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.
Highlights
The genetic outcomes of plastid gain and loss have been actively investigated
Our results show that Pfiesteria piscicida expresses numerous genes involved in metabolic pathways of plastids despite it not having any sub-cellular membranous structure assignable to plastids [29]
The heterogeneous origins of the plastid genes suggest that P. piscicida had experienced multiple endosymbioses, both from a secondary plastid and at least one tertiary endosymbiosis
Summary
The genetic outcomes of plastid gain and loss have been actively investigated. Dinoflagellates together with apicomplexans [1,2,3] and ciliates [4,5] have drawn special attention in terms of plastid evolution. A photosynthetic ancestor postulated for a larger group, the Chromoalveolates [7,8] have been challenged recently [9,10] These results are originally based on the discovery of genes associated with photosynthetic organelles found in some non-photosynthetic lineages (e.g. apicomplexans) [1]. Some dinoflagellates replaced the peridinin-containing plastid with others either from a green alga, cryptophytes, haptophytes or diatoms via tertiary endosymbiosis events or a second secondary endosymbiotic event [13] This unique evolutionary gain and loss and regain of plastids among dinoflagellates [14] and the transfer of genes to the nucleus have lead to plastid-derived genes, mostly genes involved in photosynthesis or other critical plastid functions, from several lineages. These metagenomic conclusions have recently been challenged due to undue care in phylogenetic interpretation [10,16]
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