Seasonality in marine microorganisms has been classically observed in phytoplankton blooms, and more recently studied at the community level in prokaryotes, but rarely investigated at the scale of individual microbial taxa. Here we test if specific marine eukaryotic phytoplankton, bacterial and archaeal taxa display yearly rhythms at a coastal site impacted by irregular environmental perturbations. Our seven-year study in the Bay of Banyuls (North Western Mediterranean Sea) shows that despite some fluctuating environmental conditions, many microbial taxa displayed significant yearly rhythms. The robust rhythmicity was found in both autotrophs (picoeukaryotes and cyanobacteria) and heterotrophic prokaryotes. Sporadic meteorological events and irregular nutrient supplies did, however, trigger the appearance of less common non-rhythmic taxa. Among the environmental parameters that were measured, the main drivers of rhythmicity were temperature and day length. Seasonal autotrophs may thus be setting the pace for rhythmic heterotrophs. Similar environmental niches may be driving seasonality as well. The observed strong association between Micromonas and SAR11, which both need thiamine precursors for growth, could be a first indication that shared nutritional niches may explain some rhythmic patterns of cooccurrence.

The ecology and distribution of green phytoplankton (Chlorophyta) in the ocean is poorly known because most studies have focused on groups with large cell size such as diatoms or dinoflagellates that are easily recognized by traditional techniques such as microscopy. The Ocean Sampling Day (OSD) project sampled surface waters quasi-simultaneously at 141 marine locations, mostly in coastal waters. The analysis of the 18S V4 region OSD metabarcoding dataset reveals that Chlorophyta are ubiquitous and can be locally dominant in coastal waters. Chlorophyta represented 29% of the global photosynthetic reads (Dinoflagellates excluded) and their contribution was especially high at oligotrophic stations (up to 94%) and along the European Atlantic coast. Mamiellophyceae dominated most coastal stations. At some coastal stations, they were replaced by Chlorodendrophyceae, Ulvophyceae, Trebouxiophyceae or Chlorophyceae as the dominating group, while oligotrophic stations were dominated either by Chloropicophyceae or the uncultured prasinophytes clade IX. Several Chlorophyta classes showed preferences in terms of nitrate concentration, distance to the coast, temperature and salinity. For example, Chlorophyceae preferred cold and low salinity coastal waters, and prasinophytes clade IX warm, high salinity, oligotrophic oceanic waters.

Mamiellophyceae (unicellular green algae) are a key phytoplankton group in coastal waters. Although extensively studied over the last 20 years, the overall oceanic distribution of the major species/clades is still poorly known. To address this problem, we analyzed the 2014 Ocean Sampling Day (OSD) metabarcoding dataset providing sequences from the V4 hypervariable region of the 18S rRNA gene for 157 samples collected at 143 mostly coastal stations. Mamiellophyceae were found at nearly all OSD stations and represented 55% of the green microalgae (Chlorophyta) reads. We performed phylogenetic analyses of unique OSD metabarcodes (amplicon single variants, ASVs) and GenBank reference sequences from cultures and from the environment, focusing on the four most represented genera: Ostreococcus (45% of the Mamiellophyceae reads), Micromonas (34%), Bathycoccus (10%) and Mantoniella (8.7%). These analyses uncovered novel diversity within each genus except Bathycoccus. In Ostreococcus, a new clade (E) was the second most represented clade after Ostreococcus “lucimarinus”. Micromonas could be separated into nine clades, exceeding the six species and candidate species already described. Finally, we found two new environmental clades within Mantoniella. Each Mamiellophyceae clade had a specific distribution in the OSD dataset suggesting that they are adapted to different ecological niches.

Prasinophytes clade VII is a group of pico/nano-planktonic green algae (division Chlorophyta) for which numerous ribosomal RNA (rRNA) sequences have been retrieved from the marine environment in the last 15 years. A large number of strains have also been isolated but have not yet received a formal taxonomic description. A phylogenetic analysis of available strains using both the nuclear 18S and plastidial 16S rRNA genes demonstrates that this group composes at least 10 different clades: A1-A7 and B1-B3. Analysis of sequences from the variable V9 region of the 18S rRNA gene collected during the Tara Oceans expedition and in the frame of the Ocean Sampling Day consortium reveal that clade VII is the dominant Chlorophyta group in oceanic waters, replacing Mamiellophyceae, which have this role in coastal waters. At some location, prasinophytes clade VII can even be the dominant photosynthetic eukaryote representing up to 80% of photosynthetic metabarcodes overall. B1 and A4 are the overall dominant clades and different clades seem to occupy distinct niches, for example, A6 is dominant in surface Mediterranean Sea waters, whereas A4 extend to high temperate latitudes. Our work demonstrates that prasinophytes clade VII constitute a highly diversified group, which is a key component of phytoplankton in open oceanic waters but has been neglected in the conceptualization of marine microbial diversity and carbon cycle.

We compared the composition of eukaryotic communities using two genetic markers (18S rRNA V4 and V9 regions) at 27 sites sampled during Ocean Sampling Day 2014, with a focus on photosynthetic groups and, more specifically green algae (Chlorophyta). Globally, the V4 and V9 regions of the 18S rRNA gene provided similar images of alpha diversity and ecological patterns. However, V9 provided 20% more OTUs built at 97% identity than V4. 34% of the genera were found with both markers and, of the remnant, 22% were found only with V4 and 44% only with V9. For photosynthetic groups, V4 and V9 performed equally well to describe global communities at different taxonomic levels from the division to the genus and provided similar Chlorophyta distribution patterns. However, at lower taxonomic level, the V9 dataset failed for example to describe the diversity of Dolichomastigales (Chlorophyta, Mamiellophyceae) emphasizing the lack of V9 sequences for this group and the importance of the reference database for metabarcode analysis. We conclude that in order to address questions regarding specific groups (e.g., a given genus), it is necessary to choose the marker based not only on the genetic divergence within this group but also on the existence of reference sequences in databases.

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Abstract. The Green Edge initiative was developed to investigate the processes controlling the primary productivity and fate of organic matter produced during the Arctic phytoplankton spring bloom (PSB) and to determine its role in the ecosystem. Two field campaigns were conducted in 2015 and 2016 at an ice camp located on landfast sea ice southeast of Qikiqtarjuaq Island in Baffin Bay (67.4797∘ N, 63.7895∘ W). During both expeditions, a large suite of physical, chemical and biological variables was measured beneath a consolidated sea-ice cover from the surface to the bottom (at 360 m depth) to better understand the factors driving the PSB. Key variables, such as conservative temperature, absolute salinity, radiance, irradiance, nutrient concentrations, chlorophyll a concentration, bacteria, phytoplankton and zooplankton abundance and taxonomy, and carbon stocks and fluxes were routinely measured at the ice camp. Meteorological and snow-relevant variables were also monitored. Here, we present the results of a joint effort to tidy and standardize the collected datasets, which will facilitate their reuse in other Arctic studies. The dataset is available at https://doi.org/10.17882/59892 (Massicotte et al., 2019a).

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