Highly Reduced Plastid Genomes of the Non-photosynthetic Dictyochophyceans Pteridomonas spp. (Ochrophyta, SAR) Are Retained for tRNA-Glu-Based Organellar Heme Biosynthesis

• Published in: Frontiers in plant science Vol. 11; p. 602455
• Main Authors: Kayama, Motoki, Maciszewski, Kacper, Yabuki, Akinori, Miyashita, Hideaki, Karnkowska, Anna, Kamikawa, Ryoma
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 27.11.2020
• Subjects: complex plastid; heme biosynthesis; Ochrophyta; Plant Science; plastid genome; reductive evolution; heme biosynthesis; plastid genome; Ochrophyta; reductive evolution; complex plastid
• ISSN: 1664-462X; 1664-462X
• DOI: 10.3389/fpls.2020.602455

Organisms that have lost their photosynthetic capabilities are present in a variety of eukaryotic lineages, such as plants and disparate algal groups. Most of such non-photosynthetic eukaryotes still carry plastids, as these organelles retain essential biological functions. Most non-photosynthetic plastids possess genomes with varied protein-coding contents. Such remnant plastids are known to be present in the non-photosynthetic, bacteriovorous alga (Dictyochophyceae, Ochrophyta), which, regardless of its obligatory heterotrophic lifestyle, has been reported to retain the typically plastid-encoded gene for ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) large subunit ( ). The presence of without photosynthetic activity suggests that investigating the function of plastids in spp. would likely bring unique insights into understanding the reductive evolution of plastids, their genomes, and plastid functions retained after the loss of photosynthesis. In this study, we demonstrate that two newly established strains of the non-photosynthetic genus possess highly reduced plastid genomes lacking gene, in contrast to the previous report. Interestingly, we discovered that all plastid-encoded proteins in spp. are involved only in housekeeping processes (e.g., transcription, translation and protein degradation), indicating that all metabolite synthesis pathways in their plastids are supported fully by nuclear genome-encoded proteins. Moreover, through an in-depth survey of the available transcriptomic data of another strain of the genus, we detected no candidate sequences for nuclear-encoded, plastid-directed Fe-S cluster assembly pathway proteins, suggesting complete loss of this pathway in the organelle, despite its widespread conservation in non-photosynthetic plastids. Instead, the transcriptome contains plastid-targeted components of heme biosynthesis, glycolysis, and pentose phosphate pathways. The retention of the plastid genomes in spp. is not explained by the Suf-mediated constraint against loss of plastid genomes, previously proposed for Alveolates, as they lack Suf genes. Bearing all these findings in mind, we propose the hypothesis that plastid DNA is retained in spp. for the purpose of providing glutamyl-tRNA, encoded by gene, as a substrate for the heme biosynthesis pathway.