Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid

Abstract

Euglena spp. are phototrophic flagellates with considerable ecological presence and impact. Euglena gracilis harbours secondary green plastids, but an incompletely characterised proteome precludes accurate understanding of both plastid function and evolutionary history.Using subcellular fractionation, an improved sequence database and MS we determined the composition, evolutionary relationships and hence predicted functions of the E. gracilis plastid proteome.We confidently identified 1345 distinct plastid protein groups and found that at least 100 proteins represent horizontal acquisitions from organisms other than green algae or prokaryotes. Metabolic reconstruction confirmed previously studied/predicted enzymes/pathways and provided evidence for multiple unusual features, including uncoupling of carotenoid and phytol metabolism, a limited role in amino acid metabolism, and dual sets of the SUF pathway for FeS cluster assembly, one of which was acquired by lateral gene transfer from Chlamydiae. Plastid paralogues of trafficking-associated proteins potentially mediating fusion of transport vesicles with the outermost plastid membrane were identified, together with derlin-related proteins, potential translocases across the middle membrane, and an extremely simplified TIC complex.The Euglena plastid, as the product of many genomes, combines novel and conserved features of metabolism and transport.

Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa

“…of the mitochondria proteome [28], while not recognized as the plastid-localized protein [42]. These results consistently suggest that the POP_e1 homologs found in this study are mitochondrionlocalized.…”

“…On the other hand, neither SignalP [40] nor TMHMM [41] predicted the N-terminal amino acid sequence of Euglena gracilis POP_e1 as a typical plastid targeting signal (PTS). Importantly, POP_e1 was detected as a part of the mitochondria proteome [28], while not recognized as the plastid-localized protein [42]. These results consistently suggest that the POP_e1 homologs found in this study are mitochondrion-localized.…”

“…Likewise, no PTS was predicted at the N-terminus of Euglena gracilis POP_e2. Indeed, Euglena gracilis POP_e2 was recognized as neither a mitochondrial nor plastid protein in the proteomic studies [42]. Thus, we conclude that the POP_e2 homologs are localized in the cytosol.…”

Evolution of metabolic capabilities and molecular features of diplonemids, kinetoplastids, and euglenids

“…They include bacteriovorous (e.g., Petalomonas), eukaryovorous (e.g., Peranema), osmotrophic (e.g., Rhabdomonas), and photosynthetic lineages (e.g., Euglena) [8]. The latter acquired a secondary plastid of green algal origin [9] and some interesting functional differences from other plastids [10]. Although several high-coverage transcriptomic datasets have become available recently [11][12][13][14], obtaining chromosome-level assemblies for these organisms is complicated by large sizes of their genomes [15].…”

Catalase and Ascorbate Peroxidase in Euglenozoan Protists

“…The corresponding APX contains two homologous catalytic domains, forming an intramolecular dimeric structure and a class II plastid-targeting bipartite sequence [48]. Previously, the APX activity was demonstrated to be cytosolic [48], which is most likely an artifact of the procedure, given the presence of the encoded targeting sequence and recent proteomic evidence [49]. We propose that the high APX activity in E. gracilis, comparable with that in plant plastids [35], mainly mitigates photosynthetic ROS production in plastids, rather than amends the absence of CAT.…”