Abstract
Colpodellids are free-living, predatory flagellates, but their close relationship to photosynthetic chromerids and plastid-bearing apicomplexan parasites suggests they were ancestrally photosynthetic. Colpodellids may therefore retain a cryptic plastid, or they may have lost their plastids entirely, like the apicomplexan Cryptosporidium. To find out, we generated transcriptomic data from Voromonas pontica ATCC 50640 and searched for homologs of genes encoding proteins known to function in the apicoplast, the non-photosynthetic plastid of apicomplexans. We found candidate genes from multiple plastid-associated pathways including iron-sulfur cluster assembly, isoprenoid biosynthesis, and tetrapyrrole biosynthesis, along with a plastid-type phosphate transporter gene. Four of these sequences include the 5′ end of the coding region and are predicted to encode a signal peptide and a transit peptide-like region. This is highly suggestive of targeting to a cryptic plastid. We also performed a taxon-rich phylogenetic analysis of small subunit ribosomal RNA sequences from colpodellids and their relatives, which suggests that photosynthesis was lost more than once in colpodellids, and independently in V. pontica and apicomplexans. Colpodellids therefore represent a valuable source of comparative data for understanding the process of plastid reduction in humanity's most deadly parasite.
Highlights
Most lineages of photosynthetic eukaryotes have nonphotosynthetic members
Voromonas pontica transcriptome Here we report transcriptomic data from the marine, predatory protist V. pontica, the first transcriptomic data reported for any colpodellid
We searched for homologs of experimentally localized apicoplast proteins downloaded from ApiLoc v. 3, and in addition to ALAD previously identified during our pathway search, we found a homolog of the apicoplast triosephosphate transporter
Summary
Most lineages of photosynthetic eukaryotes have nonphotosynthetic members. The best-known examples are parasitic land plants [1,2], but parasitic and heterotrophic green algae and parasitic red algae are known [3,4,5,6,7]. The discovery of Chromera velia and Vitrella brassicaformis, close photosynthetic relatives of apicomplexans whose plastids share characteristics with both apicomplexans and dinoflagellates, has confirmed that apicomplexans and dinoflagellates share a red plastid-bearing photosynthetic ancestor [14,18,19] From this perspective, the other, lesser-known descendants of this ancestor, namely colpodellids, perkinsids, and Oxyrrhis, might be expected to maintain a non-photosynthetic plastid. Two apicomplexan lineages (or possibly one, if gregarines and Cryptosporidium are sister groups [22,23]) have lost the ancestral plastid completely [24,25,26] To date it is unknown whether any colpodellids retain a non-photosynthetic plastid
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