Daniel Grzebyk

THE ROLE AND EVOLUTION OF SUPEROXIDE DISMUTASES IN ALGAE1

Superoxide dismutases (SOD) catalyze the disproportionation of the potentially destructive superoxide anion radical (O2•−, a byproduct of aerobic metabolism) to molecular oxygen and hydrogen peroxide: 2O2•−+2H+→H2O2+O2. Based on metal cofactors, four known metalloforms of SOD enzymes have been identified: they contain either Fe, Mn, Cu and Zn, or Ni. Orthologs of all metalloforms are present in oxygenic photoautotrophs. The expression of SOD is highly regulated, with specific metalloforms playing an inducible protective role for specific cellular compartments. The various metalloforms of SOD are not distributed equally within either cyanobacteria or eukaryotic algae. Typically, cyanobacteria contain either an NiSOD alone or combinations of Mn and Ni or Fe and Mn metalloforms (CuZn is rare among the cyanobacteria). The bacillariophytes and rhodophytes retain an active MnSOD, whereas the chlorophytes, haptophytes, and embryophytes have either FeSOD or multiple combinations of Fe, Mn, and CuZnSODs. The NiSOD is a relatively novel SOD and has been generally excluded from evolutionary analyses. In both cyanobacteria and chlorophyte algae, the FeSOD metalloform appears to be associated with PSI, where its primary role is most likely to deactivate reactive oxygen produced by the Mehler reaction. The CuZnSOD also appears to be associated with the plastid but is phylogenetically more restricted in its distribution. In eukaryotic algae, SODs are all nuclear encoded and, based on nucleotide sequence, protein structures, and phylogenetic distributions, appear to have unique evolutionary histories arising from the lateral gene transfer of three distinct genes to the nucleus after the endosymbiotic acquisition of mitochondria and plastids. The varied phylogenetic histories and subcellular localizations suggest significantly different selection on these SOD metalloforms after the endosymbiont organelle‐to‐host gene transfer.

THE MESOZOIC RADIATION OF EUKARYOTIC ALGAE: THE PORTABLE PLASTID HYPOTHESIS1

Although all chloroplasts appear to have been derived from a common ancestor, a major schism occurred early in the evolution of eukaryotic algae that gave rise to red and green photoautotrophic lineages. In Paleozoic and earlier times, the fossil record suggests that oceanic eukaryotic phytoplankton were dominated by the green (chl b‐containing) algal line. However, following the end‐Permian extinction, a diverse group of eukaryotic phytoplankton evolved from secondary symbiotic associations in the red (chl c‐containing) line and subsequently rose to ecological prominence. In the contemporary oceans, red eukaryotic phytoplankton taxa continue to dominate marine pelagic food webs, whereas the green line is relegated to comparatively minor ecological and biogeochemical roles. To help elucidate why the oceans are not dominated by green taxa, we analyzed and compared whole plastid genomes in both the red and green lineages. Our results suggest that whereas all algal plastids retain a core set of genes, red plastids retain a complementary set of genes that potentially confer more capacity to autonomously express proteins regulating oxygenic photosynthetic and energy transduction pathways. We hypothesize that specific gene losses in the primary endosymbiotic green plastid reduced its portability for subsequent symbiotic associations. This corollary of the plastid “enslavement” hypothesis may have limited subsequent evolutionary advances in the green lineage while simultaneously providing a competitive advantage to the red lineage.