Functional repertoire convergence of distantly related eukaryotic plankton lineages revealed by genome-resolved metagenomics

Abstract

Marine planktonic eukaryotes play a critical role in global biogeochemical cycles and climate. However, their poor representation in culture collections limits our understanding of the evolutionary history and genomic underpinnings of planktonic ecosystems. Here, we used 280 billion metagenomic reads from 143 Tara Oceans stations to reconstruct and manually curate more than 700 abundant and widespread eukaryotic metagenome-assembled genomes ranging from 10 Mbp to up to 1.3 Gbp. The resulting non-redundant genomic resource of 25 billion nucleotides that describe 10 million genes covers a wide range of poorly characterized unicellular and multicellular eukaryotic lineages that complement the long-standing contributions of culture efforts to survey the tree of marine life while better representing plankton from the open ocean. Phylogeny of the DNA-dependent RNA polymerase placed this genomic resource in a comprehensive evolutionary framework that provided insights into the relationships of eukaryotic supergroups. From there, classification of unicellular eukaryotic plankton based on functions encoded in their genes revealed four major groups connecting distantly related lineages such as the diatoms and green algae. There has been a recurrent problem in understanding the interplay between eukaryotes' vertical evolution and their phenotype. By disentangling phylogenetic signals from functional trends with genomics, we found that neither the classical trophic mode of plankton nor its vertical evolutionary history could fully explain the genomic functional landscape of marine eukaryotes that coexisted for millions of years.

Genomic evidence for global ocean plankton biogeography shaped by large-scale current systems

“…We interpret this as being a result of the expected significantly lower resolution in imaging data as compared to metagenomic data (a similar difference of resolution in OTU data versus metagenomic data is discussed in Supplementary Information 1). Finally, we also confirmed our metagenome sequence read comparison-based results by comparing them to β-diversity among sampling sites using a collection of metagenome-assembled genomes (MAGs), which are likely to represent the most abundant genomes, from the 20-180 µm size fraction (the size fraction in which the largest proportion of metagenomic reads were mapped to MAGs, 18.4%) 21 . Metagenomic and MAG β-diversity were highly correlated (Spearman's ρ 0.94) and consequently they displayed similar biogeographical patterns ( Supplementary Fig.…”

“…MAG relative abundances in metagenomic samples were retrieved from Delmont et al 21 . β-diversity was estimated by calculating the Bray-Curtis dissimilarities between pairs of stations based on the relative abundances of each of the 713 MAGs calculated by read mapping in the metagenomes of size fraction 20-180 μm (the size fraction in which MAGs recruit the largest relative share of all reads).…”

“…We focus on analyses of metagenomic dissimilarity here, with accompanying results for OTU dissimilarity presented in Supplementary Figures, and validation by comparison to abundance differences among metagenome-assembled genomes 21 and to more traditional imaging data presented independently below.…”

Restructuring of genomic provinces of surface ocean plankton under climate change

“…Overall, our projections for the end of the century do not take into account possible future changes of major bio-physico-chemical factors such as dynamics of community mixing, trophic interactions through transport 46 , the potential dynamics of the genomes 14,16,17 (adaptation or acclimation) and biomass variations 45 . New sampling in current and future expeditions 47 , as well as ongoing technological improvements in bio-physico-chemical characterization of seawater samples 38,47,48 will soon refine functional 18,49 , environmental (micronutrients 50 ) and phylogenetic 16,17 characterization of plankton ecosystems for various biological entities (genotypes, species or communities) and spatio-temporal scales 47 . Ultimately, crossing this varied information will allow a better understanding of the conditions of emergence of ecological niches in the seascape and their response to a changing ocean.…”

“…These genomes are Metagenome-Assembled Genomes (MAGs) obtained from Tara Oceans metagenomes. For each size class, we select MAGs that are present (according to a criteria defined in Delmont et al 38 ) in at least 5 samples. We computed an index of presence enrichment of MAGs within provinces as the Jaccard index 51 , defined as follows: M 11 is the number of samples where the MAG is present and match a sample of the province.…”