Abstract
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 Pteridomonas danica (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 (rbcL). The presence of rbcL without photosynthetic activity suggests that investigating the function of plastids in Pteridomonas 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 Pteridomonas possess highly reduced plastid genomes lacking rbcL gene, in contrast to the previous report. Interestingly, we discovered that all plastid-encoded proteins in Pteridomonas 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 Pteridomonas 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 Pteridomonas spp. for the purpose of providing glutamyl-tRNA, encoded by trnE gene, as a substrate for the heme biosynthesis pathway.
Highlights
Plastids came into existence by endosymbiosis between a cyanobacterium and an ancient eukaryotic host that is currently believed to be the common ancestor of Archaeplastida
In the initial stage of this project, we have established two strains of Pteridomonas spp., strain YPF1301 and strain NY0221. Both strains are closely related to the P. danica investigated in the study presented by Sekiguchi et al (2002), and to the P. danica strain PT, from which transcriptomic data has been obtained in the Marine Microbial Eukaryote Transcriptome Sequencing Project (Keeling et al, 2014) (Figure 1)
As no other contig has been detected as a candidate plastid genome fragment, we conclude that the 55 kb-long DNA covers the almost complete plastid genome of Pteridomonas sp
Summary
Plastids show the punctate distribution in various branches of the eukaryotic tree of life, as they have been laterally transferred through multiple independent secondary and/or higher order endosymbioses (Archibald, 2009; Keeling, 2010) These photosynthetic organisms are capable of efficiently converting solar energy to biochemical energy, which is subsequently utilized for various metabolic processes, such as carbon fixation, amino acid synthesis, nitrogen and sulfur metabolism, carotenoid synthesis, heme and chlorophyll synthesis, and a wide array of other metabolite synthesis pathways (Yasuno and Wada, 2002; Kleffmann et al, 2004; DellaPenna and Pogson, 2006; Hörtensteiner and Kräutler, 2011; Terashima et al, 2011; Przybyla-Toscano et al, 2018). All of the Apicomplexa (one of the main lineages of Alveolata) are descendants of a single ancestor that lost its photosynthetic capabilities, while in other lineages, such as diatoms, cryptophytes, or euglenids, losses of photosynthesis are documented to have occurred more than once in a single genus (Marin et al, 2003; Kamikawa et al, 2015; Salomaki and Kolisko, 2019)
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