Search bioRxiv⌕ Search

Biology subjects

Brock, D. A.

Publications and source records attributed to Brock, D. A..

6 recordsLinked to original sources

Reduced social function in experimentally evolved Dictyostelium discoideum implies selection for social conflict in nature

Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimeric aggregates containing multiple unrelated lineages, cheaters can gain an advantage by undercontributing, but the extent to which wild D. discoideum has adapted to cheat is not fully clear. In this study, we experimentally evolved D. discoideum in an environment where there were no selective pressures to cheat or resist cheating in chimeras. D. discoideum lines grown in this environment evolved reduced competitiveness within chimeric aggregates and reduced ability to migrate during the slug stage. By contrast, we did not observe a reduction in cell number, a trait for which selection was not relaxed. The observed loss of traits that our laboratory conditions had made irrelevant suggests that these traits were adaptations driven and maintained by selective pressures D. discoideum faces in its natural environment. Our results suggest that D. discoideum faces social conflict in nature, and illustrate a general approach that could be applied to searching for social or non-social adaptations in other microbes. SIGNIFICANCE STATEMENTMicrobes interact in diverse and important ways, but the difficulty of directly observing microbes in nature can make it challenging to understand the adaptive significance of these interactions. In this study, we present an experimental evolution approach to infer the selective pressures behind an apparently social trait in the microbe Dictyostelium discoideum. We take advantage of the observation that organisms use it or lose it - when selective pressures are relaxed, adaptations that evolved in response to those pressures tend to be lost. Our work helps resolve debate over the importance of cheating in D. discoideum, and demonstrates a general approach that could be applied to the study of other microbial traits that are difficult to observe in nature.

evolutionary biology↗

Costs of being a diet generalist in the super-generalist protist predator Dictyostelium discoideum

Consumers lie on a continuum between diet specialization on few resources to being generalist feeders on many resources. Generalism has the clear advantage of having more resources to exploit, but the costs that limit generalism are less clear. We explore two understudied costs of generalism in a super-generalist amoeba predator, Dictyostelium discoideum, feeding on naturally co-occurring bacterial prey. Both involve costs of combining different prey. First, amoebas exhibit a reduction in growth rate when they switch from one species of prey bacteria to another, something we call resource-switching costs. These switching costs typically disappear within a day, indicating adjustment to new prey bacteria. Second, amoebas usually divide more slowly on mixtures of bacteria compared to on single bacteria, something we call resource-mixing costs. Both results support that idea that, although amoebas can consume a huge variety of prey, they must use partially different methods and thus must pay costs to handle multiple prey, either sequentially or simultaneously. Significance StatementPerhaps the most fundamental conflict in nature occurs when one organism consumes another. Diet generalists benefit from the advantage of eating many prey but then must deal with many prey defences. We explore costs associated with a broad diet in a protist microbial predator, Dictyostelium discoideum. These predators of bacteria show a delay in growth when switched from one bacteria to another, supporting the hypothesis that they must deploy different strategies. They also experience costs when grown on many bacteria at once, suggesting that the alternative strategies for consuming different prey are partly incompatible with each other. Our findings shed light on the nature of diet generalism and highlight the complexity of predation in the microbial world.

ecology↗

Symbiotic bacteria, immune-like sentinel cells, and the response to pathogens in a social amoeba

Some endosymbionts living within a host must modulate their hosts immune systems in order to infect and persist. We studied the effect of a bacterial endosymbiont on a facultatively multicellular social amoeba host. Aggregates of the amoeba Dictyostelium discoideum contain a subpopulation of sentinel cells that function akin to the immune systems of more conventional multicellular organisms. Sentinel cells sequester and discard toxins from D. discoideum aggregates and may play a central role in defense against pathogens. We measured the number and functionality of sentinel cells in aggregates of D. discoideum infected by bacterial endosymbionts in the genus Paraburkholderia. Infected D. discoideum produced fewer and less functional sentinel cells, suggesting that Paraburkholderia may interfere with its hosts immune system. Despite impaired sentinel cells, however, infected D. discoideum were less sensitive to ethidium bromide toxicity, suggesting that Paraburkholderia may also have a protective effect on its host. By contrast, D. discoideum infected by Paraburkholderia did not show differences in their sensitivity to two non-symbiotic pathogens. Our results expand previous work on yet another aspect of the complicated relationship between D. discoideum and Paraburkholderia, which has considerable potential as a model for the study of symbiosis.

ecology↗

Loss of altruism in the social amoeba Dictyostelium discoideum is associated with the G protein-coupled receptor, grlG

Aggregative multicellularity relies on cooperation among individual cells to form a multicellular body. In Dictyostelium discoideum this cooperation is maintained by high relatedness. Previous work showed that experimental evolution under low-relatedness resulted in an increase of cheaters (cells that contribute proportionally more to spores than to the sterile stalk) and that many clones completely lost cooperation and the ability to form fruiting bodies. Here, we investigate the genomic changes underlying the evolution of the cheating phenotype using whole-genome sequencing and variant analysis of these previously evolved D. discoideum lines. We identified 38 single nucleotide polymorphisms in 29 genes, none of which have been previously implicated in cheating. Each gene has one variant except for the G protein-coupled receptor grlG, which has at least one variant in over half of the lines. Upon identifying the parallel evolution of grlG, we screened additional clones to investigate the correlation between variants in the gene and the loss of cooperation (identified by the inability to form a fruiting body). We found that variants in the 5 half of grlG that impact the signal peptide or extracellular binding domain are significantly associated with the loss of cooperation (non-fruiting); the association was not significant in the 3 half of the gene. This suggests that the loss of grlG was adaptive under low-relatedness and that the 5 half of the gene in particular is important for cooperation and multicellular development. This confirms the importance of high relatedness in the evolution of altruism in the social amoeba D. discoideum.

evolutionary biology↗

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↗