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The marine picoeukaryote Bathycoccus prasinos has been considered a cosmopolitan alga, although recent studies indicate two ecotypes exist, Clade BI (B. prasinos) and Clade BII. Viruses that infect Bathycoccus Clade BI are known (BpVs), but not that infect BII. We isolated three dsDNA prasinoviruses from the Sargasso Sea against Clade BII isolate RCC716. The BII-Vs do not infect BI, and two (BII-V2 and BII-V3) have larger genomes (~210 kb) than BI-Viruses and BII-V1. BII-Vs share ~90% of their proteins, and between 65% to 83% of their proteins with sequenced BpVs. Phylogenomic reconstructions and PolB analyses establish close-relatedness of BII-V2 and BII-V3, yet BII-V2 has 10-fold higher infectivity and induces greater mortality on host isolate RCC716. BII-V1 is more distant, has a shorter latent period, and infects both available BII isolates, RCC716 and RCC715, while BII-V2 and BII-V3 do not exhibit productive infection of the latter in our experiments. Global metagenome analyses show Clade BI and BII algal relative abundances correlate positively with their respective viruses. The distributions delineate BI/BpVs as occupying lower temperature mesotrophic and coastal systems, whereas BII/BII-Vs occupy warmer temperature, higher salinity ecosystems. Accordingly, with molecular diagnostic support, we name Clade BII Bathycoccus calidus sp. nov. and propose that molecular diversity within this new species likely connects to the differentiated host-virus dynamics observed in our time course experiments. Overall, the tightly linked biogeography of Bathycoccus host and virus clades observed herein supports species-level host specificity, with strain-level variations in infection parameters.

The abundance, biomass, and composition of phototrophic picoeukaryotes (PPE, cell size less than 3 μm) were studied in Onega Bay of the White Sea in June 2015. The highest PPE abundance and biomass were registered in the 0–5-m water layer. In the bay, in the 0–5-m water layer, the average abundance and biomass varied from 0 to 36.8 × 104 cell/L and from 0 to 117 μg С/m3, respectively. The Illumina sequencing of V4 region of 18S rRNA gene revealed eight classes of PPE. Mamiellophyceae dominated both by number of reads and by operational taxonomic units. The green algae Bathycoccus prasinos, Ostreococcus tauri, and Micromonas pusila, as well as diatoms Skeletonema marinoi and Minidiscus trioculatus, were identified to the species level.

Bathycoccus and Ostreococcus are broadly distributed marine picoprasinophyte algae. We enumerated small phytoplankton using flow cytometry and qPCR assays for phylogenetically distinct Bathycoccus clades BI and BII and Ostreococcus clades OI and OII. Among 259 photic-zone samples from transects and time-series, Ostreococcus maxima occurred in the North Pacific coastal upwelling for OI (36 713 ± 1485 copies ml−1) and the Kuroshio Front for OII (50 189 ± 561 copies ml−1) and the two overlapped only in frontal regions. The Bathycoccus overlapped more often with maxima along Line-P for BI (10 667 ± 1299 copies ml−1) and the tropical Atlantic for BII (4125 ± 339 copies ml−1). Only BII and OII were detected at warm oligotrophic sites, accounting for 34 ± 13 of 1589 ± 448 eukaryotic phytoplankton cells ml−1 (annual average) at Station ALOHA's deep chlorophyll maximum. Significant distributional and molecular differences lead us to propose that Bathycoccus clade BII represents a separate species which tolerates higher temperature oceanic conditions than Bathycoccus prasinos (BI). Morphological differences were not evident, but quick-freeze deep-etch electron microscopy provided insight into Bathycoccus scale formation. Our results highlight the importance of quantitative seasonal abundance data for inferring ecological distributions and demonstrate significant, differential picoprasinophyte contributions in mesotrophic and open-ocean waters. © 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

Although marine picophytoplankton are at the base of the global food chain, accounting for half of the planetary primary production, they are outnumbered 10 to 1 and are largely controlled by hugely diverse populations of viruses. Eukaryotic microalgae form a ubiquitous and particularly dynamic fraction of such plankton, with environmental clone libraries from coastal regions sometimes being dominated by one or more of the three genera Bathycoccus , Micromonas , and Ostreococcus (class Prasinophyceae). The complete sequences of two double-stranded (dsDNA) Bathycoccus , one dsDNA Micromonas , and one new dsDNA Ostreococcus virus genomes are described. Genome comparison of these giant viruses revealed a high degree of conservation, both for orthologous genes and for synteny, except for one 36-kb inversion in the Ostreococcus lucimarinus virus and two very large predicted proteins in Bathycoccus prasinos viruses. These viruses encode a gene repertoire of certain amino acid biosynthesis pathways never previously observed in viruses that are likely to have been acquired from lateral gene transfer from their host or from bacteria. Pairwise comparisons of whole genomes using all coding sequences with homologous counterparts, either between viruses or between their corresponding hosts, revealed that the evolutionary divergences between viruses are lower than those between their hosts, suggesting either multiple recent host transfers or lower viral evolution rates.

Eukaryotic algae within the picoplankton size class (≤2 μm in diameter) are important marine primary producers, but their spatial and ecological distributions are not well characterized. Here, we studied three picoeukaryotic prasinophyte genera and their cyanobacterial counterparts, Prochlorococcus and Synechococcus , during two cruises along a North Pacific transect characterized by different ecological regimes. Picoeukaryotes and Synechococcus reached maximum abundances of 1.44 × 10 5 and 3.37 × 10 5 cells · ml −1 , respectively, in mesotrophic waters, while Prochlorococcus reached 1.95 × 10 5 cells · ml −1 in the oligotrophic ocean. Of the picoeukaryotes, Bathycoccus was present at all stations in both cruises, reaching 21,368 ± 327 18S rRNA gene copies · ml −1 . Micromonas and Ostreococcus clade OI were detected only in mesotrophic and coastal waters and Ostreococcus clade OII only in the oligotrophic ocean. To resolve proposed Bathycoccus ecotypes, we established genetic distances for 1,104 marker genes using targeted metagenomes and the Bathycoccus prasinos genome. The analysis was anchored in comparative genome analysis of three Ostreococcus species for which physiological and environmental data are available to facilitate data interpretation. We established that two Bathycoccus ecotypes exist, named here BI (represented by coastal isolate Bathycoccus prasinos ) and BII. These share 82% ± 6% nucleotide identity across homologs, while the Ostreococcus spp. share 75% ± 8%. We developed and applied an analysis of ecomarkers to metatranscriptomes sequenced here and published -omics data from the same region. The results indicated that the Bathycoccus ecotypes cooccur more often than Ostreococcus clades OI and OII do. Exploratory analyses of relative transcript abundances suggest that Bathycoccus NRT2.1 and AMT2.2 are high-affinity NO 3 − and low-affinity NH 4 + transporters, respectively, with close homologs in multiple picoprasinophytes. Additionally, in the open ocean, where dissolved iron concentrations were low (0.08 nM), there appeared to be a shift to the use of nickel superoxide dismutases (SODs) from Mn/Fe/Cu SODs closer inshore. Our study documents the distribution of picophytoplankton along a North Pacific ecological gradient and offers new concepts and techniques for investigating their biogeography.

9 pages, 4 figures, 4 tables, The class Prasinophyceae (Chlorophyta) contains several photosynthetic picoeukaryotic species described from cultured isolates. The ecology of these organisms and their contributions to the picoeukaryotic community in aquatic ecosystems have received little consideration. We have designed and tested eight new 18S ribosomal DNA oligonucleotide probes specific for different Prasinophyceae clades, genera, and species. Using fluorescent in situ hybridization associated with tyramide signal amplification, these probes, along with more general probes, have been applied to samples from a marine coastal site off Roscoff (France) collected every 2 weeks between July 2000 and September 2001. The abundance of eukaryotic picoplankton remained high (>103 cells ml-1) during the sampling period, with maxima in summer (up to 2 × 104 cells ml-1), and a single green algal species, Micromonas pusilla (Prasinophyceae), dominated the community all year round. Members of the order Prasinococcales and the species Bathycoccus prasinos (Mamiellales) displayed sporadic occurrences, while the abundances of all other Prasinophyceae groups targeted remained negligible, This work was funded by the following programs: PICODIV, supported by the European Union (EVK3-CT-1999-00021); PICMANCH, supported by the Région Bretagne; and BIOSOPE, supported by PROOF (CNRS). F.N. was supported by a doctoral fellowship from the French Research Ministry

Rapid shifts in picoeukaryote community structure were observed during a CO2 perturbation experiment in which we followed the development of phytoplankton blooms in nutrient-amended mesocosms under present day or predicted future atmospheric pCO2 (750 μatm, seawater pH 7.8). Analysis of rbcL clone libraries (encoding the large subunit of RubisCO) and specific QPCR assays showed that two prasinophytes closely related to Micromonas pusilla and Bathycoccus prasinos were present but responded very differently to high CO2/acidification. We found that the abundance of Micromonas-like phylotypes was significantly higher (>20-fold) under elevated CO2/low pH, whereas the Bathycoccus-like phylotypes were more evenly distributed between treatments and dominated the prasinophyte community under ambient conditions. Rapid shifts in picoeukaryote community structure were observed during a CO2 perturbation experiment in which we followed the development of phytoplankton blooms in nutrient-amended mesocosms under present day or predicted future atmospheric pCO2 (750 μatm, seawater pH 7.8). Analysis of rbcL clone libraries (encoding the large subunit of RubisCO) and specific QPCR assays showed that two prasinophytes closely related to Micromonas pusilla and Bathycoccus prasinos were present but responded very differently to high CO2/acidification. We found that the abundance of Micromonas-like phylotypes was significantly higher (>20-fold) under elevated CO2/low pH, whereas the Bathycoccus-like phylotypes were more evenly distributed between treatments and dominated the prasinophyte community under ambient conditions.

A non-motile, picoplanktonic species, Bathycoccus prasinos gen. et sp. nov. (Mamiellaceae, Mamiellales, Prasinophyceae) is described from the Gulf of Naples, Italy. Resembling a comma, the cells ar...

BackgroundBathycoccus prasinos is an extremely small cosmopolitan marine green alga whose cells are covered with intricate spider's web patterned scales that develop within the Golgi cisternae before their transport to the cell surface. The objective of this work is to sequence and analyze its genome, and to present a comparative analysis with other known genomes of the green lineage.ResearchIts small genome of 15 Mb consists of 19 chromosomes and lacks transposons. Although 70% of all B. prasinos genes share similarities with other Viridiplantae genes, up to 428 genes were probably acquired by horizontal gene transfer, mainly from other eukaryotes. Two chromosomes, one big and one small, are atypical, an unusual synapomorphic feature within the Mamiellales. Genes on these atypical outlier chromosomes show lower GC content and a significant fraction of putative horizontal gene transfer genes. Whereas the small outlier chromosome lacks colinearity with other Mamiellales and contains many unknown genes without homologs in other species, the big outlier shows a higher intron content, increased expression levels and a unique clustering pattern of housekeeping functionalities. Four gene families are highly expanded in B. prasinos, including sialyltransferases, sialidases, ankyrin repeats and zinc ion-binding genes, and we hypothesize that these genes are associated with the process of scale biogenesis.ConclusionThe minimal genomes of the Mamiellophyceae provide a baseline for evolutionary and functional analyses of metabolic processes in green plants.

Among marine phytoplankton, Mamiellales encompass several species from the genera Micromonas, Ostreococcus and Bathycoccus, which are important contributors to primary production. Previous studies based on single gene markers described their wide geographical distribution but led to discussion because of the uneven taxonomic resolution of the method. Here, we leverage genome sequences for six Mamiellales species, two from each genus Micromonas, Ostreococcus and Bathycoccus, to investigate their distribution across 133 stations sampled during the Tara Oceans expedition. Our study confirms the cosmopolitan distribution of Mamiellales and further suggests non-random distribution of species, with two triplets of co-occurring genomes associated with different temperatures: Ostreococcus lucimarinus, Bathycoccus prasinos and Micromonas pusilla were found in colder waters, whereas Ostreococcus spp. RCC809, Bathycoccus spp. TOSAG39-1 and Micromonas commoda were more abundant in warmer conditions. We also report the distribution of the two candidate mating-types of Ostreococcus for which the frequency of sexual reproduction was previously assumed to be very low. Indeed, both mating types were systematically detected together in agreement with either frequent sexual reproduction or the high prevalence of a diploid stage. Altogether, these analyses provide novel insights into Mamiellales’ biogeography and raise novel testable hypotheses about their life cycle and ecology.