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Biology subjects

Nakov, T.

Publications and source records attributed to Nakov, T..

7 recordsLinked to original sources

Local adaptation of a marine diatom is governed by genome-wide changes in diverse metabolic processes

Marine phytoplankton play essential roles in global primary production and biogeochemical cycles. Yet, the evolutionary genetic underpinnings of phytoplankton adaptation to complex marine and coastal environments, where many environmental variables fluctuate and interact, remain unclear. We combined population genomics data with experimental transcriptomics to investigate the genomic basis underlying a natural evolutionary experiment that has played out over the past 8,000 years in one of the worlds largest brackish water bodies: the colonization of the Baltic Sea by the marine diatom Skeletonema marinoi. To this end, we used a novel approach for protist population genomics, combining target capture of the entire nuclear genome with pooled sequencing, and showed that the method performs well on both cultures and single cells. Genotype-environment association analyses identified >3,000 genes with signals of selection in response to major environmental gradients in the Baltic Sea, which apart from salinity, include marked differences in temperature and nutrient availability. Locally adapted genes were related to diverse metabolic processes, including signal transduction, cell cycle, DNA methylation, and maintenance of homeostasis. The locally adapted genes showed significant overlap with salinity-responsive genes identified in a laboratory common garden experiment, suggesting the Baltic salinity gradient is a major factor driving local adaptation of S. marinoi. Altogether, our data show that local adaptation of phytoplankton to complex coastal environments, which are characterized by a multitude of environmental gradients, is driven by intricate changes in diverse metabolic pathways and functions.

microbiology↗

Genotype-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline

The salinity gradient separating marine and freshwater environments represents a major ecological divide for microbiota, yet the mechanisms by which marine microbes have adapted to and ultimately diversified in freshwater environments are poorly understood. Here, we take advantage of a natural evolutionary experiment: the colonization of the brackish Baltic Sea by the ancestrally marine diatom Skeletonema marinoi. To understand how diatoms respond to low salinity, we characterized transcriptomic responses of S. marinoi grown in a common garden. Our experiment included eight genotypes from source populations spanning the Baltic Sea salinity cline. Changes in gene expression revealed a shared response to salinity across genotypes, where low salinities induced profound changes in cellular metabolism, including upregulation of carbon fixation and storage compound biosynthesis, and increased nutrient demand and oxidative stress. Nevertheless, the genotype effect overshadowed the salinity effect, as genotypes differed significantly in their response, both in the magnitude and direction of gene expression. Intraspecific differences included regulation of transcription and translation, nitrogen metabolism, cell signaling, and aerobic respiration. The high degree of intraspecific variation in gene expression observed here highlights an important but often overlooked source of biological variation associated with how diatoms respond and adapt to environmental change.

microbiology↗

Hot and sick: impacts of warming and oomycete parasite infection on endemic dominant zooplankter of Lake Baikal.

Climate warming impacts ecosystems through multiple interacting pathways, including via direct thermal responses of individual taxa and the combined responses of closely interacting species. In this study we examined how warming and infection by an oomycete parasite affect the dominant zooplankter of Russias Lake Baikal, the endemic cold-adapted stenotherm Epischura baikalensis (Copepoda). We used a combination of laboratory experiments, long-term monitoring data and population modeling. Experiments showed large thermal mismatch between host and parasite, with strong negative effects of warm temperatures on E. baikalensis survival and reproduction and a negative synergistic effect of Saprolegnia infection. However, Saprolegnia infection had an unexpected positive effect on E. baikalensis reproductive output, which may be consistent with fecundity compensation by infected females. Long-term monitoring data showed that Saprolegnia infections were most common during the warmest periods of the year and that infected individuals tended to accumulate in deep water. Population models, parameterized with experimental and literature data, correctly predicted the timing of Saprolegnia epizootics, but overestimated the negative effect of warming on E.baikalensis populations. Models suggest that diel vertical migration may allow E. baikalensis to escape the negative effects of increasing temperatures and parasitism and enable E. baikalensis to persist as Lake Baikal warms. Our results contribute to understanding of how multiple interacting stressors affect warming pelagic ecosystems of cold lakes and oceans and show that the population-level consequences of thermal mismatch between hosts and parasites can vary seasonally, interannual and spatially.

ecology↗

Freshwater diatoms diversify faster than marine in both planktonic and benthic habitats

Many clades that span the marine-freshwater boundary are disproportionately more diverse in the younger, shorter-lived, and scarcer freshwater environments than they are in the marine realm. This disparity is thought to be related to differences in diversification rates between marine and freshwater lineages. However, marine and freshwaters are not ecologically homogeneous, so the study of diversification across the salinity divide should also account for other potentially interacting variables. In diatoms, freshwater and substrate-associated (benthic) lineages are several-fold more diverse than their marine and suspended (planktonic) counterparts. These imbalances provide an excellent system to understand whether these variables interact with diversification. Using multistate hidden-state speciation and extinction models we found that freshwater lineages diversify faster than marine lineages regardless of whether they inhabit the plankton or the benthos. Freshwater lineages also had higher turnover rates (speciation + extinction), suggesting that habitat transitions impact speciation and extinction rates jointly. The plankton-benthos contrast was also consistent with state-dependent diversification, but with modest differences in diversification and turnover rates. Asymmetric, and bidirectional transitions rejected hypotheses about the plankton and freshwaters as absorbing, inescapable habitats. Our results further suggest that the high turnover rate of freshwater diatoms is related to high turnover of freshwater systems themselves.

evolutionary biology↗

A single loss of photosynthesis in diatoms

Loss of photosynthesis is a common and often repeated trajectory in nearly all major groups of photosynthetic eukaryotes. One small subset of apochloritic diatoms in the genus Nitzschia have lost their ability to photosynthesize and require extracellular carbon for growth. Similar to other secondarily nonphotosynthetic taxa, apochloritic diatoms maintain colorless plastids with highly reduced plastid genomes. Although the narrow taxonomic breadth of apochloritic diatoms suggests a single loss of photosynthesis in the common ancestor of these species, previous phylogenetic analyses suggested that photosynthesis was lost multiple times. We sequenced additional phylogenetic markers from the nuclear and mitochondrial genomes for a larger set of taxa and found that the best trees for datasets representing all three genetic compartments provided low to moderate support for monophyly of apochloritic Nitzschia, consistent with a single loss of photosynthesis in diatoms. We sequenced the plastid genome of one apochloritic species and found that it was highly similar in all respects to the plastid genome of another apochloritic Nitzschia species, indicating that streamlining of the plastid genome had completed prior to the split of these two species. Finally, it is increasingly clear that some locales host relatively large numbers apochloritic Nitzschia species that span the phylogenetic diversity of the group, indicating that these species co-exist because of resource abundance or resource partitioning in ecologically favorable habitats. A better understanding of the phylogeny and ecology of this group, together with emerging genomic resources, will help identify the factors that have driven and maintained the loss of photosynthesis in this group, a rare event in diatoms.

evolutionary biology↗

Phylogenomics reveals an extensive history of genome duplication in diatoms (Bacillariophyta)

Premise of the studyDiatoms are one of the most species-rich lineages of microbial eukaryotes. Similarities in clade age, species richness, and contributions to primary production motivate comparisons to flowering plants, whose genomes have been inordinately shaped by whole genome duplication (WGD). These events that have been linked to speciation and increased rates of lineage diversification, identifying WGDs as a principal driver of angiosperm evolution. We synthesized a relatively large but scattered body of evidence that, taken together, suggests that polyploidy may be common in diatoms.\n\nMethodsWe used data from gene counts, gene trees, and patterns of synonymous divergence to carry out the first large-scale phylogenomic analysis of genome-scale duplication histories for a phylogenetically diverse set of 37 diatom taxa.\n\nKey resultsSeveral methods identified WGD events of varying age across diatoms, though determining the exact number and placement of events and, more broadly, inferences of WGD at all, were greatly impacted by gene-tree uncertainty. Gene-tree reconciliations supported allopolyploidy as the predominant mode of polyploid formation, with particularly strong evidence for ancient allopolyploid events in the thalassiosiroid and pennate diatom clades.\n\nConclusionsWhole genome duplication appears to have been an important driver of genome evolution in diatoms. Denser taxon sampling will better pinpoint the timing of WGDs and likely reveal many more of them. We outline potential challenges in reconstructing paleopolyploid events in diatoms that, together with these results, offer a framework for understanding the evolutionary roles of genome duplication in a group that likely harbors substantial genomic diversity.

evolutionary biology↗

Insights into global planktonic diatom diversity:Comparisons between phylogenetically meaningful unitsthat account for time

Metabarcoding has offered unprecedented insights into microbial diversity. In many studies, short DNA sequences are binned into consecutively higher Linnaean ranks, and ranked groups (e.g., genera) are the units of biodiversity analyses. These analyses assume that Linnaean ranks are biologically meaningful and that identically ranked groups are comparable. We used a meta-barcode dataset for marine planktonic diatoms to illustrate the limits of this approach. We found that the 20 most abundant marine planktonic diatom genera ranged in age from 4 to 134 million years, indicating the non-equivalence of genera because some had more time to diversify than others. Still, species richness was only weakly correlated with genus age, highlighting variation in rates of speciation and/or extinction. Taxonomic classifications often do not reflect phylogeny, so genus-level analyses can include phylogenetically nested genera, further confounding rank-based analyses. These results underscore the indispensable role of phylogeny in understanding patterns of microbial diversity.

evolutionary biology↗