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Vyverman, W.

Publications and source records attributed to Vyverman, W..

10 recordsLinked to original sources

A Myb-dominated gene regulatory network universally controls sexual cell fate transitions in diatoms

Diatoms are the foundation of aquatic food webs and contribute about 40% of the total marine primary productivity. Yet, the regulation of their complex size-dependent life cycles remains obscure. Here, we leveraged single-cell transcriptomics and transgenic reporter lines to uncover the molecular mechanisms behind partner recognition, nuclear fusion, and the remarkable 15-fold size expansion of auxospores. Gene regulatory network inference revealed that the irreversible commitment to differentiate into gametes is controlled by Myb transcription factors, whose specific activity in the global ocean underscores their significance for ploidy transitions across diatom clades. These findings reinforce microalgae as powerful models to study cell fate transitions and provide a mechanistic framework for the life cycle dynamics that underpin the functioning of aquatic systems worldwide. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=67 SRC="FIGDIR/small/714157v1_ufig1.gif" ALT="Figure 1"> View larger version (32K): org.highwire.dtl.DTLVardef@162f523org.highwire.dtl.DTLVardef@1cbe836org.highwire.dtl.DTLVardef@1fa6c9eorg.highwire.dtl.DTLVardef@1f12217_HPS_FORMAT_FIGEXP M_FIG C_FIG

microbiology↗

Molecular fingerprints of cell size sensing and mating type differentiation in pennate diatoms

O_LIA unique cell size sensing mechanism is at the heart of the life cycle of diatoms. During population growth, cell size decreases until a Sexual Size Threshold (SST) is reached, below which cells become sexually competent. In most pennate diatoms, the two mating types undergo biochemical and behavioral differentiation below the SST, although the molecular pathways underlying their size-dependent maturation remain unknown. C_LIO_LIHere, we developed a method to shorten the generation time of Cylindrotheca closterium through single-cell microsurgery, enabling the transcriptomic comparison of genetically identical large and undifferentiated cells with small, sexually competent cells for six different genotypes. C_LIO_LIWe identified 21 genes upregulated in small cells regardless of their mating type, revealing how cells undergo specific transcriptional reprogramming when passing the SST. Furthermore, we revealed a size-regulated gene cluster with three mating type-specific genes susceptible to sex-inducing pheromones. In addition, comparative transcriptomics confirmed the shared mating type specificity of Mating-type Related Minus 2 homologs in three pennate diatoms, suggesting them to be part of a conserved partner-recognition mechanism. C_LIO_LIThis study sheds light on how diatoms acquire sexual competence in a strictly size-dependent manner, revealing a complex machinery underlying size-dependent maturation, mating behavior, and heterothally in pennate diatoms. C_LI

plant biology↗

Diatom adhesive trail proteins acquired by horizontal gene transfer from bacteria serve as primers for marine biofilm formation

O_LIBiofilm-forming benthic diatoms are key primary producers in coastal habitats, where they frequently dominate sunlit submerged and intertidal substrata. The development of a unique form of gliding motility in raphid diatoms was a key molecular adaptation that contributed to their evolutionary success. Gliding motility is hypothesized to be driven by an intracellular actin-myosin motor and requires the secretion of polysaccharide- and protein-based adhesive materials. To date, the structure-function correlation between diatom adhesives utilized for gliding and their relationship to the extracellular matrix that constitutes the diatom biofilm is unknown. C_LIO_LIProteomics analysis of the adhesive material from Craspedostauros australis revealed eight novel, diatom-specific proteins. Four of them constitute a new family of proteins, named Trailins, which contain an enigmatic domain termed Choice-of-Anchor-A (CAA). Immunostaining demonstrated that Trailins are only present in the adhesive trails required to generate traction on native substrata, but are absent from the extracellular matrix of biofilms. Phylogenetic analysis and Protein 3D structure prediction suggests that the CAA-domains in Trailins were obtained from bacteria by horizontal gene transfer, and exhibit a striking structural similarity to ice-binding proteins. C_LIO_LIOur work advances the understanding of the molecular basis for diatom underwater adhesion and biofilm formation providing evidence that there is a molecular switch between proteins required for initial surface colonization and those required for 3D biofilm matrix formation. C_LI

plant biology↗

Novel diversity of polar Cyanobacteria revealed by genome-resolved metagenomics

Benthic microbial mats dominated by Cyanobacteria are important features of polar lakes. Although culture-independent studies have provided important insights into their diversity, only a handful of genomes of polar Cyanobacteria have been sequenced to date. Here, we applied a genome-resolved metagenomics approach to data obtained from Arctic, sub-Antarctic, and Antarctic microbial mats. We recovered 22 unique metagenome-assembled genomes (MAGs) of Cyanobacteria, most of which are only distantly related to genomes that have been sequenced so far. These include i) lineages that are common in polar microbial mats such as the filamentous taxa Pseudanabaena, Leptolyngbya, Microcoleus/Tychonema, and Phormidium; ii) the less common taxa Crinalium and Chamaesiphon; iii) an enigmatic Chroococcales lineage only distantly related to Microcystis; and iv) an early branching lineage in the order Gloeobacterales that is almost exclusively restricted to the cold biosphere, for which we propose the name Candidatus Sivonenia alaskensis. Our results show that genome-resolved metagenomics is a powerful tool for expanding our understanding of the diversity of Cyanobacteria, especially in understudied remote and extreme environments. Data summaryThe sequencing data generated in this study have been submitted to the European Nucleotide Archive (ENA) under the BioProject PRJEB59431. Individual accession numbers for raw reads and genomic bins are listed in Table S1 and Table S3, respectively. Genomic bins can also be downloaded from doi.org/10.6084/m9.figshare.22003967. The commands used throughout this study are available in github.com/igorspp/polar-cyanobacteria-MAGs. Impact statementCyanobacteria are photosynthetic microorganisms that play important roles in polar lacustrine ecosystems. Many Cyanobacteria are difficult to grow in the laboratory, particularly in isolation from other organisms, which makes it challenging to sequence their genomes. As such, considerably fewer genomes of Cyanobacteria have been sequenced so far compared to other bacteria. In this study, we used a metagenomics approach to recover novel genomes of Cyanobacteria from Arctic and Antarctic microbial mats without the need to isolate the organisms. The community DNA was extracted and sequenced, and the genomes of individual populations were separated using bioinformatics tools. We recovered 22 different genomes of Cyanobacteria, many of which have not been sequenced before. We describe in more detail an interesting lineage of ancestral Cyanobacteria in the order Gloeobacterales, for which we propose the name Candidatus Sivonenia alaskensis. Our study shows that genome-resolved metagenomics is a valuable approach for obtaining novel genomes of Cyanobacteria, which are needed to improve our understanding of life in the polar regions and the planet at large.

microbiology↗

More than just hitchhikers: a survey of bacterial communities associated with diatoms originating from marine reptiles

Diatoms and bacteria are known for being the first colonizers of submerged surfaces including the skin of marine reptiles. Sea turtle carapace and skin harbour diverse prokaryotic and eukaryotic microbial taxa, including several epizoic diatoms. However, the importance of diatom-bacteria associations is hardly investigated in biofilms associated with animal hosts. This study provides a detailed inventory of diatoms, bacteria, and diatom-associated bacteria originating from several loggerhead sea turtles using a combination of metabarcoding and culturing approaches. Carapace and skin samples rbcL and 16S rRNA amplicon sequencing showed a high diversity of diatoms and bacteria, respectively. Cultures of putative epizoic and non-epizoic diatom strains contained from 18 to 101 bacterial amplicon sequence variants (ASVs) and their bacterial assemblages strongly reflected those of their source host. Diatom strains allowed for enrichment and isolation of rare-in-source bacterial families such as Marinobacteraceae, Alteromonadaceae, and Alcanivoracaceae. When accounting for phylogenetic relationships between bacterial ASVs, we observed related diatom genera might retain related microbial taxa in culture, regardless of the source environment. These data provide deeper insights into several levels of sea turtle epizoic diatom and bacterial communities, and reveal the potential of epizoic biofilms as a source of novel microbes and possibly important diatom-bacteria associations.

microbiology↗

Diurnal transcript profiling of the diatom Seminavisrobusta reveals adaptations to a benthic lifestyle

1Coastal regions contribute an estimated 20% of annual gross primary production in the oceans, despite occupying only 0.03% of their surface area. Diatoms frequently dominate coastal sediments, where they experience large variations in light regime resulting from the interplay of diurnal and tidal cycles. Here, we report on an extensive diurnal transcript profiling experiment of the motile benthic diatom Seminavis robusta. Nearly 90% (23,328) of expressed protein-coding genes and 66.9% (1124) of expressed long intergenic non-coding RNAs (lincRNAs) showed significant expression oscillations and are predominantly phasing at night with a periodicity of 24h. Phylostratigraphic analysis found that rhythmic genes are enriched in deeply conserved genes, while diatom-specific genes are predominantly associated with midnight expression. Integration of genetic and physiological cell cycle markers with silica depletion data revealed potential new silica cell wall associated gene families specific to diatoms. Additionally, we observed 1752 genes with a remarkable semidiurnal (12-h) periodicity, while the expansion of putative circadian transcription factors may reflect adaptations to cope with highly unpredictable external conditions. Taken together, our results provide new insights into the adaptations of diatoms to the benthic environment and serve as a valuable resource for diurnal regulation in photosynthetic eukaryotes. O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

systems biology↗

Mitotic interhomolog recombination drives genomic diversity in diatoms

Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific variability in natural populations. However, the process generating such diversity is unknown. Here we estimated the variability within a natural diatom population and subsequently mapped the genomic changes arising within cultures clonally propagated from single diatom cells. We demonstrate that genome rearrangements and mitotic recombination between homologous chromosomes underlie clonal variability, resulting in haplotype diversity accompanied by the appearance of novel protein variants and loss of heterozygosity resulting in the fixation of alleles. The frequency of interhomolog mitotic recombination exceeds 4 out of 100 cell divisions and increases under environmental stress. We propose that this plastic response in the interhomolog mitotic recombination rate increases the evolutionary potential of diatoms, contributing to their ecological success. One Sentence SummaryRecombination between homologous chromosomes in diatom vegetative cells leads to extensive genomic diversity in clonal populations.

genomics↗

Mating type specific transcriptomic response to sex inducing pheromone in the pennate diatom Seminavis robusta

Sexual reproduction is a fundamental phase in the life cycle of most diatoms. Despite its role as a source of genetic variation, it is rarely reported in nature and its molecular foundations remain largely unknown. Here, we integrate independent transcriptomic datasets, in order to prioritize genes responding to sex inducing pheromones (SIPs) in the pennate diatom Seminavis robusta. We observe marked gene expression changes associated with SIP treatment in both mating types, including an inhibition of S-phase progression, chloroplast division, mitosis and cell wall formation. Meanwhile, meiotic genes are upregulated in response to SIP, including a sexually induced diatom specific cyclin (dsCyc). Our data further suggest an important role for reactive oxygen species, energy metabolism and cGMP signaling during the early stages of sexual reproduction. In addition, we identify several genes with a mating type specific response to SIP, and link their expression pattern with physiological responses such as the production of the attraction pheromone diproline and mate-searching behaviour in MT+. Combined, our results provide a model for early sexual reproduction in pennate diatoms and significantly expand the suite of target genes to detect sexual reproduction events in natural diatom populations.

molecular biology↗

The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms

Benthic diatoms are the main primary producers in shallow freshwater and coastal environments, fulfilling important ecological functions such as nutrient cycling and sediment stabilization. However, little is known about their evolutionary adaptations to these highly structured but heterogeneous environments. Here, we report a reference genome for the marine biofilm-forming diatom Seminavis robusta, showing that gene family expansions are responsible for a quarter of all 36,254 protein-coding genes. Tandem duplications play a key role in extending the repertoire of specific gene functions, including light and oxygen sensing, which are probably central for its adaptation to benthic habitats. Genes differentially expressed during interactions with bacteria are strongly conserved in other benthic diatoms while many species-specific genes are strongly upregulated during sexual reproduction. Combined with re-sequencing data from 48 strains, our results offer new insights on the genetic diversity and gene functions in benthic diatoms.

bioinformatics↗

Optimal foraging of benthic diatoms evolving novel movement behaviours

Adaptive locomotion of living organisms contributes to their competitive abilities and helps maintain their fitness in diverse environments. To date, however, our understanding of searching behavior and its ultimate cause remains poorly understood in ecology and biology. Here, we investigate motion patterns of biofilm-inhabiting marine raphid diatom Navicula arenaria var. rostellata in two-dimensional space. We report that individual Navicula cells display a "circular run-and-reversal" movement behavior at different concentrations of dissolved silicic acid (dSi). We show that gliding motions of cells can be predicted accurately with a universal Langevin model. Our experimental results are consistent with an optimal foraging strategy and a maximized diffusivity of the theoretical outcomes in which both circular-run and reversal behaviors are important ingredients. Our theoretical results suggest that the evolving movement behaviors of diatoms may be driven by optimization of searching behavioral strategy, and predicted behavioral parameters coincide with the experimental observations. These optimized movement behaviors are an evolutionarily stable strategy to cope with environmental complexity. ONE SENTENCE SUMMARYNovel experiments and modelling reveal that raphid diatoms can actively exploit resources in complex environments by adjusting their movement behavior.

ecology↗