Still Acting Green: Continued Expression of Photosynthetic Genes in the Heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)

Abstract

The loss of photosynthetic function should lead to the cessation of expression and finally loss of photosynthetic genes in the new heterotroph. Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as “kleptoplastids” multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value <e−30) with proteins associated with plastid and photosynthetic function. Most of the genes involved in the Calvin-Benson cycle were found, genes of the light-dependent reaction were also identified. Also genes of associated pathways including the chorismate pathway and genes involved in starch metabolism were discovered. BLAST searches and phylogenetic analysis suggest that these plastid-associated genes originated from several different photosynthetic ancestors. The Calvin-Benson cycle genes are mostly associated with genes derived from the secondary plastids of peridinin-containing dinoflagellates, while the light-harvesting genes are derived from diatoms, or diatoms that are tertiary plastids in other dinoflagellates. The continued expression of many genes involved in photosynthetic pathways indicates that the loss of transcriptional regulation may occur well after plastid loss and could explain the organism's ability to “capture” new plastids (i.e. different secondary endosymbiosis or tertiary symbioses) to renew photosynthetic function.

Microbiomes of Healthy and Bleached Corals During a 2016 Thermal Bleaching Event in the Upper Gulf of Thailand

“…Consistent with this "replacement" hypothesis, our analysis also found increased abundances of unclassified genera in Dinophyceae and Alveolata and genus Navicula in all bleached coral species. We suggest that Dinophyceae and Alveolata could provide photosynthesis (Gómez, 2012;Kim et al, 2013) and the diatom Navicula could replace nitrogen and phosphate recyclings (Kwon et al, 2013), for nutrients in corals that have lost Symbiodinium during a bleaching event. Moreover, the correlation analysis between coral-associated prokaryotic and eukaryotic genera highlighted a uniqueness of Symbiodinium that conferred a positive correlation to the otherwise prokaryotic genera that had negative correlations to other eukaryotic genera.…”

Feeding diverse prey as an excellent strategy of mixotrophic dinoflagellates for global dominance

“…The data on the transcriptome assembly of the kleptoplastidic dinoflagellate P. piscicida and mixotrophic dinoflagellates Y. yeosuensis and Ansanella granifera were obtained from our previous studies (28)(29)(30). Moreover, the transcriptomic sequences of the heterotrophic dinoflagellates Oxyrrhis marina, Noctiluca scintillans, kleptoplastidic dinoflagellate D. acuminata, mixotrophic dinoflagellates Lingulodinium polyedra, Gymnodinium catenatum, A. andersonii, Heterocapsa steinii, and the autotrophic dinoflagellate Pelagodinium bei were obtained from the Marine Microbial Eukaryote Transcriptome Sequencing Project (table S6) (31,32).…”

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

“…ATCC50920, the diatom Nitzschia sp. NIES-3581, and the non-photosynthetic chrysophytes, revealed the presence of a subset of CB enzymes, including ptPGK and ptGAPDH, but not of RuBisCO (Kim et al 2013; Pombert et al 2014; Kamikawa et al 2017; Graupner et al 2018). Hence, the constellation of the CB enzymes retained in the E. longa plastid seems to be unique.…”