Shruti Malviya

Eukaryotic plankton diversity in the sunlit ocean

Marine plankton support global biological and geochemical processes. Surveys of their biodiversity have hitherto been geographically restricted and have not accounted for the full range of plankton size. We assessed eukaryotic diversity from 334 size-fractionated photic-zone plankton communities collected across tropical and temperate oceans during the circumglobal Tara Oceans expedition. We analyzed 18S ribosomal DNA sequences across the intermediate plankton-size spectrum from the smallest unicellular eukaryotes (protists, >0.8 micrometers) to small animals of a few millimeters. Eukaryotic ribosomal diversity saturated at ~150,000 operational taxonomic units, about one-third of which could not be assigned to known eukaryotic groups. Diversity emerged at all taxonomic levels, both within the groups comprising the ~11,200 cataloged morphospecies of eukaryotic plankton and among twice as many other deep-branching lineages of unappreciated importance in plankton ecology studies. Most eukaryotic plankton biodiversity belonged to heterotrophic protistan groups, particularly those known to be parasites or symbiotic hosts.

Plankton networks driving carbon export in the oligotrophic ocean.

The biological carbon pump is the process by which CO2 is transformed to organic carbon via photosynthesis, exported through sinking particles, and finally sequestered in the deep ocean. While the intensity of the pump correlates with plankton community composition, the underlying ecosystem structure driving the process remains largely uncharacterized. Here we use environmental and metagenomic data gathered during the Tara Oceans expedition to improve our understanding of carbon export in the oligotrophic ocean. We show that specific plankton communities, from the surface and deep chlorophyll maximum, correlate with carbon export at 150 m and highlight unexpected taxa such as Radiolaria and alveolate parasites, as well as Synechococcus and their phages, as lineages most strongly associated with carbon export in the subtropical, nutrient-depleted, oligotrophic ocean. Additionally, we show that the relative abundance of a few bacterial and viral genes can predict a significant fraction of the variability in carbon export in these regions.

Insights into global diatom distribution and diversity in the world’s ocean

Significance Diatoms, considered one of the most diverse and ecologically important phytoplanktonic groups, contribute around 20% of global primary productivity. They are particularly abundant in nutrient-rich coastal ecosystems and at high latitudes. Here, we have explored the dataset generated by Tara Oceans from a wide range of oceanic regions to characterize diatom diversity patterns on a global scale. We confirm the dominance of diatoms as a major photosynthetic group and identify the most widespread and diverse genera. We also provide a new estimate of marine planktonic diatom diversity and a global view of their distribution in the world’s ocean. 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.

Environmental characteristics of Agulhas rings affect interocean plankton transport

Agulhas rings provide the principal route for ocean waters to circulate from the Indo-Pacific to the Atlantic basin. Their influence on global ocean circulation is well known, but their role in plankton transport is largely unexplored. We show that, although the coarse taxonomic structure of plankton communities is continuous across the Agulhas choke point, South Atlantic plankton diversity is altered compared with Indian Ocean source populations. Modeling and in situ sampling of a young Agulhas ring indicate that strong vertical mixing drives complex nitrogen cycling, shaping community metabolism and biogeochemical signatures as the ring and associated plankton transit westward. The peculiar local environment inside Agulhas rings may provide a selective mechanism contributing to the limited dispersal of Indian Ocean plankton populations into the Atlantic.

Diatom Phytochromes Reveal the Existence of Far-Red-Light-Based Sensing in the Ocean

Diatom phytochromes (DPH) display high sensitivity to far-red light in the far-red poor aquatic environment, opening new perspectives on signaling mechanisms in the marine realm. The absorption of visible light in aquatic environments has led to the common assumption that aquatic organisms sense and adapt to penetrative blue/green light wavelengths but show little or no response to the more attenuated red/far-red wavelengths. Here, we show that two marine diatom species, Phaeodactylum tricornutum and Thalassiosira pseudonana, possess a bona fide red/far-red light sensing phytochrome (DPH) that uses biliverdin as a chromophore and displays accentuated red-shifted absorbance peaks compared with other characterized plant and algal phytochromes. Exposure to both red and far-red light causes changes in gene expression in P. tricornutum, and the responses to far-red light disappear in DPH knockout cells, demonstrating that P. tricornutum DPH mediates far-red light signaling. The identification of DPH genes in diverse diatom species widely distributed along the water column further emphasizes the ecological significance of far-red light sensing, raising questions about the sources of far-red light. Our analyses indicate that, although far-red wavelengths from sunlight are only detectable at the ocean surface, chlorophyll fluorescence and Raman scattering can generate red/far-red photons in deeper layers. This study opens up novel perspectives on phytochrome-mediated far-red light signaling in the ocean and on the light sensing and adaptive capabilities of marine phototrophs.

Nanoplanktonic diatoms are globally overlooked but play a role in spring blooms and carbon export

Diatoms are one of the major primary producers in the ocean, responsible annually for ~20% of photosynthetically fixed CO2 on Earth. In oceanic models, they are typically represented as large (>20 µm) microphytoplankton. However, many diatoms belong to the nanophytoplankton (2–20 µm) and a few species even overlap with the picoplanktonic size-class (<2 µm). Due to their minute size and difficulty of detection they are poorly characterized. Here we describe a massive spring bloom of the smallest known diatom (Minidiscus) in the northwestern Mediterranean Sea. Analysis of Tara Oceans data, together with literature review, reveal a general oversight of the significance of these small diatoms at the global scale. We further evidence that they can reach the seafloor at high sinking rates, implying the need to revise our classical binary vision of pico- and nanoplanktonic cells fueling the microbial loop, while only microphytoplankton sustain secondary trophic levels and carbon export.Diatoms are major oceanic primary producers, but some species belonging to the nano- and even picoplankton size are poorly characterized. Here the authors describe a massive spring bloom of the smallest known diatom in the Mediterranean Sea and reveal their general oversight at the global scale.

Ubiquitous abundance distribution of non-dominant plankton across the global ocean

Marine plankton populate 70% of Earth’s surface, providing the energy that fuels ocean food webs and contributing to global biogeochemical cycles. Plankton communities are extremely diverse and geographically variable, and are overwhelmingly composed of low-abundance species. The role of this rare biosphere and its ecological underpinnings are however still unclear. Here, we analyse the extensive dataset generated by the Tara Oceans expedition for marine microbial eukaryotes (protists) and use an adaptive algorithm to explore how metabarcoding-based abundance distributions vary across plankton communities in the global ocean. We show that the decay in abundance of non-dominant operational taxonomic units, which comprise over 99% of local richness, is commonly governed by a power-law. Despite the high spatial turnover in species composition, the power-law exponent varies by less than 10% across locations and shows no biogeographical signature, but is weakly modulated by cell size. Such striking regularity suggests that the assembly of plankton communities in the dynamic and highly variable ocean environment is governed by large-scale ubiquitous processes. Understanding their origin and impact on plankton ecology will be important for evaluating the resilience of marine biodiversity in a changing ocean.Analysing data from the Tara Oceans expedition, the authors show that the abundance distributions of non-dominant marine microbial eukaryotes are characterized by a power-law decay, the exponent of which varies by less than 10% across the global ocean.

Neobodonids are dominant kinetoplastids in the global ocean: Kinetoplastids in the oceans

Kinetoplastid flagellates comprise basal mostly free-living bodonids and derived obligatory parasitic trypanosomatids, which belong to the best-studied protists. Due to their omnipresence in aquatic environments and soil, the bodonids are of ecological significance. Here, we present the first global survey of marine kinetoplastids and compare it with the strikingly different patterns of abundance and diversity in their sister clade, the diplonemids. Based on analysis of 18S rDNA V9 ribotypes obtained from 124 sites sampled during the Tara Oceans expedition, our results show generally low to moderate abundance and diversity of planktonic kinetoplastids. Although we have identified all major kinetoplastid lineages, 98% of kinetoplastid reads are represented by neobodonids, namely specimens of the Neobodo and Rhynchomonas genera, which make up 59% and 18% of all reads, respectively. Most kinetoplastids have small cell size (0.8-5 µm) and tend to be more abundant in the mesopelagic as compared to the euphotic zone. Some of the most abundant operational taxonomic units have distinct geographical distributions, and three novel putatively parasitic neobodonids were identified, along with their potential hosts.

Clade-specific diversification dynamics of marine diatoms since the Jurassic

Diatoms are one of the most abundant and diverse groups of phytoplankton and play a major role in marine ecosystems and the Earth’s biogeochemical cycles. Here we combine DNA metabarcoding data from the Tara Oceans expedition with palaeoenvironmental data and phylogenetic models of diversification to analyse the diversity dynamics of marine diatoms. We reveal a primary effect of variation in carbon dioxide partial pressure (pCO2) on early diatom diversification, followed by a major burst of diversification in the late Eocene epoch, after which diversification is chiefly affected by sea level, an influx of silica availability and competition with other planktonic groups. Our results demonstrate a remarkable heterogeneity of diversification dynamics across diatoms and suggest that a changing climate will favour some clades at the expense of others.DNA metabarcoding data from the Tara Oceans expedition are combined with palaeoenvironmental data and phylogenetic models of diversification to analyse the diversity dynamics of marine diatoms since the Jurassic period.