Abstract
The triose phosphate transporter (TPT) is one of the prerequisites to exchange metabolites between the cytosol and plastids. In this study, we demonstrated that the four plastid TPT homologues in the non-photosynthetic diatom Nitzschia sp. NIES-3581 were highly likely integrated into plastid envelope membranes similar to counterparts in the model photosynthetic diatom Phaeodactylum tricornutum, in terms of target membranes and C-terminal orientations. Three of the four Nitzschia TPT homologues are capable of transporting various metabolites into proteo-liposomes including triose phosphates (TPs) and phosphoenolpyruvate (PEP), the transport substrates sufficient to support the metabolic pathways retained in the non-photosynthetic diatom plastid. Phylogenetic analysis of TPTs and closely related transporter proteins indicated that diatoms and other algae with red alga-derived complex plastids possess only TPT homologues but lack homologues of the glucose 6-phosphate transporter (GPT), xylulose 5-phosphate transporter (XPT), and phosphoenolpyruvate transporter (PPT). Comparative sequence analysis suggests that many TPT homologues of red alga-derived complex plastids potentially have the ability to transport mainly TPs and PEP. TPTs transporting both TPs and PEP highly likely mediate a metabolic crosstalk between a red alga-derived complex plastid and the cytosol in photosynthetic and non-photosynthetic species, which explains the lack of PPTs in all the lineages with red alga-derived complex plastids. The PEP-transporting TPTs might have emerged in an early phase of endosymbiosis between a red alga and a eukaryote host, given the broad distribution of that type of transporters in all branches of red alga-derived complex plastid-bearing lineages, and have probably played a key role in the establishment and retention of a controllable, intracellular metabolic connection in those organisms.
Highlights
The triose phosphate transporter (TPT) is one of the prerequisites to exchange metabolites between the cytosol and plastids
It has been proposed that the TPT homologues in red alga-derived complex plastids originated via endosymbiotic gene transfer (EGT) of a TPT gene provided by the endosymbiotic red alga[18,19]
We demonstrate that NspTPT1, NspTPT2, and NspTPT4a integrated in the artificial liposomes are capable of transporting triose phosphates (TP), phosphoenolpyruvate (PEP), and 3-phosphoglycerate (3-PGA), but seem to be incapable of transporting glucose-6P (G6-P; Table 1)
Summary
The triose phosphate transporter (TPT) is one of the prerequisites to exchange metabolites between the cytosol and plastids. Three of the four Nitzschia TPT homologues are capable of transporting various metabolites into proteo-liposomes including triose phosphates (TPs) and phosphoenolpyruvate (PEP), the transport substrates sufficient to support the metabolic pathways retained in the non-photosynthetic diatom plastid. The GPT homologue of G. sulphuraria is capable of transporting a wide range of sugar phosphates except for phosphorylated glucose and phosphorylated ring sugar moieties[13,17], while the TPT and the PPT of this red alga are capable of transporting DHAP and PEP, respectively, but not 3-PGA17. Substrate-specificity of TPT homologues in those complex plastids was investigated with transporters of non-photosynthetic plastid-derived organelles called apicoplasts in apicomplexan parasites[20] and with photosynthetic plastid membranes (and proteo-liposomes) of a cryptophyte[21]. Substrate transport through proteo-liposome membranes harboring membrane proteins of the cryptophyte Guillardia theta was investigated and indicated TP- and PEP-transport activity[9,21]
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