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

Brock, Debra A.; Hubert, Alicia N.M.; Noh, Suegene; DiSalvo, Susanne; Geist, Katherine S; Haselkorn, Tamara S.; Queller, David C.; Strassmann, Joan E.

doi:10.1101/304352

Cited by 12 publications

(18 citation statements)

References 22 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We cannot, however, rule out “long branch attraction” causing the grouping of B. hayleyella and B. bonniea , which is a pattern seen in many endosymbionts that have undergone rapid sequence evolution, genome degradation and nucleotide composition bias (Moran, McCutcheon, & Nakabachi, ; Ruano‐Rubio & Fares, ). However, a phylogeny using k‐mers based on the entire genome sequence of Burkholderia exemplars, retains this pattern (Brock, Hubert, et al, ).…”

Section: Resultsmentioning

confidence: 99%

“…Burkholderia haplotypes outside of these species (Figure 2 (atpD, gltB, lepA, phaC, and trpB) shows 10 unique haplotypes of persistently associating Burkholderia (B. agricolaris, B. hayleyella, and B. bonniea) is a pattern seen in many endosymbionts that have undergone rapid sequence evolution, genome degradation and nucleotide composition bias (Moran, McCutcheon, & Nakabachi, 2008;Ruano-Rubio & Fares, 2007). However, a phylogeny using k-mers based on the entire genome sequence of Burkholderia exemplars, retains this pattern (Brock, Hubert, et al, 2018).…”

Section: The Multi-locus Phylogeny Of Burkholderia Shows At Least Tmentioning

confidence: 97%

See 1 more Smart Citation

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

et al. 2019

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: The Multi-locus Phylogeny Of Burkholderia Shows At Least Tmentioning

confidence: 97%

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

et al. 2019

Self Cite

View full text Add to dashboard Cite

show abstract

“…It is unclear whether this fitness misalignment/conflict is due to recency of establishment. Phylogenetic placement suggests B. hayleyella has been evolving in isolation from related Burkholderia for a long time (Brock, Hubert, et al, ; Haselkorn et al, ), perhaps as a result of being an intracellular symbiont of D. discoideum . The genome sizes of the Burkholderia symbionts also align with this possibility.…”

Section: Discussionmentioning

confidence: 99%

“…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, ).…”

Section: Introductionmentioning

confidence: 99%

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

Garcia

Larsen

Queller

et al. 2019

Ecology and Evolution

Self Cite

View full text Add to dashboard Cite

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 the Dictyostelium discoideum microbiome (Burkholderia agricolaris and Burkholderia hayleyella). Using two indicators of bacterial fitness, growth rate and abundance, we determined the effect of D. discoideum on Burkholderia fitness. In liquid culture, we found that D. discoideum amoebas lowered the growth rate of both Burkholderia species. In soil microcosms, we tracked the abundance of Burkholderia grown with and without D. discoideum over a month and found that B. hayleyella had larger populations when associating with D. discoideum while B. agricolaris was not significantly affected. Overall, we find that both B. agricolaris and B. hayleyella pay a cost to associate with D. discoideum, but B. hayleyella can also benefit under some conditions. Understanding how fitness varies in facultative symbionts will help us understand the persistence of host–symbiont relationships. OPEN RESEARCH BADGES 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 at https://openscholarship.wustl.edu/data/15/

show abstract

“…We tested three B. agricolaris (B1qs70, B1qs159 and B1nc21) and three B. hayleyella (B2qs11, B2qs21 and B2nc28) Burkholderia clones. We also used three non-carried Burkholderia species (Burkholderia unamae, Burkholderia tuberum and Burkholderia silvatlantica, [74]) to see if attraction to D. discoideum is specific to the carried species ( Fig. 1).…”

Section: Burkholderia Isolates From Wild D Discoideum Farmersmentioning

confidence: 99%

Burkholderia bacteria use chemotaxis to find social amoeba Dictyostelium discoideum hosts

et al. 2018

Self Cite

View full text Add to dashboard Cite

A key question in cooperation is how to find the right partners and maintain cooperative relationships. This is especially challenging for horizontally transferred bacterial symbionts where relationships must be repeatedly established anew. In the social amoeba Dictyostelium discoideum farming symbiosis, two species of inedible Burkholderia bacteria (Burkholderia agricolaris and Burkholderia hayleyella) initiate stable associations with naive D. discoideum hosts and cause carriage of additional bacterial species. However, it is not clear how the association between D. discoideum and its carried Burkholderia is formed and maintained. Here, we look at precisely how Burkholderia finds its hosts. We found that both species of Burkholderia clones isolated from D. discoideum, but not other tested Burkholderia species, are attracted to D. discoideum supernatant, showing that the association is not simply the result of haphazard engulfment by the amoebas. The chemotactic responses are affected by both partners. We find evidence that B. hayleyella prefers D. discoideum clones that currently or previously carried Burkholderia, while B. agricolaris does not show this preference. However, we find no evidence of Burkholderia preference for their own host clone or for other hosts of their own species. We further investigate the chemical differences of D. discoideum supernatants that might explain the patterns shown above using a mass spectrometry based metabolomics approach. These results show that these bacterial symbionts are able to preferentially find and to some extent choose their unicellular partners. In addition, this study also suggests that bacteria can actively search for and target phagocytic cells, which may help us better understand how bacteria interact with immune systems.

show abstract

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

Cited by 12 publications

References 22 publications

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

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

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

Burkholderia bacteria use chemotaxis to find social amoeba Dictyostelium discoideum hosts

Contact Info

Product

Resources

About