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

   https://doi.org/10.1002/ece3.5529  

   Garcia, Justine R. ; Larsen, Tyler J. ; Queller, David C. ; Strassmann, Joan E. ( August 2019 , Ecology and Evolution)

   Hosts and their associated microbes can enter into different relationships, which can range from mutualism, where both partners benefit, to exploitation, where one partner benefits at the expense of the other. Many host–microbe relationships have been presumed to be mutualistic, but frequently only benefits to the host, and not the microbial symbiont, have been considered. Here, we address this issue by looking at the effect of host association on the fitness of two facultative members of theDictyostelium discoideummicrobiome (Burkholderia agricolarisandBurkholderia hayleyella). Using two indicators of bacterial fitness, growth rate and abundance, we determined the effect ofD. discoideumonBurkholderiafitness. In liquid culture, we found thatD. discoideumamoebas lowered the growth rate of bothBurkholderiaspecies. In soil microcosms, we tracked the abundance ofBurkholderiagrown with and withoutD. discoideumover a month and found thatB. hayleyellahad larger populations when associating withD. discoideumwhileB. agricolariswas not significantly affected. Overall, we find that bothB. agricolarisandB. hayleyellapay a cost to associate withD. discoideum, butB. hayleyellacan also benefit under some conditions. Understanding how fitness varies in facultative symbionts will help us understand the persistence of host–symbiont relationships.

   This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available athttps://openscholarship.wustl.edu/data/15/

    

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

   https://doi.org/10.1111/mec.14982  

   Haselkorn, Tamara S. ; DiSalvo, Susanne ; Miller, Jacob W. ; Bashir, Usman ; Brock, Debra A. ; Queller, David C. ; Strassmann, Joan E. ( February 2019 , Molecular Ecology)

   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 amoebaDictyostelium discoideum, certain strains ofBurkholderiabacteria 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. SomeBurkholderiastrains 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 ofBurkholderiasymbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates ofD. discoideumand found 25% infected withBurkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions byBurkholderiato the symbiotic lifestyle. Finally, we tested the ability of 38 strains ofBurkholderiafromD. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis inD. discoideum. OnlyD. discoideumnative isolates belonging to theBurkholderia agricolaris,B. hayleyella, andB. bonnieaspecies were able to form persistent symbiotic associations withD. discoideum.TheBurkholderia–Dictyosteliumrelationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.

    

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3. The social amoeba Dictyostelium discoideum rescues Paraburkholderia hayleyella , but not P. agricolaris , from interspecific competition

   https://doi.org/10.1093/femsec/fiad055  

   Medina, James M. ; Queller, David C. ; Strassmann, Joan E. ; Garcia, Justine R. ( May 2023 , FEMS Microbiology Ecology)

   Bacterial endosymbionts can provide benefits for their eukaryotic hosts, but it is often unclear if endosymbionts benefit from these relationships. The social amoeba Dictyostelium discoideum associates with three species of Paraburkholderia endosymbionts, including P. agricolaris and P. hayleyella. These endosymbionts can be costly to the host but are beneficial in certain contexts because they allow D. discoideum to carry prey bacteria through the dispersal stage. In experiments where no other species are present, P. hayleyella benefits from D. discoideum while P. agricolaris does not. However, the presence of other species may influence this symbiosis. We tested if P. agricolaris and P. hayleyella benefit from D. discoideum in the context of resource competition with Klebsiella pneumoniae, the typical laboratory prey of D. discoideum. Without D. discoideum, K. pneumoniae depressed the growth of both Paraburkholderia symbionts, consistent with competition. P. hayleyella was more harmed by interspecific competition than P. agricolaris. We found that P. hayleyella was rescued from competition by D. discoideum, while P. agricolaris was not. This may be because P. hayleyella is more specialized as an endosymbiont; it has a highly reduced genome compared to P. agricolaris and may have lost genes relevant for resource competition outside of its host.

    

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

   https://doi.org/10.7717/peerj.9151  

   Brock, Debra A. ; Noh, Suegene ; Hubert, Alicia N.M. ; Haselkorn, Tamara S. ; DiSalvo, Susanne ; Suess, Melanie K. ; Bradley, Alexander S. ; Tavakoli-Nezhad, Mahboubeh ; Geist, Katherine S. ; Queller, David C. ; et al ( January 2020 , PeerJ)

   Here we give names to three new species of Paraburkholderia that can remain in symbiosis indefinitely in the spores of a soil dwelling eukaryote, Dictyostelium discoideum . The new species P. agricolaris sp. nov. , P. hayleyella sp. nov. , and P. bonniea sp. nov . are widespread across the eastern USA and were isolated as internal symbionts of wild-collected D. discoideum . We describe these sp. nov. using several approaches. Evidence that they are each a distinct new species comes from their phylogenetic position, average nucleotide identity, genome-genome distance, carbon usage, reduced length, cooler optimal growth temperature, metabolic tests, and their previously described ability to invade D. discoideum amoebae and form a symbiotic relationship . All three of these new species facilitate the prolonged carriage of food bacteria by D. discoideum, though they themselves are not food. Further studies of the interactions of these three new species with D. discoideum should be fruitful for understanding the ecology and evolution of symbioses. 

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5. Paraburkholderia symbionts isolated from Dictyostelium discoideum induce bacterial carriage in other Dictyostelium species

   https://doi.org/10.1098/rspb.2023.0977  

   Mather, Rory Vu ; Larsen, Tyler J. ; Brock, Debra A. ; Queller, David C. ; Strassmann, Joan E. ( July 2023 , Proceedings of the Royal Society B: Biological Sciences)

   The social amoeba Dictyostelium discoideum engages in a complex relationship with bacterial endosymbionts in the genus Paraburkholderia, which can benefit their host by imbuing it with the ability to carry prey bacteria throughout its life cycle. The relationship between D. discoideum and Paraburkholderia has been shown to take place across many strains and a large geographical area, but little is known about Paraburkholderia’s potential interaction with other dictyostelid species. We explore the ability of three Paraburkholderia species to stably infect and induce bacterial carriage in other dictyostelid hosts. We found that all three Paraburkholderia species successfully infected and induced carriage in seven species of Dictyostelium hosts. While the overall behaviour was qualitatively similar to that previously observed in infections of D. discoideum, differences in the outcomes of different host/symbiont combinations suggest a degree of specialization between partners. Paraburkholderia was unable to maintain a stable association with the more distantly related host Polysphondylium violaceum. Our results suggest that the mechanisms and evolutionary history of Paraburkholderia’s symbiotic relationships may be general within Dictyostelium hosts, but not so general that it can associate with hosts of other genera. Our work further develops an emerging model system for the study of symbiosis in microbes. 

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