Abundance and Biogeography of Picoprasinophyte Ecotypes and Other Phytoplankton in the Eastern North Pacific Ocean

Abstract

Eukaryotic algae within the picoplankton size class (<2 m 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.

Survey of the green picoalga Bathycoccus genomes in the global ocean

“…The former corresponds to the B1 clade and the latter to the B2 clade as, defined recently11. Orthologous proteins of these two genomes share only 78% identity, which is similar to the 74% of amino-acid identity shared by the two sequenced Ostreococcus isolates which belong to different clades52.…”

“…A previous study11 estimated a lower genetic distance (82% of identical nucleotides) between the two Bathycoccus using metagenomic data. This difference is probably as expected because of the reduced dataset of highly conserved and single copy genes (1 104 genes) considered in the latter analysis.…”

“…In contrast to cyanobacteria, the phylogenetic diversity of eukaryotic phytoplankton is wide, with species belonging to virtually all photosynthetic protist groups5. Among them, three genera of green algae belonging to the order Mamiellales (class Mamiellophyceae6), Micromonas, Ostreococcus and Bathycoccus are particularly important ecologically because they are found in a wide variety of oceanic ecosystems, from the poles to the tropics789101112. The cosmopolitan distribution of these genera raises the questions of their diversity and their adaptation to local environmental conditions.…”

“…Bathycoccus has been since found to be widespread in the oceanic environment, in particular in coastal waters2021, and one genome sequence from a coastal strain is available22. Metagenomic data have suggested the existence of two Bathycoccus ecotypes101123, recently named B1 and B211. These two ecotypes have identical 18S rRNA sequences and therefore cannot be discriminated when using metabarcodes such as the V4 or V9 regions of the 18S rRNA genes10.…”

Diversity and oceanic distribution of prasinophytes clade VII, the dominant group of green algae in oceanic waters

“…For example, Ostreococcus clade A seems to be typical from surface waters, whereas clade B appears to be associated with deeper layers of the euphotic zone Six et al, 2005). However, the physiological and environment parameter influencing clade distribution are more complex than irradiance alone, as showed for Ostreococcus (Simmons et al, 2016).…”