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Hiltunen, T.

Publications and source records attributed to Hiltunen, T..

13 recordsLinked to original sources

Eco-evolutionary dynamics and environmental detoxification jointly shape bacterial community response to antibiotic perturbation

Microbial communities frequently encounter recurrent antibiotic disturbance, yet how ecological, evolutionary, and environmental processes jointly shape the response remains unresolved. Here we experimentally disentangle these mechanisms using a 23-species bacterial community exposed to ampicillin pulses with pre-pulse and resistance priming. Pre-pulse priming preconditioned community composition toward resistant taxa, reducing compositional change during the main pulse. Resistance priming was the dominant determinant of community response, buffering compositional change, relaxing selection, and altering gene expression. This buffering arose from both evolution of higher resistance and accelerated ampicillin detoxification by a dominant degrader, which transiently reduced antibiotic effects and favoured non-degrading taxa. Yet buffering did not translate into better recovery: because resistance was coupled to competitive dominance, diversity remained comparable to or below that of ancestral communities, and dominance was reinforced. Together, we show that antibiotic history reshapes microbial disturbance response through coupled eco-evolutionary and environmental feedbacks, generating a trade-off between resistance and recovery.

evolutionary biology↗

Ecological tristability driven by total carbon availability over resource complexity in a synthetic microbial community

Even though complex microbial communities are ubiquitous and provide essential services for natural and human-associated ecosystems, our knowledge about their assembly and dynamics is incomplete. There is an ongoing debate whether the behavior of complex communities can be predicted from the outcome of pairwise competition of species, and whether communities reach alternative stable states depending on the level and complexity of resource provided for growth. To estimate the effect of two resource gradients, total carbon availability and resource complexity, on the compositional dynamics of a complex microbial community, we conducted a 16-day serial passage experiment, transferring a 16-species synthetic community in 96 different resource environments. We observed that although both resource dimensions influenced community composition, total carbon exerted a considerably larger effect. Additionally, we saw the emergence of a tristable pattern along the total carbon gradient, a feature not observed for the resource complexity gradient. Using monoculture assays, we identified lag phase duration as the dominant predictor of competitive success at carbon extremes, with maximum growth rate increasing in importance as lag times converged. Total carbon availability thus structured community state transitions and regulated which growth trait governed competitive sorting. These results suggest the importance of total carbon level over resource complexity and identifying dominant species for the quest to successfully manage, maintain and manipulate complex microbial communities.

ecology↗

Normative assembly rule reveals fairness in microbial communities

Understanding and predicting how communities assemble is a paramount challenge in ecology. Here we address these questions normatively by comparing the ecological distribution of growth surplus to a game-theoretically fair distribution based on each species Shapley value. By analyzing in total 56 distinct community outcomes, we assess how fairly biomass is distributed in microbial communities displaying both competitive and cooperative interactions in different environmental conditions. We find examples of fair communities that closely follow their Shapley value across all environments as well as counterexamples where the true abundances deviate from the species objective contribution to community biomass. Our results give unique empirical insights into the distributive function of ecological dynamics and lay down the theoretical foundations of what might become a normative community assembly theory.

ecology↗

Evolution induced state shifts in a long-term microbial community experiment

Biological communities are complex, dynamic systems that underpin ecosystem functionality1, yet their long-term dynamics and predictability remain poorly understood2. Understanding how Darwinian evolution shapes these systems through eco-evolutionary feedbacks is a central challenge in ecology and evolution. Experimental studies using simplified microbial assemblages have yielded important insights into the ecological principles governing community states3-5. However, an important knowledge gap is how selection within member species drives changes of community state in multispecies systems. Here, we present a four-year evolution experiment involving a 23-species synthetic bacterial community propagated in two environments: a control medium and the same medium supplemented with the antibiotic streptomycin. Through combined analyses of community composition and genome evolution, we quantified the temporal changes in species abundances and the evolutionary trajectories of individual community members. The extended duration of the experiment enabled the detection of adaptive mutations and community state shifts that occur only over long evolutionary timescales. We show that community dynamics are environment dependent and reproducible across replicates, and that evolution of streptomycin resistance in a previously streptomycin-sensitive species on its own can induce abrupt community state shifts. Our results provide a direct demonstration of eco-evolutionary feedbacks within a multi-species community, revealing how a single adaptive mutation can reorganize complex ecological networks.

ecology↗

Data-driven symbolic regression reveals microbial growth laws

O_LIConnecting mathematical models with empirically measured microbial growth has remained challenging, as numerous competing models based on different theoretical approaches can fit observations. Therefore, we develop a method to automatically propose growth models from microbial data alone. We validate this approach using an available dataset of E. coli grown on known resources, and study sixteen species across various concentrations of a rich medium. C_LIO_LIThe inherently interpretable approach of symbolic regression infers explicit dynamical models directly from growth data. Using symbolic regression natively, does not favour biologically interpretable models, but we find cumulative population gain to be a more informative machine learning feature than population size. C_LIO_LIRandom Forest machine learning allows us to relate this finding to the approximation of a constant-rate per capita resource consumption. This suggests that the area under the growth curve (AUC) measured in routine experiments provides information on the effective resource dynamics governing microbial growth. Finally, we use theoretical insights to inform the symbolic regression algorithm and favour biologically interpretable models. C_LIO_LIOverall, we found that balancing between data fit, parsimony and biological relevance favoured both the simplest, linear approximation, and models based on a Monod dynamics, with either one or two underlying resources. Therefore, our approach to read growth laws off of microbial batch cultures provides insights on data-driven modelling. C_LI

ecology↗

ESBL plasmid compatibility with the surrounding microbial community influences ESBL gene survival under CRISPR-antimicrobial targeting

Bacteria often acquire resistance against antibiotics through the transfer of conjugative resistance plasmids. Hence, it is vital to develop strategies to mitigate the dispersal of antimicrobial resistance (AMR). CRISPR-based antimicrobial tools offer a sequence-specific solution to diminish and restrict the dissemination of antimicrobial resistance genes among bacteria. CRICON (CRISPR via conjugation) is an antimicrobial CRISPR tool that has been shown to efficiently reduce multi-resistance when targeting ESBL (Extended Spectrum Beta-Lactamase) harboring plasmids. However, conjugatively delivered genetic elements may be subjected to bacterial defense, lead to resistance development, and revert the efficiency of the CRISPR tools. Here, we studied the evolutionary consequences of four ESBL-harboring Escherichia coli strains targeted by CRICON in a 10-day multispecies microcosm experiment. We show that CRICON reduces the ESBL prevalence within the bacterial community, while the final ESBL persistence depends on the initial community composition. We observed an unexpected survival strategy of an ESBL-plasmid by escaping into a more competitive host species. Further, we show the development of partial resistance against the CRISPR-antimicrobials during the experiment. Our results underline the importance of the ecological and evolutionary factors in multispecies bacterial communities, as they may disrupt the effective use of CRISPR-based antimicrobial strategies via undesired outcomes of targeted therapies against plasmid-bearing multi-resistant bacteria.

microbiology↗

Universal bacterial clade dynamics dominate under predation despite altered phenotypes and mutation targets

Recent studies have revealed bacterial genome-wide evolution to be complex and dynamic even in a constant environment, characterized by the emergence of new clades competing or temporarily coexisting as each clade undergoes evolutionary change. Previous studies on predator-prey dynamics tracking simple ecological and phenotypic metrics have shown predation to fundamentally alter prey evolution, facilitating defense evolution followed by coevolution and frequency dependent selection between defended and undefended prey genotypes. Here we sought to consolidate these fields by examining genome-wide evolution in five bacterial prey species separately subjected to long-term evolution under ciliate predation. We hypothesized that the presence of predation could change the pattern of clonal dynamics, for example, by more frequently producing selective sweeps if predation-defense-related mutations are under strong selection. For all species, we found mutational signals of prey adaptation, with phenotypic data and genomic mutation targets demonstrating changes in composition between the experimental treatments. Intriguingly, despite higher variant counts, overall temporal clade dynamics across the coevolved prey species were strikingly similar to those of bacteria evolving alone, with constant emergence, competition and quasi-stable coexistence of clades. This study shows that long-term molecular evolution in bacterial prey under predation is more interesting and less predictable than we might expect based on existing coevolutionary theories.

evolutionary biology↗

Localized coevolution between microbial predator and prey alters community-wide gene expression and ecosystem function

In dynamic and spatially heterogeneous microbial communities, pairs of locally coevolved species interact between themselves and other species across multiple spatial and temporal scales. We currently do not understand how local pairwise coevolutionary processes scale to influence whole microbial communities and how local coevolutionary processes affect wider species interaction networks. Here we investigate the community-wide functional response to a coevolutionary mismatch between a focal bacterial prey species and its ciliate predator in a synthetic 30 species microbial community over two months. We observed that the coevolved prey had little influence 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 coevolved focal species. 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 species. Our findings suggest that the disruption of localized pairwise coevolution can alter community-wide transcriptional networks, even when the overall ecological response is muted. We propose that these altered expression patterns may be an important signal of future diversification and ecological change. SignificanceClosely 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 an idealized 30 species microbial community where we experimentally manipulated the coevolutionary history of a predator and a single prey species. Altering the coevolutionary history of the prey had little effect on the ecology of the system but induced large functional changes in community transcription and metabolic potential. Our results illustrate that localized coevolutionary processes between species pairs can reverberate through ecosystem-scale transcriptional networks with important consequences for broader ecosystem function.

ecology↗

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus populations in separate ocean basins often mirrors the selective pressures imposed by the regions 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 low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus 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, particularly 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 Prochlorococcus.

ecology↗

Within-species trait diversity reorganizes consumer competitive hierarchy and prey community structure in an experimental microbial ecosystem

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 favor 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 ciliates 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 defense 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.

ecology↗

Strong Selective Agents Determine Resistance Evolution in a Multidrug Therapeutic Regime

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 utilising 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 -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.

evolutionary biology↗

Repeatable ecological dynamics govern response of experimental community to antibiotic pulse perturbation

In an era of pervasive anthropogenic ecological disturbances, there is a pressing need to understand the factors constituting 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 experiencing antibiotic perturbation represent a key system with important medical dimensions. However, previous microbiome studies on the 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 passaged 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 by amplicon sequencing, we combined 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, owing to an increasingly strong yet canalized response at increasing antibiotic levels, which could be partly attributed to key species traits (antibiotic susceptibility and growth rate). Increasing antibiotic levels were also coupled with increasing species extinction probability, making species immigration preventing this critical for community resilience. Moreover, we could detect 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 which appears as classic species sorting but is nevertheless accompanied by rapid within-species evolution.

ecology↗

Coevolution alters predator life history traits, behavior and morphology in experimental microbial communities

Predator-prey interactions are key for the dynamics of many ecosystems. An increasing body of evidence suggests that rapid evolution and co-evolution can alter these interactions, with important ecological implications, by acting on traits determining fitness, including reproduction, anti-predatory defense 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 ~600 generations in a predator-prey (ciliate-bacteria) evolutionary experiment. Predators independently evolved on seven different prey species, allowing generalization of the predators evolutionary response. We used highly resolved automated image analysis to quantify changes in predator life history, morphology and behavior. Consistent with previous studies, we found that prey evolution impaired growth of the predator. In contrast, predator evolution did not cause a clear increase in fitness when feeding on ancestral prey. However, predator evolution affected morphology and behavior, 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 offense level without translating into an increased ability of the predator to grow on the ancestral prey type.

evolutionary biology↗