The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence, species, genetic and phenotypic diversity

Abstract

The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoeba Dictyostelium discoideum, certain strains of Burkholderia bacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. Some Burkholderia strains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence of Burkholderia symbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates of D. discoideum and found 25% infected with Burkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions by Burkholderia to the symbiotic lifestyle. Finally, we tested the ability of 38 strains of Burkholderia from D. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis in D. discoideum. Only D. discoideum native isolates belonging to the Burkholderia agricolaris, B. hayleyella, and B. bonniea species were able to form persistent symbiotic associations with D. discoideum. The Burkholderia–Dictyostelium relationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.

Fitness costs and benefits vary for two facultative Burkholderia symbionts of the social amoeba, Dictyostelium discoideum

“…They were collected from a variety of locations over a period of years, mostly by our laboratory group [but see (Francis & Eisenberg, ); Table ]. Some of these clones consistently harbored Burkholderia, and subsequent analysis has shown that about 25% of wild D. discoideum harbor one or more Burkholderia species [though the percentage of infected D. discoideum varies significantly in different locations; (Haselkorn et al, )]. The original, wild‐caught host and symbiont pairings have been preserved in glycerol stock, and we refer to these as “native” infections.…”

“…The original, wild‐caught host and symbiont pairings have been preserved in glycerol stock, and we refer to these as “native” infections. We have found that all D. discoideum ‐associated Burkholderia tested to date can infect D. discoideum clones other than their original host (Haselkorn et al, ) and we call these “non‐native” infections. In this study, all experiments were done with native host–symbiont pairings.…”

“…In the wild, D. discoideum contains a small microbiome of edible and inedible bacteria (Brock, Haselkorn, et al, ). Of these bacteria, three Burkholderia species confer upon D. discoideum the ability to carry bacterial prey during dispersal (Figure b; Brock, Douglas, Queller, & Strassmann, ; Brock, Hubert, et al, ; DiSalvo et al, ; Haselkorn et al, ). This provides a fitness advantage to D. discoideum when there is not an acceptable food source in the new location (Figure b; Brock et al, ; DiSalvo et al, ), but decreases slug migration distance (Brock, Jones, Queller, & Strassmann, ) and is costly when a Burkholderia infection is newly established (Shu, Brock, et al, ) or when food is abundant (Brock et al, ).…”

“…In this study, we use the D. discoideum–Burkholderia system to investigate the effect of symbiosis on the fitness of facultative symbionts (Figure ). We focused on two of the three Burkholderia symbiont species ( B. agricolaris and B. hayleyella ) because they encompass most of the phenotypic and genotypic diversity found in the D. discoideum symbionts (Haselkorn et al, ). In experiment 1, we measured the effect of D. discoideum on the growth rate of independent, nonsymbiotic Burkholderia cells in liquid culture (Figure c).…”

A brief historical and evolutionary perspective on the origin of cellular microbiology research

“…This interaction even turns out to induce a “ménage à trois” in which Burkholderia not only forces the otherwise bactivorous amoebae to carry them in their spores but to also become “tolerant” to food bacteria that are normally, in absence of Burkholderia , rapidly killed and degraded in their phagosomes (Shu et al, ). Extended studies now show that several bacteria genera are able to evade phagocytosis and persist in D. discoideum cells and spores through one or more social cycles, creating a form of semistable and mutualistic proto‐microbiome, which might play an important role in supporting D. discoideum growth in nutrient‐poor conditions (Brock et al, ; Haselkorn et al, ).…”