The evolution of organellar metabolism in unicellular eukaryotes

Abstract

Metabolic innovation has facilitated the radiation of microbes into almost every niche environment on the Earth, and over geological time scales transformed the planet on which we live. A notable example of innovation is the evolution of oxygenic photosynthesis which was a prelude to the gradual transformation of an anoxic Earth into a world with oxygenated oceans and an oxygen-rich atmosphere capable of supporting complex multicellular organisms. The influence of microbial innovation on the Earth's history and the timing of pivotal events have been addressed in other recent themed editions of Philosophical Transactions of Royal Society B (Cavalier-Smith et al. 2006; Bendall et al. 2008). In this issue, our contributors provide a timely history of metabolic innovation and adaptation within unicellular eukaryotes. In eukaryotes, diverse metabolic portfolios are compartmentalized across multiple membrane-bounded compartments (or organelles). However, as a consequence of pathway retargeting, organelle degeneration or novel endosymbiotic associations, the metabolic repertoires of protists often differ extensively from classic textbook descriptions of intermediary metabolism. These differences are often important in the context of niche adaptation or the structure of microbial communities. Fundamentally interesting in its own right, the biochemical, cell biological and phylogenomic investigation of organellar metabolism also has wider relevance. For instance, in some pathogens, notably those causing some of the most significant tropical diseases, including malaria, unusual organellar metabolism provides important new drug targets. Moreover, the study of organellar metabolism in protists continues to provide critical insight into our understanding of eukaryotic evolution.

Figure 1.

Eukaryotic phylogeny and diverse organellar metabolism. (a) Relationships between eukaryotic supergroups (note: the animals, choanoflagellates, icthyosporeans and fungi are collectively known as the opisthokonts). Likely relationships within supergroups of the key groups discussed in many of the articles published in this themed edition are also shown. These putative relationships represent consensus views of recent datasets (Embley & Martin 2006; Rodriguez-Ezpeleta et al. 2007; Burki et al. 2008; Lee et al. 2008; Hampl et al. 2009; Roger & Simpson 2009). (b) Some of the key taxa discussed in articles published in this theme are stated. The symbols give some indication as to the unusual organellar metabolism that is covered elsewhere in this issue. Black circles and hexagons with white interiors denote non-photosynthetic plastids of either primary or secondary origin, respectively. Taxa drawn beneath lines (e.g. Cryptosporidium) represent basal or early-diverging taxa within the stated group. Chromera velia is shown as the closest known relative to the Apicomplexa, although it is not included within this phylum (Moore et al. 2008). Purple circle, mitochondria-like organelles/hydrogenosomes; pink circle, mitosomes; black circle, 1° plastid; red hexagon, 2° red plastid; green hexagon, 2° green plastid; yellow hexagon, 3° plastid; black star, plastid loss; blue star, peroxisome loss; orange hexagons, discussed in the context of an unusual endosymbiotic relationship.