Lateral transfer and recompartmentalization of Calvin cycle enzymes of plants and algae

Abstract

Certain Calvin cycle enzymes also function in glycolysis or gluconeogenisis, thus photosynthetic eukaryotes would be predicted to have ancestrally possessed cytosolic homologues of these enzymes derived from the eukaryotic host and plastid homologues from the cyanobacterial endosymbiont. In practice, the evolutionary histories of these enzymes are often more complex. Focusing on eukaryotes with secondary plastids, we have examined the evolution of four such genes: class I and II fructose bisphosphate aldolase (FBA), sedoheptulose bisphosphatase (SBPase), and fructose bisphosphatase (FBPase). We show that previously observed distributions of plastid and cytosolic homologues are not always found in algae with secondary plastids: there is evidence for multiple events of both lateral gene transfer and retargeting to a new cellular compartment for both cytosolic and plastid enzymes of plants and algae. In particular, we show that a clade of class II FBAs spans a greater diversity of eukaryotes that previously recognized and contains both plastid-targeted (Phaeodactylum, Odontella) and cytosolic (ascomycetes, oomycetes, Euglena, and Bigelowiella) forms. Lateral transfer events also gave rise to a subset of plant cytosolic FBA, as well as cytosolic FBPase in Toxoplasma and other coccidian apicomplexa. In contrast, it has recently been suggested that the Trypanosoma FBA and SBPase are derived from a plastid, however, greater taxonomic sampling shows that these enzymes provide no evidence for a plastid-containing ancestor of Trypanosoma. Altogether, the evolutionary histories of the FBA and SBPase/FBPase gene families are complex, including extensive paralogy, lateral transfer, and retargeting between cellular compartments.