bioRxiv Science⌕ Search

Biology subjects

Becks, L.

Publications and source records attributed to Becks, L..

13 recordsLinked to original sources

Convergent responses to light stress in oligohymenophorean ciliates bearing green algal symbionts

Photosymbiosis has evolved multiple times independently in ciliates. However, these associations can be antagonized by shifts in environmental parameters that impose stress on the host, necessitating the evolution of mechanisms to contend with this stress and to control the symbiont population. To investigate whether convergent strategies have evolved among algae-bearing ciliates in the class Oligohymenophorea, we imposed light stress on three host species that represent at least two independent evolutionary origins of photosymbiosis and measured their cellular responses. Under high light, all three species experienced an initial drop in host cell density which recovered to levels commensurate with those under low-light conditions as they decreased their symbiont loads. We then performed a comparative transcriptomic study to investigate whether a core set of genes exists that is involved in this response. Thirty-one gene families possess differentially expressed transcripts across all three species that included the upregulation C1 and S28 class peptidases, genes involved in ROS mitigation, and a gene with potential involvement in mitochondrial remodeling associated with changes in algal symbiont load. We additionally found downregulation in Dicer, which could mitigate the processing of algal transcripts by the hosts RNAi machinery that are freed upon algal digestion, and downregulation of motor proteins that may reflect changes in the hosts swimming behaviors and transport of intracellular vesicles in response to light. The 31 gene families are present and widespread in non-symbiotic oligohymenophoreans, illustrating that a pre-existing genetic toolkit exists in this clade that helps explain how it is predisposed to evolving photosymbioses.

genomics↗

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↗

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↗

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↗

The mechanistic rules for species coexistence

Global biodiversity loss requires effective ecological community management, reliant on accurate predictions of species coexistence and community assembly1-4. Traditional methods, predicting coexistence from the effect of one species on another5-8 (i.e., phenomenologically), are sensitive to environmental context9-13. This is because they ignore the fundamental processes that can be applied across environments. While mechanistic approaches offer promise14-17, empirical tests remain rare18,19. Here, we integrated a mechanistic consumer-resource model with the growth of 12 phytoplankton species in monoculture over a range of phosphorous, nitrate or ammonium concentrations. We found that the mechanistic approach accurately predicts the composition of 960 communities across species richness and resource conditions. As confirmed by simulations, species competing for substitutable resources (ammonium vs. nitrate) exhibit greater diversity than those competing for essential resources (phosphorus vs. nitrate), especially when initial species richness is high. This is because when competing for essential resources, each species is likely to consume less of the resource that more limit its growth, violating the mechanistic rule of coexistence (each species must consume more of the resource that more limit it16). Our study highlights the power of the mechanistic approach in understanding and predicting species loss across environments and, ultimately, mitigating its pace.

ecology↗

Virophage replication mode determines ecological and evolutionary changes in a host-virus-virophage system

Giant viruses can control their eukaryotic host populations, shaping the ecology and evolution of aquatic microbial communities. Understanding the impact of the viruses own parasites, the virophages, on their control of microbial communities remains a challenge. Most virophages have two modes of host infection and replication. They can exist as free particles that co-infect a host cell with the virus and replicate but inhibit viral replication. Virophages can also integrate into the host genome and remain dormant until the host is infected with a virus, leading to virophage reactivation and replication that does not immediately inhibit viral replication. Both replication modes are present within host-virus-virophage communities, and their relative contributions are expected to be context dependent and dynamic over time. The consequences of this dynamic regime for ecological and evolutionary dynamics remain unexplored. Here, we test whether and how the relative contribution of virophage replication modes influences the ecological dynamics of an experimental host-virus-virophage system and the evolutionary responses of the virophage. To do this, we indirectly manipulated the level of virophage (Mavirus) integration into the host (Cafeteria burkhardae) in the presence of the giant Cafeteria roenbergensis virus (CroV) (later identified as Cafeteria burkhardae, Schoenle et al. 2020). Our results show that higher virophage integration is positively correlated with host survival, but negatively correlated with virophage reactivation. In addition, communities with higher virophage integration were characterised by lower population densities and reduced fluctuations in both host and viral populations, whereas virophage fluctuations were increased. This study reveals the complex interplay between virophages, viruses and hosts, in which the virophage dual replication mode is a dynamic and reactive mechanism contributing to persistence of the microbial community.

evolutionary biology↗

Seasonal genotypic and phenotypic differentiation of a cosmopolitan freshwater diatom

Most ecosystems are characterized by seasonality, which, through biotic and abiotic changes, influences species biomass dynamics. Recent studies have shown that ecologically important traits can evolve rapidly in response to environmental changes, resulting in eco-evolutionary dynamics with consequences for population and community dynamics. Evidence for seasonal effects on intraspecific variation is still scarce and understanding eco-evolutionary dynamics in the presence of seasonal fluctuations remains a major challenge. Following the phytoplankton spring bloom in Lake Constance, we investigated how seasonal changes influence the intraspecific diversity of Asterionella formosa both at genotypic and phenotypic levels. We found a high degree of genetic and phenotypic differentiation characterizing Asterionella population, explained by a clustering of the isolates into early and late spring according to lake thermal stratification. Yet, most traits related to environmental parameters as well as fitness in different seasonal environments did not show a clear response to seasonality (i.e., temperature and nutrients), indicating that seasonal changes in biotic interactions (i.e., parasitic chytrids) were the major drivers of the observed seasonal shift in Asterionella genotypes. Our results highlight the importance of studying eco-evolutionary processes for understanding variations in population and community dynamics in response to seasonal environmental fluctuations.

ecology↗

Population dynamics hide phenotypic changes driven by subtle chemical exposures: implications for risk assessments

Ecological risk assessment of chemicals focuses on the response of different taxa in isolation not taking ecological and evolutionary interplay in communities into account. Its consideration would, however, allow for an improved assessment by testing for implications within and across trophic levels and changes in the phenotypic and genotypic diversity within populations. We present a simple experimental system that can be used to evaluate the ecological and evolutionary responses to chemical exposure at microbial community levels. We exposed a microbial model system of the ciliate Tetrahymena thermophila (predator) and the bacterium Pseudomonas fluorescens (prey) to iron released from Magnetic Particles (MP-Fedis), which are Phosphorus (P) adsorbents used in lake restoration. Our results show that while the responses of predator single population size differed across concentrations of MP-Fedis and the responses of prey from communities differed also across concentration of MP-Fedis, the community responses (species ratio) were similar for the different MP-Fedis concentrations. Looking further at an evolutionary change in the bacterial preys defence, we found that MP-Fedis drove different patterns and dynamics of defence evolution. Overall, our study shows how similar community dynamics mask changes at evolutionary levels what would be overlooked in the design of current risk assessment protocols where evolutionary approaches are not considered.

evolutionary biology↗

Evolution of virus and virophage facilitates persistence in a tripartite microbial system

Tripartite biotic interactions are inherently complex, and the strong interdependence of species and high levels of exploitation can make these systems short-lived and vulnerable to extinction. The persistence of species depends then on the balance between exploitation and avoidance of exploitation of the resource beyond the point where sustainable exploitation is no longer possible. We used this general prediction to test the potential for long-term persistence in a recently discovered tripartite microbial system in which a eukaryotic host is preyed upon by a giant virus that is in turn parasitized by a virophage. Host and virophage may benefit from this interaction because the virophage reduces the harmful effects of the giant virus on the host population over time and the virophage can survive integrated into the host genome when giant viruses are scarce. Here, we grew hosts in the presence and absence of the giant virus and virophage over ~280 host generations. We found that the three players persisted, but that the beneficial effect of the virophage for the host population diminished over time. We further tested whether the level of exploitation and replication evolved in the giant virus and/or virophage population over the course of the experiment and whether the changes were such that they avoid overexploitation. We found that the giant virus evolved towards lower replication levels and the virophage towards increased replication but decreased giant virus exploitation. These changes are predicted to facilitate persistence by lowering giant virus and host exploitation and consequently reducing the protective effect of the virophage.

evolutionary biology↗

Change in prey genotype frequency rescues predator from extinction

Indirect evolutionary rescue (IER) is a mechanism where a non-evolving population is saved from extinction in an otherwise lethal environment by evolution in an interacting population. This process has been described in a predator-prey model, where extinction of the predator is prevented by a shift in the frequency of defended towards undefended prey when reduced predator densities lower selection for defended prey. We test here how increased mortality and the initial frequencies of the prey types affect IER. Combining the analysis of model simulations and experiments with rotifers feeding on an algal population we show IER in the presence of increased predator mortality. We found that IER was dependent on the ability of the prey population to evolve as well as on the frequency of the defended prey. High initial frequencies of defended prey resulted in predator extinction despite the possibility for prey evolution, as the increase in undefended prey was delayed too much to allow predator rescue. This frequency dependency for IER was more pronounced for higher predator mortalities. Our findings can help informing the development of conservation and management strategies that consider evolutionary responses in communities to environmental changes.

evolutionary biology↗

Life history diversity and signals of trade-offs in a large group of chloroviruses

Phytoplankton viruses are key players in aquatic ecosystems, where they control algal populations and affect nutrient flow. The ecological impact and evolution of these viruses can be understood by studying their life history traits, but very little is known about the life history diversity of related viruses. We quantified the life cycle of 34 strains in the genus Chlorovirus, which infects freshwater green algae. All chloroviral life history traits varied 5-to 75-fold across strains, in some cases rivaling the known trait range for all phytoplankton viruses. The trait variation affected viral growth rates but was not detectably constrained by life history trade-offs. This study represents the most in-depth characterization of algal viruses to date and raises the question whether all phytoplankton virus genera are equally diverse.

evolutionary biology↗

Evolutionary dynamics of transposable elements in bdelloid rotifers

Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates where males are thus far unknown. Contrary to expectations, we find a diverse range of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms, but we report that bdelloids share a large and unusual expansion of genes involved in RNAi-mediated TE suppression. This suggests that enhanced cellular defence mechanisms might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.

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↗