Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes

Abstract

The division of life into producers and consumers is blurred by evolution. For example, eukaryotic phototrophs can lose the capacity to photosynthesize, although they may retain vestigial plastids that perform other essential cellular functions. Chrysophyte algae have undergone a particularly large number of photosynthesis losses. Here, we present a plastid genome sequence from a nonphotosynthetic chrysophyte, "Spumella" sp. NIES-1846, and show that it has retained a nearly identical set of plastid-encoded functions as apicomplexan parasites. Our transcriptomic analysis of 12 different photosynthetic and nonphotosynthetic chrysophyte lineages reveals remarkable convergence in the functions of these nonphotosynthetic plastids, along with informative lineage-specific retentions and losses. At one extreme, Cornospumella fuschlensis retains many photosynthesis-associated proteins, although it appears to have lost the reductive pentose phosphate pathway and most plastid amino acid metabolism pathways. At the other extreme, Paraphysomonas lacks plastid-targeted proteins associated with gene expression and all metabolic pathways that require plastidencoded partners, indicating a complete loss of plastid DNA in this genus. Intriguingly, some of the nucleus-encoded proteins that once functioned in the expression of the Paraphysomonas plastid genome have been retained. These proteins were likely to have been dual targeted to the plastid and mitochondria of the chrysophyte ancestor, and are uniquely targeted to the mitochondria in Paraphysomonas. Our comparative analyses provide insights into the process of functional reduction in nonphotosynthetic plastids. heterotrophy | ochrophyte | phylogenomics | dual targeting | protist

A non-photosynthetic green alga illuminates the reductive evolution of plastid electron transport systems

“…In contrast, biosynthetic pathways for certain amino acids and fatty acids are reported to be lost in non-photosynthetic plastids of the chrysophycean “ Spumella ” sp. NIES-1846 bearing only glycolysis and biosynthesis of heme and Fe-S cluster [ 17 ]. The newly discovered sister lineage of red algae, Rhodelphidia, possesses a non-photosynthetic plastid metabolically functioning only for the synthesis of heme and Fe-S clusters [ 18 ].…”

The cryptic plastid of Euglena longa defines a new type of non-photosynthetic plastid organelles

“…E. longa thus joins the group of recently discovered plastid-bearing eukaryotes lacking the MEP pathway, namely the colourless diatom Nitzschia sp. NIES-3581 (Kamikawa et al 2017) and various colourless chrysophytes (Graupner et al 2018; Dorrell et al 2019). In contrast, the plastid-localized MEP pathway in apicomplexans and related alveolates (i.e.…”

“…The loss of plastid-localized fatty acid synthesis in E. longa is not without precedent, as it has been also reported for the apicoplast of Theileria parva (which is fully dependent on fatty acid supply from host), the plastid of Perkinsus marinus (Janouškovec et al 2015) and the chrysophyte “ Spumella ” sp. NIES-1846 (Dorrell et al 2019). Nevertheless, the E. longa plastid has kept plastid-targeted enzymatic steps downstream of fatty acid synthesis.…”

“…Many of them have a similar metabolic capacity as the apicoplast (Sanchez-Puerta et al 2007; Slamovits and Keeling 2008; Fernández Robledo et al 2011), and some house an even more complex metabolism that includes amino acid biosynthesis and carbohydrate metabolism pathways (Borza et al 2005; Pombert et al 2014; Smith and Lee 2014). Until recently, IPP synthesis seemed to be a process conserved even in the most reduced relic plastids, such as the genome-lacking plastids of certain alveolates (Matsuzaki et al 2008; Janouškovec et al 2015), but non-photosynthetic plastids lacking the characteristic plastidial (MEP or DOXP) pathway of IPP biosynthesis are now known (Kamikawa et al 2017; Graupner et al 2018; Dorrell et al 2019). Thus, there is generally a metabolic reason for a plastid retention, although the cases of plastid dependency differ between lineages.…”

The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

“…Nitz4. The need to conserve carbon and NADPH likely drove loss of the isoprenoid-producing MEP from the plastid, which has also been linked to loss of photosynthesis in chrysophytes [91] and euglenophytes [92]. Despite lack of a PPP in the apicoplast [90], P. falciparum has not lost its MEP, presumably because it lacks a cytosolic MVA [93], an alternate source of isoprenoid production.…”