobia nodulation, while the rhizobia increase susceptibility to nematodes. These reciprocal priority effects are almost certainly maladaptive for the host. Current evidence implicates both host defense-mediated and host resources-mediated factors in determining the outcome of co-incident infections, but how these are balanced and how they impact the different species in the interaction in not understood.
We propose that host processes are the primary component of co-colonization interactions. Therefore, we will interrogate how the host's defence response and resource allocation underpin competition and mediate parasite-mutualist interactions in the model legume Medicago truncatula. We will experimentally assess host processes and competition outcomes by infecting plants with a crop parasite (the nematode Meloidogyne hapla) that disrupts the symbiosis with nitrogen-fixing Ensifer meliloti bacteria. Further, we will use genetic manipulation to mechanistically tune host processes to determine how this influences the tri-party interaction.
The proposed research will determine the spatiotemporal scale of the reciprocal priority effects between rhizobia and nematodes and develop new tools to manipulate them (Aim 1); interrogate the relative roles of defence (Aim 2) and carbon allocation (Aim 3) in generating priority effects between parasites and symbionts on the same host; and identify genes and pathways that underlie these priority effects (Aim 4). The rhizobium-Medicago nematode system is ideal for interrogating interspecies competition as the system is genetically tractable, phenotypes are quantitative, and the biology underlying individual interactions is well established.
We propose that host processes are the primary component of co-colonization interactions. Therefore, we will interrogate how the host's defence response and resource allocation underpin competition and mediate parasite-mutualist interactions in the model legume Medicago truncatula. We will experimentally assess host processes and competition outcomes by infecting plants with a crop parasite (the nematode Meloidogyne hapla) that disrupts the symbiosis with nitrogen-fixing Ensifer meliloti bacteria. Further, we will use genetic manipulation to mechanistically tune host processes to determine how this influences the tri-party interaction.
The proposed research will determine the spatiotemporal scale of the reciprocal priority effects between rhizobia and nematodes and develop new tools to manipulate them (Aim 1); interrogate the relative roles of defence (Aim 2) and carbon allocation (Aim 3) in generating priority effects between parasites and symbionts on the same host; and identify genes and pathways that underlie these priority effects (Aim 4). The rhizobium-Medicago nematode system is ideal for interrogating interspecies competition as the system is genetically tractable, phenotypes are quantitative, and the biology underlying individual interactions is well established.
Organisations
People |
ORCID iD |
| Christine Faulkner (Principal Investigator) |