Planktonic protist diversity across contrasting Subtropical and Subantarctic waters of the southwest Pacific

Planktonic protists are an essential component of marine pelagic ecosystems where they mediate important trophic and biogeochemical functions. Although these functions are largely influenced by their taxonomic affiliation, the composition and spatial variability of planktonic protist communities remain poorly characterized in vast areas of the ocean. Here, we investigated the diversity of these communities in contrasting oceanographic conditions of the southwest Pacific sector (33-58 S) using DNA metabarcoding of the 18S rRNA. Seawater samples collected during twelve cruises (n = 482, 0-2000 m) conducted east of New Zealand were used to characterize protist communities in subtropical (STW) and subantarctic (SAW) water masses and the subtropical front (STF) that separates them. Diversity decreased with latitude and temperature but tended to be lowest in the STF. Sample ordination resulting from the abundance of amplicon single variants (ASVs) corresponded to the different water masses. Overall, Dinophyceae (34% of standardized total reads) and Chlorophyta (27%) co-dominated the euphotic zone, but their relative abundance and composition at class and lower taxonomic levels varied consistently between water masses. Among Chlorophyta, several picoplanktonic algae species of the Mamiellophyceae class including Ostreococcus lucimarinus dominated in STW, while the Chloropicophyceae species Chloroparvula pacifica was most abundant in SAW. Bacillariophyta (7%), Prymnesiophyceae (5%), and Pelagophyceae (3%) classes were less abundant but showed analogous water mass specificity at class and finer taxonomic levels. Protist community composition in the STFZ had mixed characteristics and showed regional differences with the southern STF (50 S) having more resemblance with subantarctic communities than the STF over the Chatham Rise region (42-44 S). Below the euphotic zone, Radiolaria sequences dominated the dataset (52%) followed by Dinophyceae (27%) and other heterotrophic groups like Marine Stramenopiles and ciliates (3%). Among Radiolaria, several unidentified ASVs assigned to Spumellarida were most abundant, but showed significantly different distribution between STW and SAW highlighting the need to further.

Genome Resolved Biogeography of Mamiellales

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.

Diversity of Viruses Infecting the Green Microalga Ostreococcus lucimarinus

ABSTRACTThe functional diversity of eukaryotic viruses infecting a single host strain from seawater samples originating from distant marine locations is unknown. To estimate this diversity, we used lysis plaque assays to detect viruses that infect the widespread speciesOstreococcus lucimarinus, which is found in coastal and mesotrophic systems, andO. tauri, which was isolated from coastal and lagoon sites from the northwest Mediterranean Sea. Detection of viral lytic activities againstO. tauriwas not observed using seawater from most sites, except those close to the area where the host strain was isolated. In contrast, the more cosmopolitanO. lucimarinusspecies recovered viruses from locations in the Atlantic and Pacific Oceans and the Mediterranean Sea. Six newO. lucimarinusviruses (OlVs) then were characterized and their genomes sequenced. Two subgroups of OlVs were distinguished based on their genetic distances and on the inversion of a central 32-kb-long DNA fragment, but overall their genomes displayed a high level of synteny. The two groups did not correspond to proximity of isolation sites, and the phylogenetic distance between these subgroups was higher than the distances observed among viruses infectingO. tauri. Our study demonstrates that viruses originating from very distant sites are able to infect the same algal host strain and can be more diverse than those infecting different species of the same genus. Finally, distinctive features and evolutionary distances between these different viral subgroups does not appear to be linked to biogeography of the viral isolates.IMPORTANCEMarine eukaryotic phytoplankton virus diversity has yet to be addressed, and more specifically, it is unclear whether diversity is connected to geographical distance and whether differential infection and lysis patterns exist among such viruses that infect the same host strain. Here, we assessed the genetic distance of geographically segregated viruses that infect the ubiquitous green microalgaOstreococcus. This study provides the first glimpse into the diversity of predicted gene functions inOstreococcusviruses originating from distant sites and provides new insights into potential host distributions and restrictions in the world oceans.

Marine Prasinovirus Genomes Show Low Evolutionary Divergence and Acquisition of Protein Metabolism Genes by Horizontal Gene Transfer

ABSTRACT 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.

The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation

The smallest known eukaryotes, at ≈1-μm diameter, are Ostreococcus tauri and related species of marine phytoplankton. The genome of Ostreococcus lucimarinus has been completed and compared with that of O. tauri. This comparison reveals surprising differences across orthologous chromosomes in the two species from highly syntenic chromosomes in most cases to chromosomes with almost no similarity. Species divergence in these phytoplankton is occurring through multiple mechanisms acting differently on different chromosomes and likely including acquisition of new genes through horizontal gene transfer. We speculate that this latter process may be involved in altering the cell-surface characteristics of each species. In addition, the genome of O. lucimarinus provides insights into the unique metal metabolism of these organisms, which are predicted to have a large number of selenocysteine-containing proteins. Selenoenzymes are more catalytically active than similar enzymes lacking selenium, and thus the cell may require less of that protein. As reported here, selenoenzymes, novel fusion proteins, and loss of some major protein families including ones associated with chromatin are likely important adaptations for achieving a small cell size.