Paraburkholderia Symbionts Display Variable Infection Patterns That Are Not Predictive of Amoeba Host Outcomes

Abstract

Symbiotic interactions exist within a parasitism to mutualism continuum that is influenced, among others, by genes and context. Dynamics of intracellular invasion, replication, and prevalence may underscore both host survivability and symbiont stability. More infectious symbionts might exert higher corresponding costs to hosts, which could ultimately disadvantage both partners. Here, we quantify infection patterns of diverse Paraburkholderia symbiont genotypes in their amoeba host Dictyostelium discoideum and probe the relationship between these patterns and host outcomes. We exposed D. discoideum to thirteen strains of Paraburkholderia each belonging to one of the three symbiont species found to naturally infect D. discoideum: Paraburkholderia agricolaris, Paraburkholderia hayleyella, and Paraburkholderia bonniea. We quantified the infection prevalence and intracellular density of fluorescently labeled symbionts along with the final host population size using flow cytometry and confocal microscopy. We find that infection phenotypes vary across symbiont strains. Symbionts belonging to the same species generally display similar infection patterns but are interestingly distinct when it comes to host outcomes. This results in final infection loads that do not strongly correlate to final host outcomes, suggesting other genetic factors that are not a direct cause or consequence of symbiont abundance impact host fitness.

Context-dependence in the symbiosis between Dictyostelium discoideum and Paraburkholderia

“…Each patch produces a number of spores, drawn from the distribution of our empirical spore production values, according to whether it is a food-rich or food-poor patch. Infected hosts have been found to have reduced spore production in food-rich environments that depends on infection density of Paraburkholderia endosymbionts (Brock et al 2011;DiSalvo et al 2015;Miller et al 2020). We did not detect this cost in our data, perhaps because we infected with fewer Paraburkholderia.…”

“…We varied the frequency of food-poor soil patches and calculated a phenotype's success as the geometric or arithmetic mean spore production. We included the cost of infection observed in other studies (DiSalvo et al 2015;Shu et al 2018a;Haselkorn et al 2019;Miller et al 2020) by subtracting some proportion of spores from our empirical measures for infected hosts in food-rich conditions. We classified a phenotype as a bet-hedger if the best phenotype in terms of geometric mean fitness differed from the best phenotype in terms of arithmetic mean fitness (Figure 4B).…”

Evolutionary Genetics of Microbial Symbiosis

“…In this Special Issue, we present a collection of new reviews and original research papers that target the genetic machinery behind the evolution of microbial symbioses, using both classical and novel experimental model systems. These include microbial symbioses with arthropod hosts [3][4][5], leguminous plants [6,7], social amoebae [8], and the largely understudied symbiosis of fungi in insects [9]. These papers provide key examples of current research on the microbial genetic repertoire (genes, genomic features, and their molecular evolution) and metabolic interactions (including biochemical and cellular mechanisms) involved in symbiotic interplay.…”

“…These environmentally acquired bacteria are incredibly diverse in their host range and in the phenotypes that they induce (from mutualism to pathogenesis). Here Takeshita and Kikuchi (2020) and Miller et al (2020) explore the nature of the Burkholderia symbiosis in insects [4] and amoebae [8], respectively. Takeshita and Kikuchi present a genomic study on the bean bug symbiosis with Burkholderia bacteria, which are environmentally acquired and harbored in the host midgut.…”

“…Their comparative genomic analysis highlights genes and functions conserved with other stink bug-associated Burkholderia, which may be essential for gut adaptation in insects. Miller et al (2020) explored infection patterns of Paraburkholderia symbionts in the social amoeba Dictyostelium discoideum, a powerful experimental model to study the mechanism of bacterial infection and pathogenesis [8,11]. By exposing the amoebae to several bacterial strains of three Paraburkholderia species, they found that an increase in bacterial infection titer is not detrimental to host spore productivity (i.e., it does not appear to impose a large fitness cost).…”