Complex Ancestries of Isoprenoid Synthesis in Dinoflagellates

Abstract

Isoprenoid metabolism occupies a central position in the anabolic metabolism of all living cells. In plastid-bearing organisms, two pathways may be present for de novo isoprenoid synthesis, the cytosolic mevalonate pathway (MVA) and nuclear-encoded, plastid-targeted nonmevalonate pathway (DOXP). Using transcriptomic data we find that dinoflagellates apparently make exclusive use of the DOXP pathway. Using phylogenetic analyses of all DOXP genes we inferred the evolutionary origins of DOXP genes in dinoflagellates. Plastid replacements led to a DOXP pathway of multiple evolutionary origins. Dinoflagellates commonly referred to as dinotoms due to their relatively recent acquisition of a diatom plastid, express two completely redundant DOXP pathways. Dinoflagellates with a tertiary plastid of haptophyte origin, by contrast, express a hybrid pathway of dual evolutionary origin. Here, changes in the targeting motif of signal/transit peptide likely allow for targeting the new plastid by the proteins of core isoprenoid metabolism proteins. Parasitic dinoflagellates of the Amoebophyra species complex appear to have lost the DOXP pathway, suggesting that they may rely on their host for sterol synthesis.

Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis

“…In the species with the haptophyte-derived plastids, the endosymbiotic algae are regarded to be fully integrated into the dinoflagellate (host) cells, because no cellular component except the plastid remains, and gene transfer from the endosymbiont genome to the dinoflagellate genome (i.e. endosymbiotic gene transfer or EGT) has been detected (36,(39)(40)(41)(42)(43)(44)(45). In Lepidodinium viride with the green alga-derived plastid, although a nucleus-like structure in the compartment corresponding to the cytoplasm of the endosymbiont alga was reported (31), it is still controversial (see discussion).…”

Phenotypic diversity within two toxic dinoflagellate genera: environmental and transcriptomic studies of species diversity in Alexandrium and Gambierdiscus

“…Dinoflagellates also 'recycle' genetic material to regulate their plastid photosynthetic machinery from multiple sources which sometimes results in the fusion of domains from different organisms into chimeric sequences (Méheust et al, 2016). They also recycle genes for use in different pathways, resulting in at least one documented example of a hybrid metabolic pathway with components from different evolutionary origins (Bentlage, Rogers, Bachvaroff, & Delwiche, 2016). In addition, dinoflagellates frequently are hetero-or mixotrophic, allowing them to encounter more nucleic acids, thereby increasing opportunities for HGT events.…”

Untitled

“…brevis, Karlodinium (Kl.) veneficum, and Lepidodinium chlorophorum are known to possess plastid-related genes, which bear phylogenetic affinities to the orthologous genes in peridinin-containing dinoflagellates (Takishita et al, 2004(Takishita et al, , 2008Minge et al, 2010;Nosenko et al, 2006;Patron et al, 2006;Burki et al, 2014;Bentlage et al, 2016). As the peridinin-containing plastid was most likely established in the ancestral dinoflagellates, it is reasonable to assume that the genes described above have been inherited vertically throughout the dinoflagellate evolution, rather than acquired from the endosymbiont.…”

“…Furthermore, a certain fraction of plastid-related genes was unlikely to be vertically inherited from the ancestral dinoflagellates or endosymbiotically acquired from eukaryotic algae that gave rise to non-canonical plastids (Nosenko et al 2006;Patron et al, 2006;Minge et al, 2010;Burki et al, 2014;Bentlage et al, 2016). In light of previous gene surveys in the Ke.…”

“…Likewise, we are uncertain whether there is an evolutionary consistent pattern in chimerism across multiple plastid-localized metabolic pathways within a noncanonical plastid. Prior to this study, the individual evolutionary origins of enzymes involved in the heme and isopentenyl diphosphate (IPP) biosynthetic pathways in diverse "complex algae," which acquired the plastids through green or red algal endosymbioses, have been characterized (Wilhelm et al, 2006;Cihlář & Füssy et al, 2016;Bentlage et al, 2016), albeit no comparison among their overall patterns has been compared to each other. In this study, we investigate the evolutionary origins of enzymes involved in the biosyntheses of heme and IPP, as well as that of chlorophyll a (Chl a), which links to the two aforementioned pathways, in Ke.…”