Evolution of Carotenoid and Isoprenoid Biosynthesis in Photosynthetic and Non-photosynthetic Organisms

Sterols and carotenoids are typical representatives of the group of isoprenoid lipids in plants. All isoprenoids are synthesized by condensation of the two active C5-units: dimethylallyl diphosphate, DMAPP, and isopentenyl diphosphate, IPP. Like animals, higher plants form their sterols via the classical cytosolic acetate/mevalonate (MVA) pathway of IPP biosynthesis. Plants as photosynthetic organisms, however possess a second, nonmevalonate pathway for IPP biosynthesis, the DOXP/MEP pathway. The latter operates in the chloroplasts and is responsible for the formation of carotenoids and all other plastidic isoprenoid lipids (phytol, prenylquinones). Although there exists some cooperation between both IPP producing pathways, one can never fully compensate for the other. Thus, in higher plants sterols are primarily made via the MVA pathway and carotenoids via the DOXP pathway. This also applies to several algae groups, such as red algae and Heterokontophyta. In the large and diverging group of 'Green Algae' the situation is more complex. The more advanced evolutionary groups (Charales, Zygnematales) possess, like higher plants, both IPP forming pathways and represent an evolutionary link to these. In contrast, the proper Chlorophyta, often single cell organisms (Chlorella, Scenedesmus, Trebouxia), represent a separate phylum and synthesize sterols and carotenoids via the DOXP pathway whereas the MVA pathway is lost. The common ancestor of both groups, Mesostigma viride, again exhibits both IPP pathways. In the photosynthetic Euglenophyta the situation is inverse, both the sterols and the carotenoids are formed exclusively via the MVA pathway, the DOXP pathway is lost during the secondary endosymbiosis. Also Fungi synthesize sterols and carotenoids via the MVA pathway. Animals possess only the MVA pathway for sterol biosynthesis. In contrast, the malaria parasite Plasmodium and other Apicomplexa have lost the MVA pathway and synthesize their isoprenoids only via the DOXP pathway of their plastid-type apicoplast. In evolutionary terms the DOXP/MEP pathway shows up first in photosynthetic and heterotrophic bacteria , whereas Archaea possess the MVA pathway. The early anoxigenic photosynthetic bacteria (one photosynthetic light reaction) and the later Cyanobacteria (two light reactions and oxigenic photosynthesis) that form a link to the endosymbiontic chloroplasts contain the DOXP/MEP pathway. The latter is also present in many heterotrophic pathogenic bacteria. Some bacteria possess, in addition to the DOXP/MEP pathway, some genes of the MVA pathway that they obtained apparently by lateral gene transfer. A few others have evidently lost the DOXP/MEP pathway and acquired the MVA pathway. Some members of the Streptomycetes, in turn, have both IPP producing routes, one for 'housekeeping' (DOXP/MEP pathway) and the other (MVA pathway) for synthesis of secondary isoprenoid products. When viewing the evolutionary trends it is clear that 1) the two pathways of IPP biosynthesis evolved independently, 2) lateral gene transfer has occurred especially on the bacteria level, 3) primary endosymbiosis has taken place and secondary endosymbiosis partially with differing results, and 4) a loss of the genes of the DOXP pathway took place in some organisms and in others a loss of the genes for the MVA pathway. On the basis of the available evidence an evolutionary view of IPP formation is presented.