Symbiont location, host fitness, and possible coadaptation in a symbiosis between social amoebae and bacteria

AbstractRecent 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 amoebaDictyostelium discoideumand their relationships with bacterial symbionts,Burkholderia hayleyellaandBurkholderia agricolaris. Only about a third of field-collected amoebae carry a symbiont. We cured and cross-infectedD. discoideumhosts 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, naturalB. hayleyellahosts suffered fewer fitness costs when re-infected withB. 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.

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Cooperation and conflict in the social amoeba Dictyostelium discoideum

The International Journal of Developmental Biology ◽

10.1387/ijdb.190158jm ◽

2019 ◽

Vol 63 (8-9-10) ◽

pp. 371-382

Author(s):

James M. Medina ◽

P.M. Shreenidhi ◽

Tyler J. Larsen ◽

David C. Queller ◽

Joan E. Strassmann

Keyword(s):

Dictyostelium Discoideum ◽

Fruiting Body ◽

Sexual Cycle ◽

Evolution Of Cooperation ◽

Bacterial Symbionts ◽

Spore Dispersal ◽

Social Amoeba ◽

The Social ◽

The Relationship ◽

Insight Into

The social amoeba Dictyostelium discoideum has provided considerable insight into the evolution of cooperation and conflict. Under starvation, D. discoideum amoebas cooperate to form a fruiting body comprised of hardy spores atop a stalk. The stalk development is altruistic because stalk cells die to aid spore dispersal. The high relatedness of cells in fruiting bodies in nature implies that this altruism often benefits relatives. However, since the fruiting body forms through aggregation there is potential for non-relatives to join the aggregate and create conflict over spore and stalk fates. Cheating is common in chimeras of social amoebas, where one genotype often takes advantage of the other and makes more spores. This social conflict is a significant force in nature as indicated by rapid rates of adaptive evolution in genes involved in cheating and its resistance. However, cheating can be prevented by high relatedness, allorecognition via tgr genes, pleiotropy and evolved resistance. Future avenues for the study of cooperation and conflict in D. discoideum include the sexual cycle as well as the relationship between D. discoideum and its bacterial symbionts. D. discoideum’s tractability in the laboratory as well as its uncommon mode of aggregative multicellularity have established it as a promising model for future studies of cooperation and conflict.

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Exposure to dense bacteria lawns does not cause the social amoeba Dictyostelium discoideum to carry bacteria through the social stage

10.7287/peerj.preprints.2698v1 ◽

2017 ◽

Author(s):

Debra A Brock ◽

Alicia Canas ◽

Kai Jones ◽

David C Queller ◽

Joan E Strassmann

Keyword(s):

Dictyostelium Discoideum ◽

Associated Bacteria ◽

Social Amoeba ◽

Future Studies ◽

Bacterial Cultures ◽

Large Numbers ◽

The Social ◽

External Forces ◽

Social Amoebae ◽

Food Bacteria

Background. Interactions between eukaryotic amoebae and bacteria are understudied and important. Bacteria inside of amoebae are protected from external forces including antibiotics. An excellent model for bacteria-amoeba interactions is the social amoeba Dictyostelium discoideum and its associated bacteria. A third of wild-collected clones of the soil-dwelling amoeba Dictyostelium discoideum exhibit a suite of characteristics that make them simple farmers of bacteria. They carry bacteria internally through the social spore-making stage. They then release these bacteria to grow and subsequently eat them, prudently stopping before they are entirely consumed so some bacteria can be carried to the next generation. D. discoideum defend their food bacteria with other inedible bacteria that produce compounds toxic to non-farmers. Both carried bacteria and social amoeba hosts have demonstrated co-evolved characteristics. Most farmer clones discovered to date carry inedible Burkholderia in addition to food bacteria, but it is not clear whether or not a preponderance of naïve bacteria might induce the farming state by overwhelming the phagocytic actions of the host amoebae. In this study we address this question with D. discoideum clones that naturally carry bacteria and those that do not. Will naïve bacteria in large numbers succeed in colonizing the amoebae? Methods. We grew five non-farmer clones and five farmer clones of wild-collected Dictyostelium discoideum on three different concentrations of a highly palatable bacterial food source, Klebsiella pneumoniae. We then tested them to see if they carried bacteria through the social stage. Results. We found that bacterial density did not have a significant effect on whether or not the clones carried bacteria through the social stage. Even those grown in very dense bacterial cultures were able to shed them successfully unless they were also carrying Burkholderia. Discussion. Our results indicate that even a preponderance of food bacteria cannot overwhelm the ability of social amoebae to digest and not carry bacteria. Apparently, only the inedible Burkholderia have that effect. This points to the importance of understanding co-infection with multiple bacteria because those that cannot induce carriage can nevertheless become carried, foiling digestive processes, but only in the presence of another bacterium. Future studies of host bacteria interactions should consider using multiple bacteria simultaneously.

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

Ecology and Evolution ◽

10.1002/ece3.5529 ◽

2019 ◽

Vol 9 (17) ◽

pp. 9878-9890 ◽

Cited By ~ 3

Author(s):

Justine R. Garcia ◽

Tyler J. Larsen ◽

David C. Queller ◽

Joan E. Strassmann

Keyword(s):

Dictyostelium Discoideum ◽

Costs And Benefits ◽

Fitness Costs ◽

Social Amoeba ◽

The Social

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Microbiome management in the social amoeba Dictyostelium discoideum compared to humans

The International Journal of Developmental Biology ◽

10.1387/ijdb.190240ak ◽

2019 ◽

Vol 63 (8-9-10) ◽

pp. 447-450 ◽

Cited By ~ 5

Author(s):

Timothy Farinholt ◽

Christopher Dinh ◽

Adam Kuspa

Keyword(s):

Recent Work ◽

Dictyostelium Discoideum ◽

Immune Cells ◽

Molecular Mechanisms ◽

Innate Immune ◽

Innate Immune Cells ◽

Social Amoeba ◽

The Social ◽

Physical Barriers ◽

Social Amoebae

Social amoebae and humans use common strategies to orchestrate their interactions with the bacteria in their respective environments and within their bodies. These strategies include the elimination of bacteria by phagocytosis, the establishment of mutualistic interactions, the elaboration of physical barriers, and the deployment of innate immune cells. Many of the molecular mechanisms that humans and social amoebae employ differ, but there are striking similarities that may inform studies in each organism. In this topical review we highlight the similarities and consider what we might learn by comparing these highly divergent species. We focus on recent work in Dictyostelium discoideum with hopes of stimulating work in this area and with the expectation that new mechanistic details uncovered in social amoebae-bacteria interactions will inform microbiome management in humans.

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Sex Determination in the Social Amoeba Dictyostelium discoideum

Science ◽

10.1126/science.1197423 ◽

2010 ◽

Vol 330 (6010) ◽

pp. 1533-1536 ◽

Cited By ~ 69

Author(s):

Gareth Bloomfield ◽

Jason Skelton ◽

Alasdair Ivens ◽

Yoshimasa Tanaka ◽

Robert R. Kay

Keyword(s):

Sex Determination ◽

Dictyostelium Discoideum ◽

Genetic Locus ◽

Model Organism ◽

Mating Types ◽

Type Locus ◽

Social Amoeba ◽

The Third ◽

The Social ◽

Social Amoebae

The genetics of sex determination remain mysterious in many organisms, including some that are otherwise well studied. Here we report the discovery and analysis of the mating-type locus of the model organism Dictyostelium discoideum. Three forms of a single genetic locus specify this species' three mating types: two versions of the locus are entirely different in sequence, and the third resembles a composite of the other two. Single, unrelated genes are sufficient to determine two of the mating types, whereas homologs of both these genes are required in the composite type. The key genes encode polypeptides that possess no recognizable similarity to established protein families. Sex determination in the social amoebae thus appears to use regulators that are unrelated to any others currently known.

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Exposure to dense bacteria lawns does not cause the social amoeba Dictyostelium discoideum to carry bacteria through the social stage

10.7287/peerj.preprints.2698 ◽

2017 ◽

Author(s):

Debra A Brock ◽

Alicia Canas ◽

Kai Jones ◽

David C Queller ◽

Joan E Strassmann

Keyword(s):

Dictyostelium Discoideum ◽

Associated Bacteria ◽

Social Amoeba ◽

Future Studies ◽

Bacterial Cultures ◽

Large Numbers ◽

The Social ◽

External Forces ◽

Social Amoebae ◽

Food Bacteria

Background. Interactions between eukaryotic amoebae and bacteria are understudied and important. Bacteria inside of amoebae are protected from external forces including antibiotics. An excellent model for bacteria-amoeba interactions is the social amoeba Dictyostelium discoideum and its associated bacteria. A third of wild-collected clones of the soil-dwelling amoeba Dictyostelium discoideum exhibit a suite of characteristics that make them simple farmers of bacteria. They carry bacteria internally through the social spore-making stage. They then release these bacteria to grow and subsequently eat them, prudently stopping before they are entirely consumed so some bacteria can be carried to the next generation. D. discoideum defend their food bacteria with other inedible bacteria that produce compounds toxic to non-farmers. Both carried bacteria and social amoeba hosts have demonstrated co-evolved characteristics. Most farmer clones discovered to date carry inedible Burkholderia in addition to food bacteria, but it is not clear whether or not a preponderance of naïve bacteria might induce the farming state by overwhelming the phagocytic actions of the host amoebae. In this study we address this question with D. discoideum clones that naturally carry bacteria and those that do not. Will naïve bacteria in large numbers succeed in colonizing the amoebae? Methods. We grew five non-farmer clones and five farmer clones of wild-collected Dictyostelium discoideum on three different concentrations of a highly palatable bacterial food source, Klebsiella pneumoniae. We then tested them to see if they carried bacteria through the social stage. Results. We found that bacterial density did not have a significant effect on whether or not the clones carried bacteria through the social stage. Even those grown in very dense bacterial cultures were able to shed them successfully unless they were also carrying Burkholderia. Discussion. Our results indicate that even a preponderance of food bacteria cannot overwhelm the ability of social amoebae to digest and not carry bacteria. Apparently, only the inedible Burkholderia have that effect. This points to the importance of understanding co-infection with multiple bacteria because those that cannot induce carriage can nevertheless become carried, foiling digestive processes, but only in the presence of another bacterium. Future studies of host bacteria interactions should consider using multiple bacteria simultaneously.

Download Full-text