scholarly journals Context, competition, and symbiont-induced bet-hedging between Dictyostelium discoideum and Paraburkholderia

2021 ◽  
Author(s):  
Trey J. Scott ◽  
David C. Queller ◽  
Joan E. Strassmann

AbstractSymbiotic interactions change with environmental context. We investigated context-dependence and bet-hedging in the symbiosis between social amoeba hosts and Paraburkholderia bacteria, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food-rich environments, but aid hosts dispersed to food-poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food-rich context. Second, it matters for host-symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data-based simulations show in some cases this context-dependence can lead to a symbiont-induced bet-hedging advantage for hosts. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and suggest that symbionts can induce bet-hedging in hosts.

2017 ◽  
Author(s):  
Debra A Brock ◽  
Alicia Canas ◽  
Kai Jones ◽  
David C Queller ◽  
Joan E Strassmann

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.


2016 ◽  
Vol 283 (1829) ◽  
pp. 20152727 ◽  
Author(s):  
Debra A. Brock ◽  
W. Éamon Callison ◽  
Joan E. Strassmann ◽  
David C. Queller

The social amoeba Dictyostelium discoideum is unusual among eukaryotes in having both unicellular and multicellular stages. In the multicellular stage, some cells, called sentinels, ingest toxins, waste and bacteria. The sentinel cells ultimately fall away from the back of the migrating slug, thus removing these substances from the slug. However, some D. discoideum clones (called farmers) carry commensal bacteria through the multicellular stage, while others (called non-farmers) do not. Farmers profit from their beneficial bacteria. To prevent the loss of these bacteria, we hypothesize that sentinel cell numbers may be reduced in farmers, and thus farmers may have a diminished capacity to respond to pathogenic bacteria or toxins. In support, we found that farmers have fewer sentinel cells compared with non-farmers. However, farmers produced no fewer viable spores when challenged with a toxin. These results are consistent with the beneficial bacteria Burkholderia providing protection against toxins. The farmers did not vary in spore production with and without a toxin challenge the way the non-farmers did, which suggests the costs of Burkholderia may be fixed while sentinel cells may be inducible. Therefore, the costs for non-farmers are only paid in the presence of the toxin. When the farmers were cured of their symbiotic bacteria with antibiotics, they behaved just like non-farmers in response to a toxin challenge. Thus, the advantages farmers gain from carrying bacteria include not just food and protection against competitors, but also protection against toxins.


2017 ◽  
Author(s):  
Debra A Brock ◽  
Alicia Canas ◽  
Kai Jones ◽  
David C Queller ◽  
Joan E Strassmann

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.


PLoS ONE ◽  
2012 ◽  
Vol 7 (9) ◽  
pp. e46150 ◽  
Author(s):  
Clea Scala ◽  
Xiangjun Tian ◽  
Natasha J. Mehdiabadi ◽  
Margaret H. Smith ◽  
Gerda Saxer ◽  
...  

BioEssays ◽  
2021 ◽  
pp. 2000156
Author(s):  
Sabateeshan Mathavarajah ◽  
Carter VanIderstine ◽  
Graham Dellaire ◽  
Robert J. Huber

2021 ◽  
Author(s):  
Omar Lenzi ◽  
Arpat Ozgul ◽  
Roberto Salguero-Gomez ◽  
Maria Paniw

Temporal variation in vital rates (e.g., survival, reproduction) can decrease the long-term mean performance of a population. Species are therefore expected to evolve demographic strategies that counteract the negative effects of vital rate variation on the population growth rate. One key strategy, demographic buffering, is reflected in a low temporal variation in vital rates critical to population dynamics. However, comparative studies in plants have found little evidence for demographic buffering, and little is known about the prevalence of buffering in animal populations. Here, we used vital rate estimates from 31 natural populations of 29 animal species to assess the prevalence of demographic buffering. We modeled the degree of demographic buffering using a standard measure of correlation between the standard deviation of vital rates and the sensitivity of the population growth rate to changes in such vital rates across populations. We also accounted for the effects of life-history traits, i.e., age at first reproduction and spread of reproduction across the life cycle, on these correlation measures. We found no strong or consistent evidence of demographic buffering across the study populations. Instead, key vital rates could vary substantially depending on the specific environmental context populations experience. We suggest that it is time to look beyond concepts of demographic buffering when studying natural populations towards a stronger focus on the environmental context-dependence of vital-rate variation.


Microbiology ◽  
2021 ◽  
Author(s):  
Catherine J. Pears ◽  
Julian D. Gross

The social amoeba Dictyostelium discoideum is a versatile organism that is unusual in alternating between single-celled and multi-celled forms. It possesses highly-developed systems for cell motility and chemotaxis, phagocytosis, and developmental pattern formation. As a soil amoeba growing on microorganisms, it is exposed to many potential pathogens; it thus provides fruitful ways of investigating host-pathogen interactions and is emerging as an influential model for biomedical research.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Simon Yuan Wang ◽  
Elizabeth Ann Pollina ◽  
I-Hao Wang ◽  
Lindsay Kristina Pino ◽  
Henry L. Bushnell ◽  
...  

Abstract Background The evolution of multicellularity is a critical event that remains incompletely understood. We use the social amoeba, Dictyostelium discoideum, one of the rare organisms that readily transits back and forth between both unicellular and multicellular stages, to examine the role of epigenetics in regulating multicellularity. Results While transitioning to multicellular states, patterns of H3K4 methylation and H3K27 acetylation significantly change. By combining transcriptomics, epigenomics, chromatin accessibility, and orthologous gene analyses with other unicellular and multicellular organisms, we identify 52 conserved genes, which are specifically accessible and expressed during multicellular states. We validated that four of these genes, including the H3K27 deacetylase hdaD, are necessary and that an SMC-like gene, smcl1, is sufficient for multicellularity in Dictyostelium. Conclusions These results highlight the importance of epigenetics in reorganizing chromatin architecture to facilitate multicellularity in Dictyostelium discoideum and raise exciting possibilities about the role of epigenetics in the evolution of multicellularity more broadly.


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