Tara Oceans Expedition Research Articles

Global patterns of pelagic dinoflagellate diversity across protist size classes unveiled by metabarcoding.

Dinoflagellates (Alveolata) are one of the ecologically most important groups of modern phytoplankton. Their biological complexity makes assessment of their global diversity and community structure difficult. We used massive V9 18S rDNA sequencing from 106 size-fractionated plankton communities collected across the world's surface oceans during the Tara Oceans expedition (2009-2012) to assess patterns of pelagic dinoflagellate diversity and community structuring over global taxonomic and ecological scales. Our data and analyses suggest that dinoflagellate diversity has been largely underestimated, representing overall ∼ 1/2 of protistan rDNA metabarcode richness assigned at ≥ 90% to a reference sequence in the world's surface oceans. Dinoflagellate metabarcode diversity and abundance display regular patterns across the global scale, with different order-level taxonomic compositions across organismal size fractions. While the pico to nano-planktonic communities are composed of an extreme diversity of metabarcodes assigned to Gymnodiniales or are simply undetermined, most micro-dinoflagellate metabarcodes relate to the well-referenced Gonyaulacales and Peridiniales orders, and a lower abundance and diversity of essentially symbiotic Peridiniales is unveiled in the meso-plankton. Our analyses could help future development of biogeochemical models of pelagic systems integrating the separation of dinoflagellates into functional groups according to plankton size classes.

Global distribution and vertical patterns of a prymnesiophyte-cyanobacteria obligate symbiosis.

A marine symbiosis has been recently discovered between prymnesiophyte species and the unicellular diazotrophic cyanobacterium UCYN-A. At least two different UCYN-A phylotypes exist, the clade UCYN-A1 in symbiosis with an uncultured small prymnesiophyte and the clade UCYN-A2 in symbiosis with the larger Braarudosphaera bigelowii. We targeted the prymnesiophyte-UCYN-A1 symbiosis by double CARD-FISH (catalyzed reporter deposition-fluorescence in situ hybridization) and analyzed its abundance in surface samples from the MALASPINA circumnavigation expedition. Our use of a specific probe for the prymnesiophyte partner allowed us to verify that this algal species virtually always carried the UCYN-A symbiont, indicating that the association was also obligate for the host. The prymnesiophyte-UCYN-A1 symbiosis was detected in all ocean basins, displaying a patchy distribution with abundances (up to 500 cells ml(-1)) that could vary orders of magnitude. Additional vertical profiles taken at the NE Atlantic showed that this symbiosis occupied the upper water column and disappeared towards the Deep Chlorophyll Maximum, where the biomass of the prymnesiophyte assemblage peaked. Moreover, sequences of both prymnesiophyte partners were searched within a large 18S rDNA metabarcoding data set from the Tara-Oceans expedition around the world. This sequence-based analysis supported the patchy distribution of the UCYN-A1 host observed by CARD-FISH and highlighted an unexpected homogeneous distribution (at low relative abundance) of B. bigelowii in the open ocean. Our results demonstrate that partners are always in symbiosis in nature and show contrasted ecological patterns of the two related lineages.

Regional ocean-colour chlorophyll algorithms for the Red Sea

The Red Sea is a semi-enclosed tropical marine ecosystem that stretches from the Gulf of Suez and Gulf of Aqaba in the north, to the Gulf of Aden in the south. Despite its ecological and economic importance, its biological environment is relatively unexplored. Satellite ocean-colour estimates of chlorophyll concentration (an index of phytoplankton biomass) offer an observational platform to monitor the health of the Red Sea. However, little is known about the optical properties of the region. In this paper, we investigate the optical properties of the Red Sea in the context of satellite ocean-colour estimates of chlorophyll concentration. Making use of a new merged ocean-colour product, from the European Space Agency (ESA) Climate Change Initiative, and in situ data in the region, we test the performance of a series of ocean-colour chlorophyll algorithms. We find that standard algorithms systematically overestimate chlorophyll when compared with the in situ data. To investigate this bias we develop an ocean-colour model for the Red Sea, parameterised to data collected during the Tara Oceans expedition, that estimates remote-sensing reflectance as a function of chlorophyll concentration. We used the Red Sea model to tune the standard chlorophyll algorithms and the overestimation in chlorophyll originally observed was corrected. Results suggest that the overestimation was likely due to an excess of CDOM absorption per unit chlorophyll in the Red Sea when compared with average global conditions. However, we recognise that additional information is required to test the influence of other potential sources of the overestimation, such as aeolian dust, and we discuss uncertainties in the datasets used. We present a series of regional chlorophyll algorithms for the Red Sea, designed for a suite of ocean-colour sensors, that may be used for further testing.

Evolutionary history of Chaetognatha inferred from molecular and morphological data: a case study for body plan simplification.

BackgroundChaetognatha are a phylum of marine carnivorous animals which includes more than 130 extant species. The internal systematics of this group have been intensively debated since it was discovered in the 18th century. While they can be traced back to the earlier Cambrian, they are an extraordinarily homogeneous phylum at the morphological level - a fascinating characteristic that puzzled many a scientist who has tried to clarify their taxonomy. Recent studies which have attempted to reconstruct a phylogeny using molecular data have relied on single gene analyses and a somewhat restricted taxon sampling. Here, we present the first large scale phylogenetic study of Chaetognatha based on a combined analysis of nearly the complete ribosomal RNA (rRNA) genes. We use this analysis to infer the evolution of some morphological characters. This work includes 36 extant species, mainly obtained from Tara Oceans Expedition 2009/2012, that represent 16 genera and 6 of the 9 extant families.ResultsCladistic and phenetic analysis of morphological characters, geometric morphometrics and molecular small subunit (SSU rRNA) and large subunit (LSU rRNA) ribosomal genes phylogenies provided new insights into the relationships and the evolutionary history of Chaetognatha. We propose the following clade structure for the phylum: (((Sagittidae, Krohnittidae), Spadellidae), (Eukrohniidae, Heterokrohniidae)), with the Pterosagittidae included in the Sagittidae. The clade (Sagittidae, Krohnittidae) constitutes the monophyletic order of Aphragmophora. Molecular analyses showed that the Phragmophora are paraphyletic. The Ctenodontina/Flabellodontina and Syngonata/Chorismogonata hypotheses are invalidated on the basis of both morphological and molecular data. This new phylogeny also includes resurrected and modified genera within Sagittidae.ConclusionsThe distribution of some morphological characters traditionally used in systematics and for species diagnosis suggests that the diversity in Chaetognatha was produced through a process of mosaic evolution. Moreover, chaetognaths have mostly evolved by simplification of their body plan and their history shows numerous convergent events of losses and reversions. The main morphological novelty observed is the acquisition of a second pair of lateral fins in Sagittidae, which represents an adaptation to the holoplanktonic niche.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-014-0084-7) contains supplementary material, which is available to authorized users.

Particle size distribution and estimated carbon flux across the Arabian Sea oxygen minimum zone

Abstract. The goal of the Arabian Sea section of the TARA oceans expedition was to study large particulate matter (LPM > 100 μm) distributions and possible impact of associated midwater biological processes on vertical carbon export through the oxygen minimum zone (OMZ) of this region. We propose that observed spatial patterns in LPM distribution resulted from the timing and location of surface phytoplankton bloom, lateral transport, microbial processes in the core of the OMZ, and enhanced biological processes mediated by bacteria and zooplankton at the lower oxycline. Indeed, satellite-derived net primary production maps showed that the northern stations of the transect were under the influence of a previous major bloom event while the most southern stations were in a more oligotrophic situation. Lagrangian simulations of particle transport showed that deep particles of the northern stations could originate from the surface bloom while the southern stations could be considered as driven by 1-D vertical processes. In the first 200 m of the OMZ core, minima in nitrate concentrations and the intermediate nepheloid layer (INL) coincided with high concentrations of 100 μm < LPM < 200 μm. These particles could correspond to colonies of bacteria or detritus produced by anaerobic microbial activity. However, the calculated carbon flux through this layer was not affected. Vertical profiles of carbon flux indicate low flux attenuation in the OMZ, with a Martin model b exponent value of 0.22. At three stations, the lower oxycline was associated to a deep nepheloid layer, an increase of calculated carbon flux and an increase in mesozooplankton abundance. Enhanced bacterial activity and zooplankton feeding in the deep OMZ is proposed as a mechanism for the observed deep particle aggregation. Estimated lower flux attenuation in the upper OMZ and re-aggregation at the lower oxycline suggest that OMZ may be regions of enhanced carbon flux to the deep sea relative to non OMZ regions.

The Tara Oceans Expedition

Emmanuel Reynaud and Luis Gutierrez-Heredia Reynaud and Gutierrez-Heredia discuss the Tara Oceans Expedition – a unique circumnavigation of the earth on a 36 metre schooner to analyse and collect plankton communities and coral specimens, the fundamental building blocks upon which the largest ecosystems are built.

Underway sampling of marine inherent optical properties on the Tara Oceans expedition as a novel resource for ocean color satellite data product validation

Developing and validating data records from operational ocean color satellite instruments requires substantial volumes of high quality in situ data. In the absence of broad, institutionally supported field programs, organizations such as the NASA Ocean Biology Processing Group seek opportunistic datasets for use in their operational satellite calibration and validation activities. The publicly available, global biogeochemical dataset collected as part of the two and a half year Tara Oceans expedition provides one such opportunity. We showed how the inline measurements of hyperspectral absorption and attenuation coefficients collected onboard the R/V Tara can be used to evaluate near-surface estimates of chlorophyll-a, spectral particulate backscattering coefficients, particulate organic carbon, and particle size classes derived from the NASA Moderate Resolution Imaging Spectroradiometer onboard Aqua (MODISA). The predominant strength of such flow-through measurements is their sampling rate—the 375 days of measurements resulted in 165 viable MODISA-to-in situ match-ups, compared to 13 from discrete water sampling. While the need to apply bio-optical models to estimate biogeochemical quantities of interest from spectroscopy remains a weakness, we demonstrated how discrete samples can be used in combination with flow-through measurements to create data records of sufficient quality to conduct first order evaluations of satellite-derived data products. Given an emerging agency desire to rapidly evaluate new satellite missions, our results have significant implications on how calibration and validation teams for these missions will be constructed.

The characteristics of particulate absorption, scattering and attenuation coefficients in the surface ocean; Contribution of the Tara Oceans expedition

A dataset consisting of AC-S measurements of (hyper-) spectral particulate absorption, scattering and attenuation coefficients were obtained from measurements performed on the flow-through system of the R/V Tara during its 2.5-year long expedition.The AC-S instruments were robust, working continuously with weekly maintenance for about 3 months at a time, and provided absorption (attenuation) data for 454 (375) days, or 90% (75%) of total possible days during the expedition.This dataset has been mapped to 1 km×1 km bins to avoid over emphasizing redundant data, and to match the spatial scale of typical ocean color satellite sensors. It consists of nearly 70,000 particulate absorption spectra and about 60,000 particulate scattering and attenuation spectra. These data are found to be consistent with chlorophyll extraction and with the published average shapes of particulate absorption and scattering spectra and bio-optical relationships. This dataset is richer than previous ones in the data from open-ocean (oligotrophic) environments making it more representative of global distributions and of utility for global algorithm development.

Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses

Viruses influence oceanic ecosystems by causing mortality of microorganisms, altering nutrient and organic matter flux via lysis and auxiliary metabolic gene expression and changing the trajectory of microbial evolution through horizontal gene transfer. Limited host range and differing genetic potential of individual virus types mean that investigations into the types of viruses that exist in the ocean and their spatial distribution throughout the world's oceans are critical to understanding the global impacts of marine viruses. Here we evaluate viral morphological characteristics (morphotype, capsid diameter and tail length) using a quantitative transmission electron microscopy (qTEM) method across six of the world's oceans and seas sampled through the Tara Oceans Expedition. Extensive experimental validation of the qTEM method shows that neither sample preservation nor preparation significantly alters natural viral morphological characteristics. The global sampling analysis demonstrated that morphological characteristics did not vary consistently with depth (surface versus deep chlorophyll maximum waters) or oceanic region. Instead, temperature, salinity and oxygen concentration, but not chlorophyll a concentration, were more explanatory in evaluating differences in viral assemblage morphological characteristics. Surprisingly, given that the majority of cultivated bacterial viruses are tailed, non-tailed viruses appear to numerically dominate the upper oceans as they comprised 51-92% of the viral particles observed. Together, these results document global marine viral morphological characteristics, show that their minimal variability is more explained by environmental conditions than geography and suggest that non-tailed viruses might represent the most ecologically important targets for future research.

Phylogenetic Analysis of Thecosomata Blainville, 1824 (Holoplanktonic Opisthobranchia) Using Morphological and Molecular Data

Thecosomata is a marine zooplankton group, which played an important role in the carbonate cycle in oceans due to their shell composition. So far, there is important discrepancy between the previous morphological-based taxonomies, and subsequently the evolutionary history of Thecosomata. In this study, the remarkable planktonic sampling of TARA Oceans expedition associated with a set of various other missions allowed us to assess the phylogenetic relationships of Thecosomata using morphological and molecular data (28 S and COI genes). The two gene trees showed incongruities (e.g. Hyalocylis, Cavolinia), and high congruence between morphological and 28S trees (e.g. monophyly of Euthecosomata). The monophyly of straight shell species led us to reviving the Orthoconcha, and the split of Limacinidae led us to the revival of Embolus inflata replacing Limacina inflata. The results also jeopardized the Euthecosomata families that are based on plesiomorphic character state as in the case for Creseidae which was not a monophyletic group. Divergence times were also estimated, and suggested that the evolutionary history of Thecosomata was characterized by four major diversifying events. By bringing the knowledge of palaeontology, we propose a new evolutionary scenario for which macro-evolution implying morphological innovations were rhythmed by climatic changes and associated species turn-over that spread from the Eocene to Miocene, and were shaped principally by predation and shell buoyancy.

Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes

Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 104–105 genomes ml−1 for the samples from the photic zone and 102–103 genomes ml−1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.

Gutless Worm Harnesses Carbon Monoxide; Tara Vessel Explores Plankton

The marine worm Olavius algarvensis furnishes its closely associated bacteria with carbon monoxide and hydrogen as energy sources, while they, in turn, enabled it to rid itself of its gut and kidneys by drawing on its metabolites to meet their need for organic carbon compounds, according to Nicole Dubilier and Manuel Kleiner at the Max Planck Institute for Marine Microbiol-ogy in Bremen, Germany, and their collaborators. Separately, the diversity of marine microorganisms exceeds current estimates, basing his estimates on an early analysis of samples from the recently completed Tara Oceans expedition, a three-year voyage to sample marine plankton ecosystems as well as viruses and bacteria, says Jeroen Raes of Vrije Universiteit in Brussels, Belgium. He and Dubilier spoke last June, during the conference “Marine Microbes: Bridging the Gaps from Genomes to Biomes,” held in Lucca, Italy.