The last decade has witnessed outstanding progress in sequencing the genomes of photosynthetic eukaryotes, from major cereal crops to single celled marine phytoplankton. For the algae, we now have ...whole genome sequences from green, red, and brown representatives, and multiple efforts based on comparative and functional genomics approaches have provided information about the unicellular origins of higher plants, and about the evolution of photosynthetic life in general. Here we present some of the highlights from such studies, including the endosymbiotic origins of photosynthetic protists and their positioning with respect to plants and animals, the evolution of multicellularity in photosynthetic lineages, the role of sex in unicellular algae, and the potential relevance of epigenetic processes in contributing to the adaptation of algae to their environment.
Full text
Available for:
BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
Diatoms (Bacillariophyta) constitute one of the most diverse and ecologically important groups of phytoplankton. They are considered to be particularly important in nutrient-rich coastal ecosystems ...and at high latitudes, but considerably less so in the oligotrophic open ocean. The Tara Oceans circumnavigation collected samples from a wide range of oceanic regions using a standardized sampling procedure. Here, a total of ∼12 million diatom V9-18S ribosomal DNA (rDNA) ribotypes, derived from 293 size-fractionated plankton communities collected at 46 sampling sites across the global ocean euphotic zone, have been analyzed to explore diatom global diversity and community composition. We provide a new estimate of diversity of marine planktonic diatoms at 4,748 operational taxonomic units (OTUs). Based on the total assigned ribotypes, Chaetoceros was the most abundant and diverse genus, followed by Fragilariopsis, Thalassiosira, and Corethron. We found only a few cosmopolitan ribotypes displaying an even distribution across stations and high abundance, many of which could not be assigned with confidence to any known genus. Three distinct communities from South Pacific, Mediterranean, and Southern Ocean waters were identified that share a substantial percentage of ribotypes within them. Sudden drops in diversity were observed at Cape Agulhas, which separates the Indian and Atlantic Oceans, and across the Drake Passage between the Atlantic and Southern Oceans, indicating the importance of these ocean circulation choke points in constraining diatom distribution and diversity. We also observed high diatom diversity in the open ocean, suggesting that diatoms may be more relevant in these oceanic systems than generally considered.
Full text
Available for:
BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly ...understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros, the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data.
Full text
Available for:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The ecological prominence of diatoms in the ocean environment largely results from their superior competitive ability for dissolved nitrate (NO3
−). To investigate the cellular and genetic basis of ...diatom NO3
− assimilation, we generated a knockout in the nitrate reductase gene (NR-KO) of the model pennate diatom Phaeodactylum tricornutum. In NR-KO cells, N-assimilation was abolished although NO3
− transport remained intact. Unassimilated NO3
− accumulated in NR-KO cells, resulting in swelling and associated changes in biochemical composition and physiology. Elevated expression of genes encoding putative vacuolar NO3
− chloride channel transporters plus electron micrographs indicating enlarged vacuoles suggested vacuolar storage of NO3
−. Triacylglycerol concentrations in the NR-KO cells increased immediately following the addition of NO3
−, and these increases coincided with elevated gene expression of key triacylglycerol biosynthesis components. Simultaneously, induction of transcripts encoding proteins involved in thylakoid membrane lipid recycling suggested more abrupt repartitioning of carbon resources in NR-KO cells compared with the wild type. Conversely, ribosomal structure and photosystem genes were immediately deactivated in NR-KO cells following NO3
− addition, followed within hours by deactivation of genes encoding enzymes for chlorophyll biosynthesis and carbon fixation and metabolism. N-assimilation pathway genes respond uniquely, apparently induced simultaneously by both NO3
− replete and deplete conditions.
Full text
Available for:
BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Diatoms are a major component of phytoplankton, believed to be responsible for around 20% of the annual primary production on Earth. As abundant and ubiquitous organisms, they are known to establish ...biotic interactions with many other members of plankton. Through analyses of cooccurrence networks derived from the
Oceans expedition that take into account both biotic and abiotic factors in shaping the spatial distributions of species, we show that only 13% of diatom pairwise associations are driven by environmental conditions; the vast majority are independent of abiotic factors. In contrast to most other plankton groups, on a global scale, diatoms display a much higher proportion of negative correlations with other organisms, particularly toward potential predators and parasites, suggesting that their biogeography is constrained by top-down pressure. Genus-level analyses indicate that abundant diatoms are not necessarily the most connected and that species-specific abundance distribution patterns lead to negative associations with other organisms. In order to move forward in the biological interpretation of cooccurrence networks, an open-access extensive literature survey of diatom biotic interactions was compiled, of which 18.5% were recovered in the computed network. This result reveals the extent of what likely remains to be discovered in the field of planktonic biotic interactions, even for one of the best-known organismal groups.
Diatoms are key phytoplankton in the modern ocean that are involved in numerous biotic interactions, ranging from symbiosis to predation and viral infection, which have considerable effects on global biogeochemical cycles. However, despite recent large-scale studies of plankton, we are still lacking a comprehensive picture of the diversity of diatom biotic interactions in the marine microbial community. Through the ecological interpretation of both inferred microbial association networks and available knowledge on diatom interactions compiled in an open-access database, we propose an ecosystems approach for exploring diatom interactions in the ocean.
Phytoplankton in the Tara Ocean Pierella Karlusich, Juan José; Ibarbalz, Federico M; Bowler, Chris
Annual review of marine science,
01/2020, Volume:
12, Issue:
1
Journal Article
Peer reviewed
Open access
Photosynthesis evolved in the ocean more than 2 billion years ago and is now performed by a wide range of evolutionarily distinct organisms, including both prokaryotes and eukaryotes. Our ...appreciation of their abundance, distributions, and contributions to primary production in the ocean has been increasing since they were first discovered in the seventeenth century and has now been enhanced by data emerging from the
Tara
Oceans project, which performed a comprehensive worldwide sampling of plankton in the upper layers of the ocean between 2009 and 2013. Largely using recent data from
Tara
Oceans, here we review the geographic distributions of phytoplankton in the global ocean and their diversity, abundance, and standing stock biomass. We also discuss how omics-based information can be incorporated into studies of photosynthesis in the ocean and show the likely importance of mixotrophs and photosymbionts.
Marine diatoms, the most successful photoautotrophs in the ocean, efficiently sequester a significant part of atmospheric CO
to the ocean interior through their participation in the biological carbon ...pump. However, it is poorly understood how marine diatoms fix such a considerable amount of CO
, which is vital information toward modeling their response to future CO
levels. The
Oceans expeditions generated molecular data coupled with
biogeochemical measurements across the main ocean regions, and thus provides a framework to compare diatom genetic and transcriptional flexibility under natural CO
variability. The current study investigates the interlink between the environmental variability of CO
and other physicochemical parameters with the gene and transcript copy numbers of five key enzymes of diatom CO
concentration mechanisms (CCMs): Rubisco activase and carbonic anhydrase (CA) as part of the physical pathway, together with phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme as part of the potential C4 biochemical pathway. Toward this aim, we mined >200 metagenomes and >220 metatranscriptomes generated from samples of the surface layer of 66 globally distributed sampling sites and corresponding to the four main size fractions in which diatoms can be found: 0.8-5 μm, 5-20 μm, 20-180 μm, and 180-2,000 μm. Our analyses revealed that the transcripts for the enzymes of the putative C4 biochemical CCM did not in general display co-occurring profiles. The transcripts for CAs were the most abundant, with an order of magnitude higher values than the other enzymes, thus implying the importance of physical CCMs in diatom natural communities. Among the different classes of this enzyme, the most prevalent was the recently characterized iota class. Consequently, very little information is available from natural diatom assemblages about the distribution of this class. Biogeographic distributions for all the enzymes show different abundance hotspots according to the size fraction, pointing to the influence of cell size and aggregation in CCMs. Environmental correlations showed a complex pattern of responses to CO
levels, total phytoplankton biomass, temperature, and nutrient concentrations. In conclusion, we propose that biophysical CCMs are prevalent in natural diatom communities.
The world’s oceans represent by far the largest biome, with great importance for the global ecosystem 1–4. The vast majority of ocean biomass and biodiversity is composed of microscopic plankton. ...Recent results from the Tara Oceans metabarcoding study revealed that a significant part of the plankton in the upper sunlit layer of the ocean is represented by an understudied group of heterotrophic excavate flagellates called diplonemids 5, 6. We have analyzed the diversity and distribution patterns of diplonemid populations on the extended set of Tara Oceans V9 18S rDNA metabarcodes amplified from 850 size- fractionated plankton communities sampled across 123 globally distributed locations, for the first time also including samples from the mesopelagic zone, which spans the depth from about 200 to 1,000 meters. Diplonemids separate into four major clades, with the vast majority falling into the deep-sea pelagic diplonemid clade. Remarkably, diversity of this clade inferred from metabarcoding data surpasses even that of dinoflagellates, metazoans, and rhizarians, qualifying diplonemids as possibly the most diverse group of marine planktonic eukaryotes. Diplonemids display strong vertical separation between the photic and mesopelagic layers, with the majority of their relative abundance and diversity occurring in deeper waters. Globally, diplonemids display no apparent biogeographic structuring, with a few hyperabundant cosmopolitan operational taxonomic units (OTUs) dominating their communities. Our results suggest that the planktonic diplonemids are among the key heterotrophic players in the largest ecosystem of our biosphere, yet their roles in this ecosystem remain unknown.
•Pelagic diplonemids are the most diverse planktonic eukaryotes in the ocean•They are depth stratified and are more abundant and diverse in the deep ocean•Diplonemids are cosmopolitan, with no clear biogeographic structuring•They may be key players in the ocean ecosystem, yet their role remains unknown
Flegontova et al. present detailed analysis of global diversity and distribution of diplonemids, the most diverse planktonic eukaryotes. They find diplonemids to be virtually ubiquitous but much more abundant and diverse in the deep ocean. The results suggest that they are among the key players of the ocean ecosystem, yet their role remains unknown.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Marine microorganisms form complex communities of interacting organisms that influence central ecosystem functions in the ocean such as primary production and nutrient cycling. Identifying the ...mechanisms controlling their assembly and activities is a major challenge in microbial ecology. Here, we integrated Tara Oceans meta-omics data to predict genome-scale community interactions within prokaryotic assemblages in the euphotic ocean. A global genome-resolved co-activity network revealed a significant number of inter-lineage associations across diverse phylogenetic distances. Identified co-active communities include species displaying smaller genomes but encoding a higher potential for quorum sensing, biofilm formation, and secondary metabolism. Community metabolic modelling reveals a higher potential for interaction within co-active communities and points towards conserved metabolic cross-feedings, in particular of specific amino acids and group B vitamins. Our integrated ecological and metabolic modelling approach suggests that genome streamlining and metabolic auxotrophies may act as joint mechanisms shaping bacterioplankton community assembly in the global ocean surface.
PDF
