RESUMEN

Parmales (Bolidophyceae) is a minor eukaryotic phytoplankton group, sister to diatoms, which exists as two distinct forms of unicellular organisms: silicified cells and naked flagellates. Since their discovery, many field studies on Parmales have been performed; however, their global distribution has not yet been examined in detail. We herein compiled more than 3,000 marine DNA metabarcoding datasets targeting the V4 region of the 18S rRNA gene from the EukBank database. By linking this large dataset with the latest morphological and genetic information, we provide updated estimates on the diversity and distribution of Parmales in the global ocean at a fine taxonomic resolution. Parmalean amplicon sequence variants (ASVs) were detected in nearly 90% of the samples analyzed. However, the relative abundance of parmaleans in the eukaryotic community was less than 0.2% on average, and the estimated true richness of parmalean ASVs was approximately 316 ASVs, confirming their low abundance and diversity. A phylogenetic ana-lysis divided these algae into four clades, and three known morphotypes of silicified cells were classified into three different clades. The abundance of Parmales is generally high in the poles and decreases towards the tropics, and individual clades/subclades show further distinctions in their distribution. Collectively, the present results suggest clade/subclade-specific adaptation to different ecological niches.

Asunto(s)

Biodiversidad , Diatomeas , Filogenia , Fitoplancton/genética , Diatomeas/genética , Ecosistema

RESUMEN

The order Parmales (class Bolidophyceae) is a minor group of pico-sized eukaryotic marine phytoplankton that contains species with cells surrounded by silica plates. Previous studies revealed that Parmales is a member of ochrophytes and sister to diatoms (phylum Bacillariophyta), the most successful phytoplankton group in the modern ocean. Therefore, parmalean genomes can serve as a reference to elucidate both the evolutionary events that differentiated these two lineages and the genomic basis for the ecological success of diatoms vs. the more cryptic lifestyle of parmaleans. Here, we compare the genomes of eight parmaleans and five diatoms to explore their physiological and evolutionary differences. Parmaleans are predicted to be phago-mixotrophs. By contrast, diatoms have lost genes related to phagocytosis, indicating the ecological specialization from phago-mixotrophy to photoautotrophy in their early evolution. Furthermore, diatoms show significant enrichment in gene sets involved in nutrient uptake and metabolism, including iron and silica, in comparison with parmaleans. Overall, our results suggest a strong evolutionary link between the loss of phago-mixotrophy and specialization to a silicified photoautotrophic life stage early in diatom evolution after diverging from the Parmales lineage.

Asunto(s)

Diatomeas , Estramenopilos , Diatomeas/genética , Estramenopilos/genética , Fitoplancton/metabolismo , Genoma , Dióxido de Silicio

RESUMEN

Viruses have long been viewed as entities possessing extremely limited metabolic capacities. Over the last decade, however, this view has been challenged, as metabolic genes have been identified in viruses possessing large genomes and virions-the synthesis of which is energetically demanding. Here, we unveil peculiar phenotypic and genomic features of Prymnesium kappa virus RF01 (PkV RF01), a giant virus of the Mimiviridae family. We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, such as all four succinate dehydrogenase (SDH) subunits (A-D) as well as key enzymes in the ß-oxidation pathway. The SDHA gene was transcribed upon infection, indicating that the viral SDH is actively used by the virus- potentially to modulate its host's energy metabolism. We detected orthologous SDHA and SDHB genes in numerous genome fragments from uncultivated marine Mimiviridae viruses, which suggests that the viral SDH is widespread in oceans. PkV RF01 was less virulent compared with other cultured prymnesioviruses, a phenomenon possibly linked to the metabolic capacity of this virus and suggestive of relatively long co-evolution with its hosts. It also has a unique morphology, compared to other characterized viruses in the Mimiviridae family. Finally, we found that PkV RF01 is the only alga-infecting Mimiviridae virus encoding two aminoacyl-tRNA synthetases and enzymes corresponding to an entire base-excision repair pathway, as seen in heterotroph-infecting Mimiviridae These Mimiviridae encoded-enzymes were found to be monophyletic and branching at the root of the eukaryotic tree of life. This placement suggests that the last common ancestor of Mimiviridae was endowed with a large, complex genome prior to the divergence of known extant eukaryotes.IMPORTANCE Viruses on Earth are tremendously diverse in terms of morphology, functionality, and genomic composition. Over the last decade, the conceptual gap separating viruses and cellular life has tightened because of the detection of metabolic genes in viral genomes that express complex virus phenotypes upon infection. Here, we describe Prymnesium kappa virus RF01, a large alga-infecting virus with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic (TCA) cycle and the ß-oxidation pathway). Moreover, we show that the gene corresponding to one of these enzymes (the succinate dehydrogenase subunit A) is transcribed during infection and is widespread among marine viruses. This discovery provides evidence that a virus has the potential to actively regulate energy metabolism with its own gene.