Search bioRxiv⌕ Search

Biology subjects

Krenek, S.

Publications and source records attributed to Krenek, S..

7 recordsLinked to original sources

Evolutionary Dynamics of Paramecium Mitochondrial Genomes

Ciliates are a diverse group of single-celled eukaryotes that can exhibit a wide range of genetic diversity within morphologically indistinguishable species. However, they are still not well studied as their mechanisms of speciation and the extent of diversification remain unknown. Mitochondrial genomes offer an effective framework for resolving species relationships and evolutionary changes. Here, we analyzed a globally sampled dataset of Paramecium to understand the evolution of mitochondrial genomes in ciliates. Phylogenetic analysis of linear mitochondrial genomes shows the presence of cryptic diversity beyond the P. aurelia complex, with P. bursaria lineage appearing as a deeply diverging out-group. Protein-coding genes are largely conserved, with limited rearrangements, and some ciliate-specific genes appear to be missing in P. bursaria. Population genetic analysis show little to no evidence of recombination along with substantial differences in effective population size across species. Patterns of molecular evolution also indicate purifying selection as the predominant force, the strength of which is at least as strong as in the nucleus and consistent with mitochondrial effective population sizes that are similar or larger than those of the nucleus. Across the functional groups, the electron transport chain and ribosomal genes are highly constrained, while ciliate-specific ymf genes show reduced efficacy of selection compared to the others. These findings offer a basis for connecting mitochondrial variation to evolutionary divergence, functional constraint, and speciation in microbial eukaryotes.

genomics↗

Shifts in the population-genetic landscape of the ciliate genus Paramecium

Ciliates are one of the most ecologically diverse and morphologically intricate unicellular organisms. Despite their evolutionary significance and their prominence in cell-biological research, the population-genetic processes governing their diversification have received remarkably little attention. A fundamental unresolved problem is the existence of geographic isolation among free-living protists and its consequences for species richness. We addressed this issue in the model ciliate Paramecium by sequencing genomes of hundreds of isolates collected worldwide, capturing multiple morphological and cryptic species, with multiple populations each. Contrary to previous reports, we found evidence of geographic differentiation in the majority of species. In a few cases, geographic structure became evident when deeply diverging clades in a species were treated separately. This suggests that the biogeographical patterns of Paramecium have been shaped by periods of genetic isolation leading to speciation, with rare events of global dispersal realized over its long evolutionary history. Despite being largely isolated, populations were remarkably similar in their effective population size, recombination rate, and efficacy of natural selection. Across species, selection appears to be least effective in Paramecium aurelia lineages, and most effective in P. bursaria, presumably due to differences in their breeding characteristics. Despite differences among species in the population-genetic environment, patterns of variation across the genome remained consistent. Selective constraints on a core set of genes seemed to have gradually diverged across the species phylogeny. Genes with multiple copies retained from whole-genome duplication events in P. aurelia were found to be under relatively relaxed purifying selection. Moving forward, this dataset will serve to test hypotheses on the ecological and cellular complexity of Paramecium and beyond.

evolutionary biology↗

Predicting evolution in experimental range expansions of an aquatic model system

Predicting range expansion dynamics is a challenge for both fundamental and applied research in conservation and global change biology. However, if ecological and evolutionary processes occur on the same time scale, predictions are challenging to make. Combining experimental evolution and mathematical modelling, we assessed the predictability of independent realisations of range expansions in a laboratory model system, the freshwater protozoan Paramecium caudatum. We followed ecological dynamics and evolutionary change in range core and front populations in the experiment. These settings were recreated in a predictive mathematical model, parametrized with dispersal and growth data of the of the 20 founder strains in the experiment. We find that short-term evolution was driven by selection for increased dispersal at the front and general selection for higher growth rates in all treatments. There was a good quantitative match of predicted and observed trait changes. Phenotypic divergence was mirrored by a complete genotypic divergence, indicating the highly repeatable fixation of strains that also were the most likely winners in our model. Long-term evolution in the experimental range front lines resulted in the emergence of a dispersal syndrome, namely a competition - colonisation trade-off. Altogether, both model and experiment highlight the importance of dispersal evolution as a driver of range expansions. Our study suggests that evolution at range fronts may follow predictable trajectories, at least for simple scenarios, and that predicting these dynamics may be possible from knowledge of few key parameters.

evolutionary biology↗

Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes

Ciliates are unicellular eukaryotes with both a germline genome and a somatic genome in the same cytoplasm. The somatic macronucleus (MAC), responsible for gene expression, is not sexually transmitted but develops from a copy of the germline micronucleus (MIC) at each sexual generation. In the MIC genome of Paramecium tetraurelia, genes are interrupted by tens of thousands of unique intervening sequences, called Internal Eliminated Sequences (IESs), that have to be precisely excised during the development of the new MAC to restore functional genes. To understand the evolutionary origin of this peculiar genomic architecture, we sequenced the MIC genomes of nine Paramecium species (from [~]100 Mb in P. aurelia species to > 1.5 Gb in P. caudatum). We detected several waves of IES gains, both in ancestral and in more recent lineages. While the vast majority of IESs are single-copy in present-day genomes, we identified several families of mobile IESs, including non-autonomous elements acquired via horizontal transfer, that generated tens to thousands of new copies. These observations provide the first direct evidence that transposable elements can account for the massive proliferation of IESs in Paramecium. The comparison of IESs of different evolutionary ages indicates that, over time, IESs shorten and diverge rapidly in sequence while they acquire features that allow them to be more efficiently excised. We nevertheless identified rare cases of IESs that are under strong purifying selection across the aurelia clade. The cases examined contain or overlap cellular genes that are inactivated by excision during development, suggesting conserved regulatory mechanisms. Similar to the evolution of introns in eukaryotes, the evolution of Paramecium IESs highlights the major role played by selfish genetic elements in shaping the complexity of genome architecture and gene expression.

genomics↗

Heritable variation in resistance to the endonuclear parasite Holospora undulata across clades of Paramecium caudatum

Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of genetic variation in this trait can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative genetic variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains (with broad-sense heritability > 0.5), repeatable between laboratories and ranging from total resistance to near-complete susceptibility. Early (one week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2-3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural genetic variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.

genetics↗

When enemies do not become friends: Experimental evolution of heat-stress adaptation in a vertically transmitted parasite

Strict vertical (parent-to-offspring) transmission of symbionts may be associated with benevolence and mutualism, because host reproduction and symbiont transmission are linked. Nonetheless, many such symbionts do reduce host fitness costs and the factors driving their evolution are unclear. Using microcosm populations of Caedibacter taeniospiralis, a vertically transmitted bacterial symbiont of the protozoan Paramecium tetraurelia, we investigated evolutionary change under permissive conditions (26{degrees}C) and under heat stress (32{degrees}C), over 150 host generations. We found evidence for symbiont adaptation to heat stress, involving increased infection persistence and, consequently, higher rates of vertical transmission. For certain genetic backgrounds, heat-stress adaptation was associated with higher proliferation of infected lines at 26{degrees}C, suggesting cost-free evolution of super-generalists. Despite a general decrease in symbiont virulence relative to ancestral strains, infected evolved lines still showed substantial reductions (>20%) in population growth. There was no sign of a temperature-specific reduction in virulence or protection of the host against heat stress. Our results show that obligately vertically transmitted symbionts can still qualify as parasites and evolve adaptations that do not help their hosts. Long-term infection persistence might require additional mechanisms, such as the symbiont-mediated killer trait in this system, allowing the selective elimination of uninfected individuals in the population.

evolutionary biology↗

Outwitting planarians antibacterial defence mechanisms: Rickettsiales bacterial trans-infection from Paramecium multimicronucleatum to planarians

Most of the microorganisms belonging to genera responsible for vector-borne diseases (VBD) have hematophagous arthropods as vector/reservoir. Recently, many new species of microorganisms phylogenetically related to agents of VBD were found in a variety of aquatic eukaryotic hosts, in particular, numerous new bacterial species related to the genus Rickettsia (Alphaproteobacteria, Rickettsiales) were discovered in protist ciliates and other unicellular eukaryotes. Although their pathogenicity for humans and terrestrial animals is not known, these bacteria might act as etiological agents of possible VBD of aquatic organisms, with protist as vectors. In the present study, we characterized a novel strain of the Rickettsia-Like Organism (RLO) endosymbiont \"Candidatus (Ca.) Trichorickettsia mobilis\" in the macronucleus of the ciliate Paramecium multimicronucleatum through Fluorescence In Situ Hybridization (FISH) and molecular analyses. Ultrastructural investigations on the presence of flagella confirmed previous studies on the same bacterial species. The potential trans-infection per os of this bacterium to planarians (Dugesia japonica), a widely used model system able to eliminate a wide range of bacteria pathogenic to humans and other Metazoa, was further verified. Ciliate mass cultures were set up, and trans-infection experiments were performed by adding homogenized paramecia to food of antibiotic-treated planarians, performed. Treated and non-treated (i.e. control) planarians were investigated at day 1, 3, and 7 after feeding for endosymbiont presence by means of PCR and ultrastructural analyses. Obtained results were fully concordant and suggest that this RLO endosymbiont can be transferred from ciliates to metazoans, being detected up to day 7 in treated planarian enterocytes inside and, possibly, outside phagosomes.

microbiology↗