Schizocladia ischiensis organellar genomes: estimating the origin of multicellularity in heterokonts and the emergence of shallow ocean ecosystems

Abstract Background Brown algae are key members of coastal marine ecosystems and the most recent eukaryotic lineage to transition to multicellularity. Browns are members of a heterogeneous assemblage of organisms, heterokonts, that include photosynthetic plankton, (e.g. diatoms) and non-photosynthetic taxa like the pseudofungi or labyrinthulas. We hypothesized that the origin of brown algae would coincide with the assembly of shallow coastal ecosystems. Testing this hypothesis required a robust estimate of the timeframe for the origin of multicellularity in the Gyristan (lineage including Oomycota and Ochrophyta) heterokonts and the diversification of the brown algae. A relaxed clock analysis that included organellar data from the closest sister of brown algae, Schizocladia ischiensis and other heterokonts enabled a robust estimation of this timeframe. Results Consistent with Gyristan heterokonts, the plastid and mitochondrial genomes of S. ischiensis were circular (cp ~138,101 bp, mt ~ 41,773 bp) with similar genes and genome architecture. The comparison of its organellar protein-coding genes with those of other heterokonts (21 cpDNA, 28 mtDNA) including outgroups were used to estimate the following divergence times: (1) The Gyristan assemblage split into autotrophic (Ochrophyta) and heterotrophic (Oomycetes) clades in the Paleozoic (~ 457 Ma) with the transition to multicellularity early in the Mesozoic. (2) Several phytoplankton lineages (e.g., Diatoms) diversified toward the end of the Mesozoic into the Cenozoic consistent with paleontological records and estimated stable oceanic conditions. (3) The brown algae, main architects of key coastal benthic ecosystems, arose toward the end of the Mesozoic with main lineages like the kelps or rockweeds diversifying into the Cenozoic. These divergences were consistent with fossil records and physical data for the emergence of shallow water coastal environments. Conclusions S. ischiensis’ organellar genomes combined with robust multigene phylogenomic molecular clock analyses placed the origin of brown algae late in the Mesozoic consistent to paleontological time estimates and plate tectonic models for the emergence of shallow coastal environments. These data robustly supported the hypothesis that the origin and diversification of brown algae was central to the assembly of rocky shallow coastal ecosystems. Furthermore, important communities like kelps forests or rockweed beds are relatively recent marine ecosystems.