Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros

Abstract

Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros, the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data.

Fig 1. Global patterns of Chaetoceros genus distribution based on Tara Oceans metabarcoding data of V9 18S rDNA.

The 4 eukaryotic-enriched size fractions 0.8–5 μm, 5–20 μm, 20–180 μm, and 180–2,000 μm were pooled for a total of n = 2,739 OTU barcodes in SUR and DCM depths (see S1 Data for raw values). The basemap was generated from the Natural Earth data (http://www.naturalearthdata.com/downloads/50m-physical-vectors/); Natural Earth—All maps are public domain (http://www.naturalearthdata.com/about/terms-of-use/). DCM, deep-chlorophyll maximum; OTU, operational taxonomic unit; SUR, surface.

Fig 2. Characteristics of the different Chaetoceros MAGs.

(A) Genome size, (B) level of BUSCO completion (n = 255 BUSCOs), (C) number of genes, and (D) boxplots of mean gene length (mean gene length is represented by the blue dot) of the MAGs and reference diatoms C. tenuissimus (C.t.), P. tricornutum (P.t.), and T. pseudonana (T.p.). Only the assembly scaffolds of C. tenuissimus were available, preventing us from investigating the number of genes and their length. (E, F) PCA of different gene and genome metrics of the MAGs, shaded by geographical origin (blue: Arctic Ocean; purple: Mediterranean Sea; orange: Pacific South Eastern Ocean; green: Pacific South Western Ocean; black: Southern Ocean) (See Tables B and C in S1 Table for raw values). BUSCO, Benchmarking Universal Single-Copy Orthologs; MAG, metagenome-assembled genome; PCA, principal component analysis.

Fig 3. Relatedness of the Chaetoceros MAGs.

(A) ANI. (B) Concatenated multigene ML tree generated with RAxML (100 bootstrap), based on 83 BUSCO gene clusters with the Chaetoceros MAGs highlighted in gold. Bootstrap values ≥ 50% are indicated. ANI, average nucleotide identity; BUSCO, Benchmarking Universal Single-Copy Orthologs; MAG, metagenome-assembled genome.

Fig 4. Biogeography of the Chaetoceros MAGs throughout Tara Oceans sampling sites.

(A) Relative contributions of the Chaetoceros MAGs in SUR and DCM depths (see Tables A and B in S4 Table for details). The basemap was generated from the Natural Earth data (http://www.naturalearthdata.com/downloads/50m-physical-vectors/); Natural Earth—All maps are public domain (http://www.naturalearthdata.com/about/terms-of-use/). (B) Pairwise correlation patterns of the MAG relative abundances across Tara Oceans stations (the colour bar represents Spearman’s correlation rho; values are shown when p-value is inferior to 0.05). (C) Bubble plot corresponding to the measured temperature at the sampling stations where each MAG was detected. DCM, deep-chlorophyll maximum; MAG, metagenome-assembled genome; SUR, surface.

Fig 5. Population genomic analyses of Chaetoceros MAGs.

(A) Scatterplot representing the number of SNVs compared to the number of reads for all samples considered in this study with Pearson’s correlation rho (n = 29). (B) Relative number of SNVs within ARC_116 populations. (C) F_ST distribution profile of ARC_116. (D) Pairwise F_ST matrix of ARC_116 populations. (E) Global pairwise F_ST matrix of all MAGs among Arctic Ocean regions (refers to ARC_116, ARC_189, ARC_217, PSW_256, and SOC_37). D: deep-chlorophyll maximum; S: surface. (F) Polar view of the Arctic Ocean regions (based on [48]). The basemap was generated from the Natural Earth data (http://www.naturalearthdata.com/downloads/50m-physical-vectors/); Natural Earth—All maps are public domain (http://www.naturalearthdata.com/about/terms-of-use/). MAG, metagenome-assembled genome; SNV, single-nucleotide variant.

Fig 6. Correlation between environmental parameters variation and Chaetoceros genomic differentiation.

Bar plots of variance partitioning analysis results for (A) ARC_116, (B) ARC_217, and (C) SOC_37 (see Sheets G–I in S7 Data for details). NO3_NO2: sum of nitrate and nitrite concentrations; Phos.: phosphate; Silic.: silicate; Temp.: temperature.

Fig 7. Selection of variants in Arctic Chaetoceros populations.

(A) and (C) represent Manhattan plots in a 10 kb window around the variants of interest, shown for ARC_217 (ISIP) and SOC_37 (spermidine/spermine synthase). Red dots correspond to SNVs considered under selection (q-value < 0.15). (B) and (D) represent the bar plots of the BAF for the respective loci of interest depending on the population considered. (E) Range-transformed heatmap of abiotic parameters for the Tara Oceans stations in the Arctic Ocean where the Chaetoceros MAGs are present (see S6 Table for raw values). The brightest yellow colour represents the most elevated values for any given parameter in the dataset, while the darkest purple indicates the lowest. D: deep-chlorophyll maximum; S: surface. BAF, B-allele frequency; ISIP, iron starvation-induced protein; MAG, metagenome-assembled genome; SNV, single-nucleotide variant.