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We present complete genome sequences from 30 bacterial species that can be used to construct defined synthetic communities that stably form in the laboratory under controlled conditions.
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Closely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with a synthetic 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and one bacterial prey species from the community. Altering the coevolutionary history of the focal prey species had little effect on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both the coevolved focal predator and prey. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple bacterial species. Our findings show that the disruption of localized coevolution between species pairs can reverberate through community-wide transcriptional networks even while community composition remains largely unchanged. We propose that these altered expression patterns may signal forthcoming evolutionary and ecological change.
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Ecossistema , Comportamento Predatório , Animais , Evolução Biológica , Bactérias/genética , Expressão Gênica , Cadeia AlimentarRESUMO
The impact of fitness landscape features on evolutionary outcomes has attracted considerable interest in recent decades. However, evolution often occurs under time-dependent selection in so-called fitness seascapes where the landscape is under flux. Fitness seascapes are an inherent feature of natural environments, where the landscape changes owing both to the intrinsic fitness consequences of previous adaptations and extrinsic changes in selected traits caused by new environments. The complexity of such seascapes may curb the predictability of evolution. However, empirical efforts to test this question using a comprehensive set of regimes are lacking. Here, we employed an in vitro microbial model system to investigate differences in evolutionary outcomes between time-invariant and time-dependent environments, including all possible temporal permutations, with three subinhibitory antimicrobials and a viral parasite (phage) as selective agents. Expectedly, time-invariant environments caused stronger directional selection for resistances compared to time-dependent environments. Intriguingly, however, multidrug resistance outcomes in both cases were largely driven by two strong selective agents (rifampicin and phage) out of four agents in total. These agents either caused cross-resistance or obscured the phenotypic effect of other resistance mutations, modulating the evolutionary outcome overall in time-invariant environments and as a function of exposure epoch in time-dependent environments. This suggests that identifying strong selective agents and their pleiotropic effects is critical for predicting evolution in fitness seascapes, with ramifications for evolutionarily informed strategies to mitigate drug resistance evolution.
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Prochlorococcus and Synechococcus are the most abundant photosynthesizing organisms in the oceans. Gene content variation among picocyanobacterial populations in separate ocean basins often mirrors the selective pressures imposed by the region's distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in Synechococcus and low-light adapted Prochlorococcus populations from deep chlorophyll maximum layers of iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher new iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower new iron flux). Picocyanobacterial siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, especially at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of marine picocyanobacteria.
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Prochlorococcus , Synechococcus , Clorofila , Ferro , Metagenoma , Oceanos e Mares , Oceano Pacífico , Filogenia , Prochlorococcus/genética , Água do Mar/microbiologia , Sideróforos , Synechococcus/genéticaRESUMO
Mutation supply can influence evolutionary and thereby ecological dynamics in important ways which have received little attention. Mutation supply influences features of population genetics, such as the pool of adaptive mutations, evolutionary pathways and importance of processes, such as clonal interference. The resultant trait evolutionary dynamics, in turn, can alter population size and species interactions. However, controlled experiments testing for the importance of mutation supply on rapid adaptation and thereby population and community dynamics have primarily been restricted to the first of these aspects. To close this knowledge gap, we performed a serial passage experiment with wild-type Pseudomonas fluorescens and a mutant with reduced mutation rate. Bacteria were grown at two resource levels in combination with the presence of a ciliate predator. A higher mutation supply enabled faster adaptation to the low-resource environment and anti-predatory defence. This was associated with higher population size at the ecological level and better access to high-recurrence mutational targets at the genomic level with higher mutation supply. In contrast, mutation rate did not affect growth under high-resource level. Our results demonstrate that intrinsic mutation rate influences population dynamics and trait evolution particularly when population size is constrained by extrinsic conditions.
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Evolução Biológica , Microbiota , Pseudomonas fluorescens , Mutação , Dinâmica Populacional , Pseudomonas fluorescens/genéticaRESUMO
A popular idea in ecology is that trait variation among individuals from the same species may promote the coexistence of competing species. However, theoretical and empirical tests of this idea have yielded inconsistent findings. We manipulated intraspecific trait diversity in a ciliate competing with a nematode for bacterial prey in experimental microcosms. We found that intraspecific trait variation inverted the original competitive hierarchy to favour the consumer with variable traits, ultimately resulting in competitive exclusion. This competitive outcome was driven by foraging traits (size, speed and directionality) that increased the ciliate's fitness ratio and niche overlap with the nematode. The interplay between consumer trait variation and competition resulted in non-additive cascading effects-mediated through prey defence traits-on prey community assembly. Our results suggest that predicting consumer competitive population dynamics and the assembly of prey communities will require understanding the complexities of trait variation within consumer species.
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Variação Biológica da População , Ecologia , Animais , Fenótipo , Dinâmica Populacional , Comportamento PredatórioRESUMO
The rapid spread of antibiotic resistance challenges modern medicine. So far, mechanistic and quantitative knowledge concerning the spread of resistance genes mainly relies on laboratory experiments with simplified setups, e.g. two strain communities. Thus, the transferability of the obtained process rates might be limited. To investigate the role of a diverse community concerning the dissemination of the multidrug resistance plasmid RP4, an Escherichia coli harboring RP4 invaded a microbial community consisting of 21 species. Changes in the community composition as well as plasmid uptake by community members were monitored for 22 days. Special focus was laid on the question of whether the observed changes were dependent on the actual invading donor isolate and the ambient antibiotic concentration. In our microcosm experiment, the community composition was primarily influenced by the given environmental variables and only secondarily by the particular invader E. coli. The establishment of resistance within the community, however, was directly dependent on the donor identity. The extent to which ambient conditions influence the spread of RP4 depended on the E. coli donor strain. These results emphasize that even within one species there are great differences in the ability to conquer an ecological niche and to spread antibiotic resistance.
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Escherichia coli , Transferência Genética Horizontal , Antibacterianos/farmacologia , Bactérias/genética , Conjugação Genética , Resistência Microbiana a Medicamentos , Escherichia coli/genética , Plasmídeos/genéticaRESUMO
In an era of pervasive anthropogenic ecological disturbances, there is a pressing need to understand the factors that constitute community response and resilience. A detailed understanding of disturbance response needs to go beyond associations and incorporate features of disturbances, species traits, rapid evolution and dispersal. Multispecies microbial communities that experience antibiotic perturbation represent a key system with important medical dimensions. However, previous microbiome studies on this theme have relied on high-throughput sequencing data from uncultured species without the ability to explicitly account for the role of species traits and immigration. Here, we serially passage a 34-species defined bacterial community through different levels of pulse antibiotic disturbance, manipulating the presence or absence of species immigration. To understand the ecological community response measured using amplicon sequencing, we combine initial trait data measured for each species separately and metagenome sequencing data revealing adaptive mutations during the experiment. We found that the ecological community response was highly repeatable within the experimental treatments, which could be attributed in part to key species traits (antibiotic susceptibility and growth rate). Increasing antibiotic levels were also coupled with an increasing probability of species extinction, making species immigration critical for community resilience. Moreover, we detected signals of antibiotic-resistance evolution occurring within species at the same time scale, leaving evolutionary changes in communities despite recovery at the species compositional level. Together, these observations reveal a disturbance response that presents as classic species sorting, but is nevertheless accompanied by rapid within-species evolution.
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Antibacterianos , Microbiota , Bactérias/genética , Metagenoma , Características de ResidênciaRESUMO
Predator-prey interactions heavily influence the dynamics of many ecosystems. An increasing body of evidence suggests that rapid evolution and coevolution can alter these interactions, with important ecological implications, by acting on traits determining fitness, including reproduction, anti-predatory defence and foraging efficiency. However, most studies to date have focused only on evolution in the prey species, and the predator traits in (co)evolving systems remain poorly understood. Here, we investigated changes in predator traits after approximately 600 generations in a predator-prey (ciliate-bacteria) evolutionary experiment. Predators independently evolved on seven different prey species, allowing generalization of the predator's evolutionary response. We used highly resolved automated image analysis to quantify changes in predator life history, morphology and behaviour. Consistent with previous studies, we found that prey evolution impaired growth of the predator, although the effect depended on the prey species. By contrast, predator evolution did not cause a clear increase in predator growth when feeding on ancestral prey. However, predator evolution affected morphology and behaviour, increasing size, speed and directionality of movement, which have all been linked to higher prey search efficiency. These results show that in (co)evolving systems, predator adaptation can occur in traits relevant to foraging efficiency without translating into an increased ability of the predator to grow on the ancestral prey type.
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Fenômenos Fisiológicos Bacterianos , Microbiota , Animais , Bactérias , Evolução Biológica , Cadeia Alimentar , Características de História de Vida , Comportamento PredatórioRESUMO
The horizontal transfer of plasmids is a key mechanism behind the spread of antibiotic resistance in bacteria. So far, transfer rate constants were measured for a variety of plasmids, donors and recipients. The employed strains typically had a long history in laboratories. Existing data are, therefore, not necessarily representative for real-world environments. Moreover, information on the inter-strain variability of plasmid transfer rates is scarce. Using a high-throughput approach, we studied the uptake of RP4 by various Escherichia coli recipients using Serratia marcescens as the donor. The recipient strains were isolated from human-borne sewage and river sediments. The rate constants of plasmid transfer generally followed a log-normal distribution with considerable variance. The rate constants for good and poor recipients (95 and 5% quantile) differed by more than three orders of magnitude. Specifically, the inter-strain variability of the rate constant was large in comparison to alterations induced by low-level antibiotic exposure. We did not find evidence for diverging efficiencies of plasmid uptake between E. coli recipients of different origin. On average, strains isolated from river bottom sediments were equally efficient in the acquisition of RP4 as isolates extracted from sewage. We conclude that E. coli strains persisting in the aquatic environment and those of direct human origin share a similar intrinsic potential for the conjugative uptake of certain plasmids. In view of the large inter-strain variability, we propose to work towards probabilistic modeling of the environmental spread of antibiotic resistance.
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Conjugação Genética/efeitos dos fármacos , Transferência Genética Horizontal/efeitos dos fármacos , Plasmídeos/efeitos dos fármacos , Antibacterianos/farmacologia , Resistência Microbiana a Medicamentos/efeitos dos fármacos , Resistência Microbiana a Medicamentos/genética , Escherichia coli/genética , Escherichia coli/metabolismo , Transferência Genética Horizontal/genética , Plasmídeos/genética , Plasmídeos/metabolismo , Rios , Serratia marcescens/genética , EsgotosRESUMO
Predator-prey relationships belong to the most important and well-studied ecological interactions in nature. Understanding the underlying mechanisms is important to predict community dynamics and to estimate coexistence probability. Historically, evolution has been considered to be too slow to affect such ecological interactions. However, evolution can occur within ecological time scales, potentially affecting predator-prey communities. In an antagonistic pair-wise relationship the prey might evolve to minimize the effect caused by the predator (e.g. mortality), while the predator might evolve to maximize the effect (e.g. food intake). Evolution of one of the species or even co-evolution of both species in predator-prey relationships is often difficult to estimate from population dynamics without measuring of trait changes in predator and/or prey population. Particularly in microbial systems, where microorganisms evolve quickly, determining whether co-evolution occurs in predator-prey systems is challenging. We simulate observational data using quantitative trait evolution models and show that the interaction between bacteria and ciliates can be best explained as a co-evolutionary process, where both the prey and predator evolve. Evolution by prey alone explains the data less well, whereas the models with predator evolution alone or no evolution are both failing. We conclude that that ecology and evolution both interact in shaping community dynamics in microcosms. Ignoring the contribution of evolution might lead to incorrect conclusions.
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Evolução Biológica , Interações Microbianas , Animais , Bactérias , Cadeia Alimentar , Fenótipo , Dinâmica Populacional , Comportamento PredatórioRESUMO
Predation is one of the key ecological mechanisms allowing species coexistence and influencing biological diversity. However, ecological processes are subject to contemporary evolutionary change, and the degree to which predation affects diversity ultimately depends on the interplay between evolution and ecology. Furthermore, ecological interactions that influence species coexistence can be altered by reciprocal coevolution especially in the case of antagonistic interactions such as predation or parasitism. Here we used an experimental evolution approach to test for the role of initial trait variation in the prey population and coevolutionary history of the predator in the ecological dynamics of a two-species bacterial community predated by a ciliate. We found that initial trait variation both at the bacterial and ciliate level enhanced species coexistence, and that subsequent trait evolutionary trajectories depended on the initial genetic diversity present in the population. Our findings provide further support to the notion that the ecology-centric view of diversity maintenance must be reinvestigated in light of recent findings in the field of eco-evolutionary dynamics.
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Coevolução Biológica , Cadeia Alimentar , Características de História de Vida , Escherichia coli/fisiologia , Modelos Biológicos , Pseudomonas fluorescens/fisiologia , Tetrahymena thermophila/fisiologiaRESUMO
Horizontal gene transfer is an essential component of bacterial evolution. Quantitative information on transfer rates is particularly useful to better understand and possibly predict the spread of antimicrobial resistance. A variety of methods has been proposed to estimate the rates of plasmid-mediated gene transfer all of which require substantial labor input or financial resources. A cheap but reliable method with high-throughput capabilities is yet to be developed in order to better capture the variability of plasmid transfer rates, e.g. among strains or in response to environmental cues. We explored a new approach to the culture-based estimation of plasmid transfer rates in liquid media allowing for a large number of parallel experiments. It deviates from established approaches in the fact that it exploits data on the absence/presence of transconjugant cells in the wells of a well plate observed over time. Specifically, the binary observations are compared to the probability of transconjugant detection as predicted by a dynamic model. The bulk transfer rate is found as the best-fit value of a designated model parameter. The feasibility of the approach is demonstrated on mating experiments where the RP4 plasmid is transfered from Serratia marcescens to several Escherichia coli recipients. The method's uncertainty is explored via split sampling and virtual experiments.
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Escherichia coli/genética , Transferência Genética Horizontal , Modelos Estatísticos , Plasmídeos/metabolismo , Serratia marcescens/genética , Evolução Biológica , Conjugação Genética , Ensaios de Triagem em Larga Escala/estatística & dados numéricos , Plasmídeos/química , IncertezaRESUMO
Parasites, such as bacterial viruses (phages), can have large effects on host populations both at the ecological and evolutionary levels. In the case of cyanobacteria, phages can reduce primary production and infected hosts release intracellular nutrients influencing planktonic food web structure, community dynamics, and biogeochemical cycles. Cyanophages may be of great importance in aquatic food webs during large cyanobacterial blooms unless the host population becomes resistant to phage infection. The consequences on plankton community dynamics of the evolution of phage resistance in bloom forming cyanobacterial populations are still poorly studied. Here, we examined the effect of different frequencies of a phage-resistant genotype within a filamentous nitrogen-fixing Nodularia spumigena population on an experimental plankton community. Three Nodularia populations with different initial frequencies (0%, 5%, and 50%) of phage-resistant genotypes were inoculated in separate treatments with the phage 2AV2, the green alga Chlorella vulgaris, and the rotifer Brachionus plicatilis, which formed the experimental plankton community subjected to either nitrogen-limited or nitrogen-rich conditions. We found that the frequency of the phage-resistant Nodularia genotype determined experimental community dynamics. Cyanobacterial populations with a high frequency (50%) of the phage-resistant genotype dominated the cultures despite the presence of phages, retaining most of the intracellular nitrogen in the plankton community. In contrast, populations with low frequencies (0% and 5%) of the phage-resistant genotype were lysed and reduced to extinction by the phage, transferring the intracellular nitrogen held by Nodularia to Chlorella and rotifers, and allowing Chlorella to dominate the communities and rotifers to survive. This study shows that even though phages represent minuscule biomass, they can have key effects on community composition and eco-evolutionary feedbacks in plankton communities.
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Bacteriófagos , Chlorella vulgaris , Cianobactérias , Rotíferos , Animais , Cadeia AlimentarRESUMO
Recognizing when and how rapid evolution drives ecological change is fundamental for our understanding of almost all ecological and evolutionary processes such as community assembly, genetic diversification and the stability of communities and ecosystems. Generally, rapid evolutionary change is driven through selection on genetic variation and is affected by evolutionary constraints, such as tradeoffs and pleiotropic effects, all contributing to the overall rate of evolutionary change. Each of these processes can be influenced by the presence of multiple environmental stressors reducing a population's reproductive output. Potential consequences of multistressor selection for the occurrence and strength of the link from rapid evolution to ecological change are unclear. However, understanding these is necessary for predicting when rapid evolution might drive ecological change. Here we investigate how the presence of two stressors affects this link using experimental evolution with the bacterium Pseudomonas fluorescens and its predator Tetrahymena thermophila. We show that the combination of predation and sublethal antibiotic concentrations delays the evolution of anti-predator defence and antibiotic resistance compared with the presence of only one of the two stressors. Rapid defence evolution drives stabilization of the predator-prey dynamics but this link between evolution and ecology is weaker in the two-stressor environment, where defence evolution is slower, leading to less stable population dynamics. Tracking the molecular evolution of whole populations over time shows further that mutations in different genes are favoured under multistressor selection. Overall, we show that selection by multiple stressors can significantly alter eco-evolutionary dynamics and their predictability.
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Evolução Biológica , Farmacorresistência Bacteriana , Cadeia Alimentar , Pseudomonas fluorescens/genética , Seleção Genética , Tetrahymena thermophila/fisiologia , Animais , Antibacterianos/efeitos adversos , Testes de Sensibilidade Microbiana , Dinâmica Populacional , Pseudomonas fluorescens/efeitos dos fármacos , Pseudomonas fluorescens/fisiologiaRESUMO
Low concentrations of antibiotics have numerous effects on bacteria. However, it is unknown whether ecological factors such as trophic interactions and spatial structuring influence the effects of low concentrations of antibiotics on multispecies microbial communities. Here, we address this question by investigating the effects of low antibiotic concentration on community composition and horizontal transfer of an antibiotic resistance plasmid in a 62-strain bacterial community in response to manipulation of the spatial environment and presence of predation. The strong effects of antibiotic treatment on community composition depend on the presence of predation and spatial structuring that have strong community effects on their own. Overall, we find plasmid transfer to diverse recipient taxa. Plasmid transfer is likely to occur to abundant strains, occurs to a higher number of strains in the presence of antibiotic, and also occurs to low-abundance strains in the presence of spatial structures. These results fill knowledge gaps concerning the effects of low antibiotic concentrations in complex ecological settings.
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Mobile genetic elements such as conjugative plasmids are responsible for antibiotic resistance phenotypes in many bacterial pathogens. The ability to conjugate, the presence of antibiotics, and ecological interactions all have a notable role in the persistence of plasmids in bacterial populations. Here, we set out to investigate the contribution of these factors when the conjugation network was disturbed by a plasmid-dependent bacteriophage. Phage alone effectively caused the population to lose plasmids, thus rendering them susceptible to antibiotics. Leakiness of the antibiotic resistance mechanism allowing Black Queen evolution (i.e. a "race to the bottom") was a more significant factor than the antibiotic concentration (lethal vs sublethal) in determining plasmid prevalence. Interestingly, plasmid loss was also prevented by protozoan predation. These results show that outcomes of attempts to resensitize bacterial communities by disrupting the conjugation network are highly dependent on ecological factors and resistance mechanisms. IMPORTANCE Bacterial antibiotic resistance is often a part of mobile genetic elements that move from one bacterium to another. By interfering with the horizontal movement and the maintenance of these elements, it is possible to remove the resistance from the population. Here, we show that a so-called plasmid-dependent bacteriophage causes the initially resistant bacterial population to become susceptible to antibiotics. However, this effect is efficiently countered when the system also contains a predator that feeds on bacteria. Moreover, when the environment contains antibiotics, the survival of resistance is dependent on the resistance mechanism. When bacteria can help their contemporaries to degrade antibiotics, resistance is maintained by only a fraction of the community. On the other hand, when bacteria cannot help others, then all bacteria remain resistant. The concentration of the antibiotic played a less notable role than the antibiotic used. This report shows that the survival of antibiotic resistance in bacterial communities represents a complex process where many factors present in real-life systems define whether or not resistance is actually lost.
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Experimental microbial ecology and evolution have yielded foundational insights into ecological and evolutionary processes using simple microcosm setups and phenotypic assays with one- or two-species model systems. The fields are now increasingly incorporating more complex systems and exploration of the molecular basis of observations. For this purpose, simplified, manageable and well-defined multispecies model systems are required that can be easily investigated using culturing and high-throughput sequencing approaches, bridging the gap between simpler and more complex synthetic or natural systems. Here we address this need by constructing a completely synthetic 33 bacterial strain community that can be cultured in simple laboratory conditions. We provide whole-genome data for all the strains as well as metadata about genomic features and phenotypic traits that allow resolving individual strains by amplicon sequencing and facilitate a variety of envisioned mechanistic studies. We further show that a large proportion of the strains exhibit coexistence in co-culture over serial transfer for 48 days in the absence of any experimental manipulation to maintain diversity. The constructed bacterial community can be a valuable resource in future experimental work.
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Understanding ecological and epidemiological factors driving pathogen evolution in contemporary time scales is a major challenge in modern health management. Pathogens that replicate outside the hosts are subject to selection imposed by ambient environmental conditions. Increased nutrient levels could increase pathogen virulence by pre-adapting for efficient use of resources upon contact to a nutrient rich host or by favouring transmission of fast-growing virulent strains. We measured changes in virulence and competition in Flavobacterium columnare, a bacterial pathogen of freshwater fish, under high and low nutrient levels. To test competition between strains in genotype mixtures, we developed a quantitative real-time PCR assay. We found that a virulent strain maintained its virulence and outcompeted less virulent strains independent of the nutrient level and resource renewal rate while a less virulent strain further lost virulence in chemostats under low nutrient level and over long-term serial culture under high nutrient level. Our results suggest that increased outside-host nutrient levels might maintain virulence in less virulent strains and increase their contribution to epidemics in aquaculture. The results highlight a need to further explore the role of resource in the outside-host environment in maintaining strain diversity and driving evolution of virulence among environmentally growing pathogens.
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Evolução Biológica , Doenças dos Peixes/microbiologia , Flavobacterium/patogenicidade , Animais , Aquicultura , Peixes , Flavobacterium/genética , Flavobacterium/metabolismo , Genótipo , VirulênciaRESUMO
Trade-offs play an important role in evolution. Without trade-offs, evolution would maximize fitness of all traits leading to a "master of all traits". The shape of trade-offs has been shown to determine evolutionary trajectories and is often assumed to be static and independent of the actual evolutionary process. Here we propose that coevolution leads to a dynamical trade-off. We test this hypothesis in a microbial predator-prey system and show that the bacterial growth-defense trade-off changes from concave to convex, i.e., defense is effective and cheap initially, but gets costly when predators coevolve. We further explore the impact of such dynamical trade-offs by a novel mathematical model incorporating de novo mutations for both species. Predator and prey populations diversify rapidly leading to higher prey diversity when the trade-off is concave (cheap). Coevolution results in more convex (costly) trade-offs and lower prey diversity compared to the scenario where only the prey evolves.