Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton

Abstract

Marine phytoplankton play important roles in the global ecosystem, with a limited number of cosmopolitan keystone species driving their biomass. Recent studies have revealed that many of these phytoplankton are complexes composed of sibling species, but little is known about the evolutionary processes underlying their formation. Gephyrocapsa huxleyi, a widely distributed and abundant unicellular marine planktonic algae, produces calcified scales (coccoliths), thereby significantly affects global biogeochemical cycles via sequestration of inorganic carbon. This species is composed of morphotypes defined by differing degrees of coccolith calcification, the evolutionary ecology of which remains unclear. Here, we report an integrated morphological, ecological and genomic survey across globally distributed G. huxleyi strains to reconstruct evolutionary relationships between morphotypes in relation to their habitats. While G. huxleyi has been considered a single cosmopolitan species, our analyses demonstrate that it has evolved to comprise at least three distinct species, which led us to formally revise the taxonomy of the G. huxleyi complex. Moreover, the first speciation event occurred before the onset of the last interglacial period (~140 ka), while the second followed during this interglacial. Then, further rapid diversifications occurred during the most recent ice-sheet expansion of the last glacial period and established morphotypes as dominant populations across environmental clines. These results suggest that glacial-cycle dynamics contributed to the isolation of ocean basins and the segregations of oceans fronts as extrinsic drivers of micro-evolutionary radiations in extant marine phytoplankton.

Biological and genomic resources for the cosmopolitan phytoplanktonBathycoccus: Insights into genetic diversity and major structural variations

“…The exploitation of natural diversity has greatly contributed to the characterization of genomic features and to the exploration of adaptive mechanisms not only in Arabidopsis but also in other wild land plants and crops cultivars (Alonso-Blanco et al, 2016; Gabur et al, 2019 for review). However, the intraspecific diversity of eukaryotic phytoplankton remains widely unexplored, with only a few studies conducted in Ostreococcus tauri (Blanc-Mathieu et al, 2017), Phaeodactylum tricornutum (Rastogi et al, 2020) and Emiliania Huxleyi (Read et al, 2013; Bendif et al, 2023). In all these studies, reference-assisted assembly approaches based on short reads mapping to a single reference genome were used.…”

A novel fluoro-electrochemical technique for classifying diverse marine nanophytoplankton

“…This is of relevance to the method, because across all our assessments using the random forest analysis it was the "Calcifying Isochrysidales" group that consistently retained the highest level of prediction accuracy of all the key functional groups. Taking our investigation further, we next take a closer look at within species variability to disentangle if any of the particular strains of E. huxleyi, representing different life stages and calcification morphologies (Green et al 1996;Young et al 2003;Bendif et al 2023), can help to identify any further trends that may lead to understanding the biological mechanism (see Figure 6). S16, SI.…”

Gephyrocapsa huxleyi (Emiliania huxleyi) as a model system for coccolithophore biology

“…Gephyrocapsa huxleyi strains show a large variability in gene content (Read et al, 2013). This genomic diversity may be driven in part by the loss of genes associated with the haploid life cycle phase in many environmental G. huxleyi isolates (Bendif et al, 2023;von Dassow et al, 2015). Recent construction of phylogenies using genome-wide single-nucleotide polymorphisms have revealed three distinct clades within the G. huxleyi supercomplex that likely represent distinct species (Bendif et al, 2023).…”

“…This genomic diversity may be driven in part by the loss of genes associated with the haploid life cycle phase in many environmental G. huxleyi isolates (Bendif et al, 2023;von Dassow et al, 2015). Recent construction of phylogenies using genome-wide single-nucleotide polymorphisms have revealed three distinct clades within the G. huxleyi supercomplex that likely represent distinct species (Bendif et al, 2023). The phylogenies of nuclear, chloroplast, and mitochondrial genes exhibit significant incongruence, pointing to a convoluted inheritance of organellar genomes during introgressive hybridization between these diverging lineages (Bendif et al, 2015;Kao et al, 2022).…”

“…The vast majority of laboratory research into coccolithophore biology has involved two species, Emiliania huxleyi and Chrysotila (formerly Pleurochrysis ) carterae . Recent phylogenetic studies have placed Emiliania within Gephyrocapsa (Bendif et al., 2023; Filatov et al., 2021), and so we will refer to this species as Gephyrocapsa huxleyi in the text below.…”