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DiSalvo, S.

Publications and source records attributed to DiSalvo, S..

5 recordsLinked to original sources

The roles of dispersal limitation and pre-adaptation in shaping Paraburkholderia endosymbiont frequencies in social amoeba communities

Endosymbiotic interactions have long played fundamental roles in shaping the evolution and diversification of eukaryotes. However, we still have a limited understanding of how ecological processes govern the distribution of endosymbionts that are still segregating in host populations. To contribute to this understanding, here we use the interactions between Paraburkholderia endosymbionts and their Dictyostelid social amoeba hosts as a model system to investigate the role of dispersal, a fundamental ecological process, in shaping the distribution and evolution of endosymbiotic interactions. We first found that patterns of endosymbiont diversification were highly biogeographic, suggesting a significant degree of dispersal limitation. We then experimentally mediated the dispersal of several endosymbiont species into environments with multiple host species and found that each symbiont was able to sustain a high prevalence in each host population. The benefit/detriment of these mediated interactions did not change with increasing phylogenetic distance from what is suspected to be the focal amoeba host species in nature. Taken together, our findings suggest Paraburkholderia endosymbionts are generally pre-adapted to occupy a variety of Dictyostelid host environments, and their distribution among host populations is subject to a high degree of dispersal limitation. Overall, our findings have significant implications for our understanding of how ecological processes facilitate and limit the evolution of endosymbiotic interactions. ImportanceEndosymbiotic interactions are ubiquitous in complex eukaryotes, as organelles such as mitochondria and chloroplasts represent the remnants of what were once free-living prokaryotes. However, how ecological processes facilitate the transition from free-living to host-associated is less understood. Selection is the most commonly invoked process to explain this transition: symbionts that are better at infecting hosts and potentially confer some benefit rise in frequency because they are selected for (and otherwise selected against). However, this only describes one fundamental process that can shape the ecology of symbiotic interactions. Here we present evidence that the importance of dispersal (and its limitations) likely exceeds that of selection in shaping the distribution and frequency of Paraburkholderia endosymbionts in their Dictyostelid social amoeba host communities. These findings highlight the need to consider the interaction between ecological processes, rather than individual processes, when understanding the ecology and evolution of endosymbiotic interactions.

evolutionary biology↗

Novel Chlamydiae and Amoebophilus endosymbionts are prevalent in wild isolates of the model social amoebae Dictyostelium discoideum

Amoebae interact with bacteria in diverse and multifaceted ways. Amoeba predation can serve as a selective pressure for the development of bacterial virulence traits. Bacteria may also adapt to life inside amoebae, resulting in symbiotic relationships (pathogenic or mutualistic). Indeed, particular lineages of obligate bacterial endosymbionts have been found in different amoebae. Here, we screened an extensive collection of Dictyostelium discoideum wild isolates for the presence of such bacterial symbionts using PCR primers that identify these endosymbionts. This is the first report of obligate symbionts in this highly-studied amoeba species. They are surprisingly common, identified in 42% of screened isolates (N=730). Members of the Chlamydiae phylum are particularly prevalent, occurring in 27% of the host strains. They are novel and phylogenetically distinct. We also found Amoebophilus symbionts in 8% of screened isolates (N=730). Antibiotic-cured amoebae behave similarly to their endosymbiont-infected counterparts, suggesting that endosymbionts do not significantly impact host fitness, at least in the laboratory. We found several natural isolates were co-infected with multiple endosymbionts, with no obvious fitness effects of co-infection under laboratory conditions. The high prevalence and novelty of amoeba endosymbiont clades in the model organism D. discoideum opens the door to future research on the significance and mechanisms of amoeba-symbiont interactions.

microbiology↗

Intracellular Burkholderia Symbionts Induce Extracellular Secondary Infections; Driving Diverse Host Outcomes that Vary by Genotype and Environment

Symbiotic associations impact and are impacted by their surrounding ecosystem. The association between Burkholderia bacteria and the soil amoeba Dictyostelium discoideum is a tractable model to unravel the biology underlying symbiont-endowed phenotypes and their impacts. Several Burkholderia species stably associate with D. discoideum and typically reduce host fitness in food-rich environments while increasing fitness in food-scarce environments. Burkholderia symbionts are themselves inedible to their hosts but induce co-infections with secondary bacteria that can serve as a food source. Thus, Burkholderia hosts are \"farmers\" that carry food bacteria to new environments, providing a benefit when food is scarce. We examined the ability of specific Burkholderia genotypes to induce secondary co-infections and assessed host fitness under a range of co-infection conditions and environmental contexts. Although all Burkholderia symbionts intracellularly infected Dictyostelium, we found that co-infections are predominantly extracellular, suggesting that farming benefits are derived from extracellular infection of host structures. Furthermore, levels of secondary infection are linked to conditional host fitness; B. agricolaris infected hosts have the highest level of co-infection and have the highest fitness in food scarce environments. This study illuminates the phenomenon of co-infection induction across Dictyostelium associated Burkholderia species and exemplifies the contextual complexity of these associations.

microbiology↗

A complex symbiosis involving within species variation in the response of Dictyostelium amoebae to Burkholderia bacteria

Recent symbioses, particularly facultative ones, are well suited for unravelling the evolutionary give and take between partners. Here we look at variation in wild-collected samples of the social amoeba Dictyostelium discoideum and their relationships with bacterial symbionts, Burkholderia hayleyella and Burkholderia agricolaris. Only about a third of field-collected amoebae carry a symbiont. We cured and cross-infected D. discoideum hosts with different symbiont association histories and then compared the responses of the amoebae to each symbiont type. Before curing, field-collected clones did not vary significantly in overall fitness, but infected hosts produced morphologically different multicellular structures. After curing and re-infecting, host fitness declined overall. However, natural B. hayleyella hosts suffered fewer fitness costs when re-infected with B. hayleyella, indicating that they have evolved mechanisms to tolerate their naturally acquired symbiont. Exploring relationships between endosymbionts and hosts that vary within species may also reveal much about disease dynamics.

microbiology↗

Endosymbiotic adaptations in three new bacterial species associated with Dictyostelium discoideum: Burkholderia agricolaris sp. nov., Burkholderia hayleyella sp. nov., and Burkholderia bonniea sp. nov.

Here we name three species of Burkholderia that can defeat the mechanisms by which bacteria are normally excluded from the spores of a soil dwelling eukaryote Dictyostelium discoideum, which is predatory on bacteria. They are B. agricolaris sp. nov., B. hayleyella sp. nov., and B. bonniea sp. nov. These new species are widespread across the eastern USA and were isolated as internal symbionts of wild collected D. discoideum. Evidence that they are each a distinct new species comes from their phylogenetic position, carbon usage, reduced cell length, cooler optimal growth temperature, and ability to invade D. discoideum amoebae and remain there for generations.

microbiology↗