bioRxiv Science⌕ Search

Biology subjects

Piganeau, G.

Publications and source records attributed to Piganeau, G..

13 recordsLinked to original sources

Epidemiological model selection unravels the molecular processes of antiviral resistance from experimental phytoplankton-virus dynamics

Phytoplankton-virus interactions are pivotal in understanding the intertwined dynamics of these key players of the global carbon cycle. Although antiviral resistance is the main hypothesis to solve the apparent paradox of their coexistence, identifying its molecular determinisms and mechanisms, as well as their dynamical consequences, remains challenging. By combining hypotheses about such determinisms and mechanisms, we designed 36 dynamical models and fitted them to experimental infection kinetics in a pioneering selection model approach. Through such a multiple hypotheses testing, we identified that resistance in the model species Ostreococcus tauri is most likely to be predominantly intracellular, to control lysis through budding, and to be acquired by phenotypic plasticity. We further showed that viral kinetics are strongly impacted by both the antiviral resistance's molecular determinants and virions' inactivation through attachment to lysis detritus, as the latter generates a key negative feedback loop during the 'bust' stage of the interaction dynamics.

ecology↗

How do the molecular determinants of antiviral resistance shape the dynamic of phytoplankton-virus interaction?

Phytoplankton sustain all marine ecosystems and are key components of the carbon cycle being responsible for ~50% of the global primary production. A major hypothesis to explain their coexistence with highly efficient lytic viruses is antiviral resistance. Although intracellular and extracellular mechanisms have been shown to underly such resistance and while its determinism is commonly associated to a genomic polymorphism or a (random or virus induced) phenotypic plasticity, comparisons of the impact of those molecular determinants on phytoplankton-virus population dynamic are genuinely lacking. We combined 12 epidemiological models with an unprecedented set of parameter estimates derived from experimental studies of the ubiquitous species Ostreococcus tauri and its prasinoviruses to provide such comprehensive predictions. We show that 'bet-hedging' strategies corresponding to random phenotypic switches between susceptible and resistant cells provide the strongest barrier to virus emergence. When such resistance is associated to intracellular mechanisms the virus' R0 is at least halved because of the strong 'dilution effect' produced by the 'dead-end' hosts. In addition, once the virus has spread, both random and virus-induced phenotypic plasticity strongly stabilize the otherwise 'boom and bust' phytoplankton-virus dynamics, which is highly consistent with the experimental dynamics observed for such interactions.

ecology↗

Plasticity of the mutation rate and spectrum in eukaryotic marine phytoplankton

The ability to adapt shapes the future of any species or population. Adaptive potential is primarily determined by the spontaneous mutation rate {micro} and the mutation spectrum, which define the new genetic variation available to selection. Increasing evidence points to the plasticity of the mutation rate and spectrum, which vary according to environment. However, data is lacking for marine phytoplankton, an essential group for marine ecosystems as well as a major player in biogeochemical cycles. Here, we measure the plasticity of mutation rates and spectra in the chlorophyte Ostreococcus tauri by mutation accumulation experiments in 4 different conditions: low salinity, high salinity, low temperature, and high temperature. {micro}SNM is lowest under low salinity, doubles under high salinity and low temperature and quadruples under high temperature. SNM spectra become increasingly biased towards C:G[->]T:A transitions with increasing {micro}SNM. While {micro}ID does not change with the environment, the structural mutation rate {micro}SM is higher at low temperature, likely due to transposon activity. Given the rapid environmental changes associated with global climate change, mutation rates and spectra plasticity may critically influence the adaptive potential of marine primary producers.

evolutionary biology↗

Metabolomic and Transcriptomic rewiring between virus resistance and susceptibility in Ostreococcus mediterraneus

The genus Ostreococcus, comprising picoeukaryotic unicellular algae, plays a key role in many coastal marine ecosystems. These phytoplankton are infected by lytic double-stranded DNA prasinoviruses against whom they have the capacity to reliably evolve stable antiviral resistance. Regulation of virus resistance and susceptibility is hypothesized to arise through a phenotypic switch, as resistant cell lines can be isolated from susceptible lines after viral exposure and vice versa. To elucidate the molecular mechanisms underlying this resistance, we integrated untargeted metabolomic analyses and transcriptomics in virus-resistant and virus-susceptible lines of O. mediterraneus. Transcriptomic analyses corroborated previous findings in O. tauri, revealing that most gene expression changes were concentrated on a single chromosome. Specifically, a [~]530 kb region was over-transcribed in virus-resistant lines, while a distinct [~]110 kb region was over-expressed in virus-susceptible lines. Comparative metabolomics identified several oxidized galactolipids and oxidized sterols as biomarkers of the susceptible phenotype, while fewer biomarkers were identified for the resistant phenotype. By integrating transcriptomic and metabolomic signatures--focusing on the expression of genes within biosynthetic pathways linked to these metabolite biomarkers--we uncovered candidate molecular mechanisms underlying the cellular physiology of susceptible versus resistant phenotypes. Authors SummaryViruses are the most abundant biological entities in the ocean, shaping the dynamics of phytoplankton communities that underpin marine food webs. Ostreococcus, one of the smallest photosynthetic eukaryotes, is frequently infected by highly abundant prasinoviruses in its natural environment. In this study, we aimed to understand the physiological bases of virus-resistant and susceptible Ostreococcus mediterraneus lines. We compared gene expression and untargeted metabolite profiles between a resistant line and a susceptible line derived from it. The metabolic profiles were much more variable between replicates than the transcriptomic profiles and the most differentially expressed genes did not include those involved in the biosynthetic pathways of the metabolite biomarkers identified. We estimated the congruence between the metabolomes and transcriptomes as the percent of relative expression changes fitting to the relative change in the metabolite. This study provides evidence of the subtle links between gene expression and metabolomic signatures and the importance of integrating multiple levels of cellular processes.

microbiology↗

Ancient eukaryotic immunity through genome editing of viral sequences

Mutations provide the raw material for evolution, but mutation rates are not uniform across genomes. Using a mutation accumulation experiment in the marine phytoplankton Bigelowiella natans, we discovered extreme local variation in mutation rate: over 1000-fold differences across its nuclear genome. While the baseline single-nucleotide mutation rate is approximately 3.5x10-10 per site per generation, a common value for unicellular species, two genomic regions derived from integrated viruses exhibit strikingly elevated rates of about 6x10-7. These two regions show a distinctive mutational signature with almost exclusively T/A[->]C/G transitions, a pattern also found in other non-eukaryote derived sequences in B. natans, contrary to the usual GC to AT mutation bias. Notably, hypermutation occurs only on TpA dinucleotides, and only in a subset of experimental lines, suggesting a regulated process rather than random genomic instability. We propose that B. natans targets invading DNA through localized hypermutation, reminiscent of deamination-based antiviral defense systems in animals, prompting the idea of genome editing as a conserved immune system in eukaryotes. Significance StatementDe novo mutations provide the raw material for adaptation, but at high frequencies they can compromise genome integrity. Here, we describe a hypermutable process targeting two integrated viral genomes in a chlorarachniophyte alga, resulting in a mutation rate 1000 times higher than in other regions and a very particular mutation spectrum. These observations are reminiscent of hypermutation-based antiviral defenses described in humans against HIV and influenza; whereby host-mediated deamination of the viral genome increases its mutation rate such that the virus loses its infectivity.

genomics↗

Environmental complexity constrains evolutionary adaptation across taxa

Complex environments combining multiple stressors are the new norm worldwide. Adaptive evolution will be critical to population persistence under these combined challenges, but how environmental complexity affects the pace of evolution remains poorly understood. Using a meta-experimental evolution approach, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors and their pairwise combinations for multiple generations, while keeping the overall stress level comparable. Populations evolving under combined stressors tended to have lower fitness increase in the selective environments, higher fitness reductions in the control environment, and shallower relation between initial maladaptation and fitness gain, than under single stressors. However, these responses varied with species and stressor type. Accounting for such constraints on evolutionary dynamics should prove crucial for the management of biodiversity. Significance StatementA pressing challenges for modern science and society in the face of ongoing global change is understanding what limits the capacity of living organisms to adapt to complex environments combining multiple stressors. To answer to this question, we conducted a large-scale meta-experimental evolution design across a diversity of organisms, exposing them for multiple generations to either single or combined-stress treatments. Combined stressors led to less adaptive fitness gain than single stressors, and imposed additional costs through reduced fitness in non-stressful conditions. This unique combination of meta-experimental approach with a careful distinction between environmental complexity and overall stress allowed us to gain robust quantitative evidence on how environmental complexity can impact the pace of evolution.

evolutionary biology↗

Chromoanagenesis is a driver of structural variationin the smallest photosynthetic eukaryote

Marine microalgae populations can rapidly evolve resistance to viruses upon infection. In Ostreococcus mediterraneus resistance to the prasinovirus OmV2 emerged within five days in all virus-exposed populations. Whole-genome sequencing of pairs of resistant and susceptible cell lines revealed extensive structural genomic changes, particularly on the Small Outlier Chromosome (SOC). SOC alterations included large deletions, duplications, rearrangements, and whole chromosome duplication, yet no consistent structural variant or single nucleotide polymorphism could be directly associated with resistance. Hybrid de novo assemblies confirmed the unique SOC assembly of each strain, with a highly polymorphic [~]2 kb tandem repeat region exhibiting an "accordion-like" pattern of expansion and contraction. No new viral insertions were found, though endogenous viral elements were conserved across lines. Two interchromosomal translocations between the SOC and chromosomes 2 and 17 provide evidence for chromoplexy, thereby offering novel insights into the mechanisms underlying the distinctive evolutionary path of this chromosome. Together, these findings demonstrate that resistance to OmV2 evolves rapidly and consistently but cannot yet be linked to any specific structural variations; instead, the high rate of localized genomic structural variations points to a distinct mechanism of chromosome evolution. SignificanceThe mechanisms and consequences of structural variation remain poorly understood in many lineages, particularly in ecologically important marine microbes. This study shows that resistance to prasinovirus OmV2 in a cosmopolitan phytoplankton species, Ostreococcus mediterraneus evolves rapidly and consistently, even though no resistance-associated SNPs or shared structural variants were identified on standard chromosomes. Instead, extensive genomic rearrangements--particularly of a single chromosome--occur independently of viral infection. These findings highlight the role of chromoplexy as the driving mechanism underlying the diversification of the enigmatic Small Outlier Chromosome in this lineage.

genomics↗

Effect of cellular nutrient economy on the evolution of genome size in phytoplankton

The origin of genome size variation remains a central question in evolutionary biology. Previous analyses suggest that the energetic costs of small insertions and deletions (indels) influence genome size by altering the cellular energy budget. Here, we present a theoretical framework for genome evolution in phytoplankton--the main producers of the sunlit ocean--whose growth depends on nutrient availability. We derive an expression for the selection coefficient on indels as a function of the minimum amount of nutrient inside the cell. Parameter estimates indicate that 1-bp indels can be counterselected in phytoplankton with minimal nutrient requirements. We then test three predictions of nutrient-driven selection on genome evolution. Altogether, this model provides a quantitative and mathematical basis for the genome streamlining hypothesis.

ecology↗

Genome wide assessment of genetic diversity and transcript variations in 17 accessions of the model diatom Phaeodactylum tricornutum

Diatoms, a prominent group of phytoplankton, have a significant impact on both the oceanic food chain and carbon sequestration, thereby playing a crucial role in regulating the climate. These highly diverse organisms show a wide geographic distribution across various latitudes. In addition to their ecological significance, diatoms represent a vital source of bioactive compounds that are widely used in biotechnology applications. In the present study, we investigated the genetic and transcriptomic diversity of 17 accessions of the model diatom Phaeodactylum tricornutum including those sampled a century ago as well as more recently collected accessions. The analysis of the data reveals a higher genetic diversity and the emergence of novel clades, indicating an increasing diversity within the P. tricornutum population structure, compared to the previous study and a persistent long-term balancing selection of genes in old and newly sampled accessions. However, the study did not establish a clear link between the year of sampling and genetic diversity, thereby, rejecting the hypothesis of loss of heterozygoty in cultured strains. Transcript analysis identified novel transcript including non-coding RNA and other categories of small RNA such as PiwiRNAs. Additionally, transcripts analysis using differential expression as well as Weighted Gene Correlation Network Analysis has provided evidence that the suppression or downregulation of genes cannot be solely attributed to loss of function mutations. This implies that other contributing factors, such as epigenetic modifications, may play a crucial role in regulating gene expression. Our study provides novel genetic resources, which are now accessible through the platform PhaeoEpiview (https://PhaeoEpiView.univ-nantes.fr), that offer both ease of use and advanced tools to further investigate microalgae biology and ecology, consequently enriching our current understanding of these organisms.

genomics↗

High rates of spontaneous chromosomal duplications are compensated by translational regulation in a photosynthetic unicellular eukaryote

While duplications have long been recognized as a fundamental process driving major evolutionary innovations, direct estimations of spontaneous chromosome duplication rates, leading to aneuploid karyotypes, are scarce. Here, we provide the first estimations of spontaneous chromosome duplication rates in six unicellular eukaryotic species from mutation accumulation (MA) experiments. The spontaneous chromosome duplication rates reach 1x10-4 to 1x10-3 per genome per generation, which is ~4 to ~50 times less frequent than spontaneous point mutations per genome, whereas chromosome duplication events can affect 1 to 7% of the total genome size. Comparative transcriptomics between MA lines with different chromosome duplications reveals a strong positive correlation between RNA expression rate and DNA copy number. However, comparative analyses of the translation rate of mRNAs estimated by polysome profiling unravel a chromosome specific dosage compensation mechanism. In particular, one chromosome with a gene average of 2.1 excess of mRNAs is compensated by an average of ~0.7 decrease in translation rates. Altogether, our results are consistent with previous observations of a chromosome dependent effect of dosage compensation and provide evidence that it may occur during translation. These results support the existence of a yet unknown post-transcriptional mechanism orchestrating the modification of translation of hundreds of transcripts from genes located on duplicated regions in eukaryotes.

evolutionary biology↗

Equatorial to Polar genomic variability of the microalgae Bathycoccus prasinos

Phytoplankton plays a fundamental role in the ecology of ocean systems and is the key player in the global carbon cycle. At a time of global warming, understanding the mechanisms of its adaptation to temperature is therefore of paramount importance. Cosmopolitan planktonic species abundant in different marine environments provide both a unique opportunity and an efficient methodological tool to study the genomic bases of their adaptation. This is the case for the eukaryotic picoalga Bathycoccus prasinos, whose genomic variability we chose to study in temperate and polar oceanic waters. Using multiple metagenomic datasets, we found that ~5% of B. prasinos genomic positions are variable, with an overwhelming majority of biallelic motifs. Cold and temperate waters are clearly associated with changes in variant frequencies, whereas in transitional waters we found more balanced polymorphism at most of these positions. Mesophilic and psychrophilic gene variants are distinguished by only a few amino acid changes located at positions critical for physical and functional protein properties. These results provide new information on the genomic diversity of a cosmopolitan eukaryotic planktonic specie and reveal "minimal mutational strategies" which finely tune the properties of specific proteins at different temperatures.

genomics↗

Virus-host coexistence in phytoplankton through the genomic lens

Phytoplankton-virus interactions are major determinants of geochemical cycles in the oceans. Viruses are responsible for the redirection of carbon and nutrients away from larger organisms back towards microorganisms via the lysis of microalgae in a process coined the viral shunt. Virus-host interactions are generally expected to follow boom and bust dynamics, whereby a numerically dominant strain is lysed and replaced by a virus resistant strain. Here, we isolated a microalga and its infective nucleo-cytoplasmic large DNA virus (NCLDV) concomitantly from the environment in the surface NW Mediterranean Sea, Ostreococcus mediterraneus, and show continuous growth in culture of both the microalga and the virus. Evolution experiments through single cell bottlenecks demonstrate that, in the absence of the virus, susceptible cells evolve from one ancestral resistant single cell, and vice-versa; that is that resistant cells evolve from one ancestral susceptible cell. This provides evidence that the observed sustained viral production is the consequence of a minority of virus-susceptible cells. The emergence of these cells is explained by low-level phase switching between virus-resistant and virus-susceptible phenotypes, akin to a bet hedging strategy. Whole genome sequencing and analysis of the ~14 Mb microalga and the ~200 kb virus points towards ancient speciation of the microalga within the Ostreococcus species complex and frequent gene exchanges between prasinoviruses infecting Ostreococcus species. Re-sequencing of one susceptible strain demonstrated that the phase switch involved a large 60 Kb deletion of one chromosome. This chromosome is an outlier chromosome compared to the streamlined, gene dense, GC-rich standard chromosomes, as it contains many repeats and few orthologous genes. While this chromosome has been described in three different genera, its size increments have been previously associated to antiviral immunity and resistance in another species from the same genus. Mathematical modelling of this mechanism predicts microalga-virus population dynamics consistent with the observation of continuous growth of both virus and microalga. Altogether, our results suggest a previously overlooked strategy in phytoplankton-virus interactions.

evolutionary biology↗

Continuous gene flow contributes to low global species abundance and distribution of a marine model diatom

Diatoms emerged in the Mesozoic period and presently constitute one of the main primary producers in the worlds ocean and are of a major economic importance. In the current study, using whole genome sequencing of ten accessions of the model diatom Phaeodactylum tricornutum, sampled at broad geospatial and temporal scales, we draw a comprehensive landscape of the genomic diversity within the species. We describe strong genetic subdivisions of the accessions into four genetic clades (A-D) with constituent populations of each clade possessing a conserved genetic and functional makeup, likely a consequence of the limited dispersal of P. tricornutum in the open ocean. We further suggest dominance of asexual reproduction across all the populations, as implied by high linkage disequilibrium. Finally, we show limited yet compelling signatures of genetic and functional convergence inducing changes in the selection pressure on many genes and metabolic pathways. We propose these findings to have significant implications for understanding the genetic structure of diatom populations in nature and provide a framework to assess the genomic underpinnings of their ecological success and impact on aquatic ecosystems where they play a major role. Our work provides valuable resources for functional genomics and for exploiting the biotechnological potential of this model diatom species.

genomics↗