Biology subjects

Strassmann, J. E.

Publications and source records attributed to Strassmann, J. E..

18 recordsLinked to original sources

bioRxiv2026

A history of symbiosis impacts the host evolutionary trajectory in experimentally evolved amoebas

Biological diversity driven by endosymbiosis arises from the intertwined evolution of microbes and their hosts. Each partner affects the fitness and therefore the evolution of the other. Here, we tested a further question: does the history of symbiosis affect evolution even after the partnership is dissolved? We analyzed phenotypic data from experimentally evolved strains of Dictyostelium discoideum hosts, each of which had had its symbiont removed, to study how their traits evolved. We found that host trait evolution was affected by the prior history of infection, specifically by which of three Paraburkolderia bacterial symbionts had been removed. Thus, symbionts affect not only current evolution but also generate path dependence that affects the subsequent evolutionary trajectories even after the symbionts are lost. Impact statementThe evolution of partner dependence in host-microbial symbioses has fundamentally shaped biological diversity and ecosystem function. To examine variation in symbiont dependence in the social amoeba, we compared how different strains of Dictyostelium discoideum respond evolutionarily after the loss of their bacterial symbionts. We analyzed phenotypic data from experimentally evolved strains and found that the absence of different symbiont species leads to distinct changes in the subsequent evolution of key traits like cell proliferation, slug migration, and spore production. This research expands our current understanding of microbial symbiosis by revealing that symbiont species may impact the evolution of their hosts even after the symbiont is gone. Data summaryWe used phenotypic traits data from our previous experimental-evolution dataset from the open-access repository Dryad (https://doi.org/10.5061/dryad.kkwh70s97). Scripts for the statistical analyses are available in a GitHub repository (https://github.com/jahanisrat/SymbiontLoss). The accompanying R project includes code to reproduce the graphs in the results section.

evolutionary biology↗

bioRxiv2025

Predation limits the abundance of {triangleup}gacA cheaters in Pseudomonas protegens populations

In bacteria, defense against predators and competitors often requires cooperation within large clonal bacterial populations. Mutations that inactivate biosynthesis of costly molecules involved in cooperative defense can increase the growth rate of the mutants, while mutant cells continue to benefit from the efforts of wild type cells. The GacA-GacS signaling pathway regulates biosynthesis and secretion of toxic secondary metabolites and proteins that play crucial roles in bacterial defense in Pseudomonas species, including resistance to the protozoan predator Dictyostelium discoideum. A P. protegens {Delta}gacA mutant is vulnerable to predation but can benefit from protection provided by wild type cells in mixed populations. Wild type P. protegens sporadically infects D. discoideum fruiting bodies which may aid in bacterial dispersal to new environments. We found that the {Delta}gacA mutant does not infect fruiting bodies and that the wild type does not infect when at low abundance in the population. The P. protegens {Delta}gacA mutant is a cheater whose fitness under predation depends on its relative abundance. Protozoan predators can limit the abundance of {Delta}gacA mutants in Pseudomonas populations, preventing selective sweeps that could lead to the loss of the important but costly Gac regulon.

microbiology↗

bioRxiv2024

Novel symbionts reveal amoebae as significant hosts for environmental chlamydiae

Chlamydiae represent a diverse group of obligate intracellular bacteria with elusive hosts in environmental settings. This study used one of the largest collections of wild amoebae (Dictyostelium discoideum and D. giganteum, 106 clones) collected over the past two decades to screen for novel environmental chlamydiae. We found that novel environmental chlamydiae are prevalent in two wild Dictyostelium species and assembled 42 novel chlamydiae metagenome-assembled genomes (MAGs). The MAGs represent three chlamydiae species previously only reported using 16S sequencing. Their genomes are divergent enough from other species to warrant placing them in two new genera (tentatively called Ca. Dictychlamydia sp. LF1, Ca. Dictychlamydia sp. LF2, and Ca. Feichlamydia sp. LF3). In addition, these chlamydiae species show strong host specificity with two Dictyostelium amoeba hosts, except one amoeba sample. Ca. Dictychlamydia sp. LF1 and Ca. Feichlamydia sp. LF3 was exclusively observed in D. discoideum, while Ca. Dictychlamydia sp. LF2 was found only in D. giganteum. Phylogenetic and comparative genomic analyses suggest that all three chlamydiae are close to arthropod-associated chlamydiae and likely have some intermediate characteristics between previously reported amoeba-associated and vertebrate-associated chlamydiae. This study significantly broadens our understanding of the chlamydial host range and underscores the role of amoebae as vital hosts for environmental chlamydiae.

microbiology↗

bioRxiv2024

Prey attraction in a generalist microbial predator, Dictyostelium discoideum

How do generalists adjust to variation in prey abundance and profitability and seek out their preferred prey? We investigated this question in the soil protist Dictyostelium discoideum, a generalist predator of many species of bacteria. Despite their generalist diet, amoebas proliferate more quickly on some bacteria than on others. We tested amoeba chemoattraction towards 23 bacterial species and found that they are generally more attracted to the more profitable prey bacteria. Naive amoebas were also preferentially more attracted to an edible mutant rather than the inedible wild type of a soil Pseudomonas isolate. These results suggest that D. discoideum amoebas have an innate prey preference that is adaptive. We also tested how experience with different prey bacteria affects chemoattraction in amoebas. Given the huge number of bacterial species in soil, learning from experience should be advantageous. However, we found no evidence that experience with prey bacteria affects preference. Our results suggest that generalist amoebas are innately attracted to the more profitable prey bacteria and this innate attraction cannot be overridden by recent experience.

evolutionary biology↗

bioRxiv2024

The genetic basis of predation resistance in Pseudomonas species associated with the bactivorous soil amoeba Dictyostelium discoideum.

Predation is likely to influence the function of bacterial communities and the evolution of bacterial pathogens, because characteristics that permit escape from predators often overlap with traits used for biocontrol of plant pathogens, virulence, or even bioremediation. Soil bacteria are preyed upon by a variety of microorganisms, including the amoeba Dictyostelium discoideum, which has led some strains to evolve resistance. We identified genes required for three Pseudomonas species associated with D. discoideum to evade predation by screening more than 6,000 transposon mutants for loss of resistance. One species required a variety of genes including toxins and secondary metabolism genes, but the other two appear to have functionally redundant mechanisms of resistance, since disruption of genes with pleiotropic effects was required to render them susceptible. We determined that GacA, which positively regulates secondary metabolism, is required for resistance in all three species. Predation resistance also appears to be a social trait based on enrichment of cooperative genes in one species and rescue of mutants by wild type in another. Many genes required for resistance are conserved among both resistant and susceptible species, but several are found in few genomes and some of these have homologs in distantly related species. Gain and loss of resistance appears to be a dynamic process in which regulatory and structural genes are well conserved across species, the specific toxins they regulate may be lost in the absence of predators, and new toxins may be acquired through horizontal gene transfer.

microbiology↗

bioRxiv2024

Non-selected incompatibilities and their effects on aggregative multicellularity in the social amoeba Dictyostelium discoideum

Multicellular organisms that form by aggregation of cells arguably do not achieve high levels of complexity. Conflict among the cells is a widely accepted explanation for this, but an alternative hypothesis is that mixing cells of different genotypes leads to failures of coordination, which we call the coordination hypothesis. We empirically tested the coordination hypothesis in the social amoeba Dictyostelium discoideum. We mixed D. discoideum clones that had evolved in isolation for generations and accumulated mutations that have not been tested against each other by selection. To quantify the effect of incompatibilities, we measured performance in terms of the developmental traits of slug migration and spore production. Importantly, kin recognition incompatibilities were avoided by mixing lines evolved from the same ancestor under conditions that would not select for the evolution of de novo recognition. Our results show no evidence of incompatibilities in coordinated movement of slugs towards light in the social amoeba. Spore production was higher than expected in mixtures, in apparent contradiction to the coordination hypothesis. However, we found support for coordination incompatibilities in an interaction between migration and spore production: in mixtures, fewer cells succeeded at migrating and becoming spores.

evolutionary biology↗

bioRxiv2023

Predation-resistant Pseudomonas bacteria engage in symbiont-like behavior with the social amoeba Dictyostelium discoideum

The soil amoeba Dictyostelium discoideum acts as both a predator and potential host for diverse bacteria. We tested fifteen Pseudomonas strains that were isolated from transiently infected wild D. discoideum for ability to escape predation and infect D. discoideum fruiting bodies. Three predation-resistant strains frequently caused extracellular infections of fruiting bodies but were not found within spores. Furthermore, infection by one of these species induces secondary infections and suppresses predation of otherwise edible bacteria. Another strain can persist inside of amoebae after being phagocytosed but is rarely ingested. We sequenced isolate genomes and discovered that predation-resistant isolates are not monophyletic. Many Pseudomonas isolates encode secretion systems and toxins known to improve resistance to phagocytosis in other species, as well as diverse secondary metabolite biosynthetic gene clusters that may contribute to predation resistance. However, the distribution of these genes alone cannot explain why some strains are edible and others are not. Each lineage may employ a unique mechanism for resistance.

microbiology↗

bioRxiv2023

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↗

bioRxiv2023

Unpredictable soil conditions affect the prevalence of a microbial symbiosis

The evolution of symbiotic interactions may be affected by unpredictable conditions. However, a link between prevalence of symbiosis and these conditions has not been widely demonstrated. We test for these associations using Dictyostelium discoideum social amoebae and their bacterial symbionts. D. discoideum are host to endosymbiotic bacteria from three taxa: Paraburkholderia, Amoebophilus and Chlamydiae. Three species of facultative Paraburkholderia symbionts are the best studied and give hosts the ability to carry food bacteria through the dispersal stage to new environments. Amoebophilus and Chlamydiae are obligate endosymbionts with no measurable impact on host fitness. We test whether the frequency of both single infections and coinfections of these symbionts are associated with the unpredictability of their soil environments by using symbiont presence-absence data from soil isolates from 21 locations across the eastern United States. We find that that Amoebophilus and Chlamydiae obligate endosymbionts and coinfections are not associated with any of our mean measures, but that unpredictable precipitation can promote or hinder symbiosis depending on the species of Paraburkholderia symbiont.

evolutionary biology↗

bioRxiv2023

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↗

bioRxiv2023

Limits to the spread of an obligate social cheater in the social amoeba Dictyostelium discoideum

Cooperation is widespread across life, but its existence can be threatened by exploitation. Social cheaters can be obligate, incapable of contributing to a necessary function, so that spread of the cheater leads to loss of the function. In the social amoeba Dictyostelium discoideum, obligate social cheaters cannot become dead stalk cells that lift spores up for dispersal, but instead depend on forming chimeras with fully functional altruistic individuals for forming a stalk. Obligate cheaters in D. discoideum are known to pay the cost of being unable to form fruiting bodies on their own. In this study we discovered that there are two additional costs that can apply to obligate cheaters. Even when there are wild-type cells to parasitize, the chimeric fruiting bodies that result have shorter stalks that are disadvantaged in spore dispersal. Furthermore, we found that obligate cheaters were overrepresented among spore cells in chimeras only when they were at low frequencies. Failure to develop into viable fruiting bodies on their own, negative frequency-dependent cheating, and shorter fruiting bodies represent three limits on obligate social cheating so it is not surprising that obligate cheaters have not been found in nature.

evolutionary biology↗

bioRxiv2022

Third-party effects in the Dictyostelium-Paraburkholderia symbiosis: food bacteria that are eaten, carried, or left behind

AbstractSymbiotic interactions may change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with prey bacteria are central to the symbiosis between Dictyostelium discoideum social amoeba hosts and Paraburkholderia facultative bacterial symbionts. Symbiosis with inedible Paraburkholderia allows host D. discoideum to carry prey bacteria through the dispersal stage where host amoebae aggregate and develop into fruiting bodies that disperse spores. Carrying prey bacteria benefits hosts when prey bacteria are scarce but harms hosts when prey bacteria are plentiful. Symbiont-carrying hosts leave some bacteria behind; this could explain the harm to hosts if left-behind bacteria include uneaten prey bacteria. Thus, understanding both benefits and costs in this symbiosis requires measuring how many prey bacteria are eaten, carried, and left behind by infected hosts. We found that Paraburkholderia infection makes hosts leave behind both symbionts and prey bacteria. However, the number of prey bacteria left uneaten was small and did not explain why infected hosts produced fewer spores than uninfected hosts. Turning to the bacteria that are carried, we found that hosts carry more prey bacteria after developing in prey- poor environments than in prey-rich ones. This suggests that carriage is actively modified to ensure hosts have prey in the harshest conditions. Our results show that multifaceted interactions with third parties shape the evolution of symbioses in complex ways.

evolutionary biology↗

bioRxiv2022

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↗

bioRxiv2022

Comparative genomics support reduced-genome Paraburkholderia symbionts of Dictyostelium discoideum amoebas are ancestrally adapted professional symbionts

The social amoeba Dictyostelium discoideum is a predatory soil protist frequently used for studying host-pathogen interactions. A subset of D. discoideum strains isolated from soil persistently carry symbiotic Paraburkholderia, recently formally described as P. agricolaris, P. bonniea, and P. hayleyella. The three facultative symbiont species of D. discoideum present a unique opportunity to study a naturally occurring symbiosis in a laboratory model protist. In addition, there is a large difference in genome size between P. agricolaris (8.7 million base pairs) vs. P. hayleyella and P. bonniea (4.1 Mbp) and in GC content (62% vs. 59%). We took a comparative genomics approach and compared the three genomes of D. discoideum-symbionts to 12 additional Paraburkholderia genomes to test for genome evolution patterns that frequently accompany host adaptation. Overall, P. agricolaris is difficult to distinguish from other Paraburkholderia based on its genome size and content, but the two reduced genomes of P. bonniea and P. hayleyella display characteristics that support evolution in a host environment. In addition, all three D. discoideum-symbiont genomes have increased secretion system and motility genes that may mediate interactions with their host. Specifically, adjacent BurBor-like type 3 and T6SS-5-like type 6 secretion system operons shared among all three D. discoideum-symbiont genomes may be important for host interaction. Ultimately, our combined evidence supports that the reduced-genome D. discoideum-symbionts have evolved to be professional symbionts ancestrally adapted to their protist hosts.

evolutionary biology↗

bioRxiv2021

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

Symbiotic interactions change with environmental context. Measuring these context-dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context-dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, 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 that symbiosis often provides a long-term fitness advantage for hosts after rounds of growth and dispersal in variable food-contexts, especially when conditions are harsh with little food. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and that both sides can frequently benefit. Impact StatementMany organisms form symbiotic relationships with other species. These symbioses often exhibit context-dependence, where the sign or magnitude of one partners effect on the other will change in different environments. Context-dependent effects make it difficult to assign interactions to categories like mutualisms or antagonisms because they involve both benefits and costs depending on the environment. However, in some cases, accounting for context-dependence can clarify an interaction so that it more easily fits a mutualism or antagonism. We investigated context-dependence using the symbiosis between Dictyostelium discoideum and two symbiotic Paraburkholderia species. In this symbiosis, Paraburkholderia bacteria allow hosts to carry food bacteria to food-poor contexts, where hosts rarely survive without food, but reduce host fitness in the more hospitable food-rich contexts. The effect of food context on Paraburkholderia symbionts is unknown. We show that Paraburkholderia symbionts are also affected by this context, through facing reduced competition after being dispersed by hosts to food-poor contexts. We also identify a new way that symbionts affect hosts, where symbiont density reduces host fitness, but less so in food-poor contexts. Finally, we use simulations to show that infected hosts benefit in the long-term across variable food contexts, especially in the harshest environments with little food. These results show that context-dependence in symbiosis can have many consequences for hosts and symbionts, though in general for D. discoideum and Paraburkholderia, both are likely to benefit.

ecology↗

bioRxiv2020

Novel Chlamydiae and Amoebophilus endosymbionts are prevalent in wild isolates of the model social amoebae Dictyostelium discoideum

Amoebae interact with bacteria in diverse and multifaceted ways. Amoeba predation can serve as a selective pressure for the development of bacterial virulence traits. Bacteria may also adapt to life inside amoebae, resulting in symbiotic relationships (pathogenic or mutualistic). Indeed, particular lineages of obligate bacterial endosymbionts have been found in different amoebae. Here, we screened an extensive collection of Dictyostelium discoideum wild isolates for the presence of such bacterial symbionts using PCR primers that identify these endosymbionts. This is the first report of obligate symbionts in this highly-studied amoeba species. They are surprisingly common, identified in 42% of screened isolates (N=730). Members of the Chlamydiae phylum are particularly prevalent, occurring in 27% of the host strains. They are novel and phylogenetically distinct. We also found Amoebophilus symbionts in 8% of screened isolates (N=730). Antibiotic-cured amoebae behave similarly to their endosymbiont-infected counterparts, suggesting that endosymbionts do not significantly impact host fitness, at least in the laboratory. We found several natural isolates were co-infected with multiple endosymbionts, with no obvious fitness effects of co-infection under laboratory conditions. The high prevalence and novelty of amoeba endosymbiont clades in the model organism D. discoideum opens the door to future research on the significance and mechanisms of amoeba-symbiont interactions.

microbiology↗

bioRxiv2018

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↗

bioRxiv2018

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↗