Abstract
BackgroundOrganelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is an abundant and broadly distributed photosynthetic marine ciliate that steals organelles from cryptophyte algae, such as Geminigera cryophila. M. rubrum is unique from most other acquired phototrophs because it also steals a functional nucleus that facilitates genetic control of sequestered plastids and other organelles. We analyzed changes in G. cryophila nuclear gene expression and transcript abundance after its incorporation into the cellular architecture of M. rubrum as an initial step towards understanding this complex system.MethodsWe compared Illumina-generated transcriptomes of the cryptophyte Geminigera cryophila as a free-living cell and as a sequestered nucleus in M. rubrum to identify changes in protein abundance and gene expression. After KEGG annotation, proteins were clustered by functional categories, which were evaluated for over- or under-representation in the sequestered nucleus. Similarly, coding sequences were grouped by KEGG categories/pathways, which were then evaluated for over- or under-expression via read count strategies.ResultsAt the time of sampling, the global transcriptome of M. rubrum was dominated (~58–62 %) by transcription from its stolen nucleus. A comparison of transcriptomes from free-living G. cryophila cells to those of the sequestered nucleus revealed a decrease in gene expression and transcript abundance for most functional protein categories within the ciliate. However, genes coding for proteins involved in photosynthesis, oxidative stress reduction, and several other metabolic pathways revealed striking exceptions to this general decline.ConclusionsMajor changes in G. cryophila transcript expression after sequestration by M. rubrum and the ciliate’s success as a photoautotroph imply some level of control or gene regulation by the ciliate and at the very least reflect a degree of coordination between host and foreign organelles. Intriguingly, cryptophyte genes involved in protein transport are significantly under-expressed in M. rubrum, implicating a role for the ciliate’s endomembrane system in targeting cryptophyte proteins to plastid complexes. Collectively, this initial portrait of an acquired transcriptome within a dynamic and ecologically successful ciliate highlights the remarkable cellular and metabolic chimerism of this system.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2052-9) contains supplementary material, which is available to authorized users.
Highlights
Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids
Filtering and annotation BLASTP searches identified 7782 polypeptide sequences as putatively of Geminigera cryophila (KN) origin out of a total of 12,650 proteins called for the Mesodinium rubrum transcriptome
Applying a more stringent cutoff to identifying KN sequences, where only proteins returning a cryptophyte hit with an e-value of 1 × 10−30 or better were considered of KN origin, still resulted in 58 % of the M. rubrum transcriptome as being derived from the stolen nucleus
Summary
Organelle retention is a form of mixotrophy that allows organisms to reap metabolic benefits similar to those of photoautotrophs through capture of algal prey and sequestration of their plastids. Mesodinium rubrum is a globally distributed marine and estuarine mixotrophic ciliate with fully functional acquired cryptophyte organelles that are maintained in a symbiotic-like state (Fig. 1) [3,4,5,6,7]. While these foreign organelles can divide in the ciliate, they are not stable components of the cell and there is no evidence that M. rubrum possesses the genetic machinery necessary to control them. While there is strong evidence that karyoklepty facilitates exploitation of prey organelles, the extent to which the kleptokaryon remains active and contributes to maintaining sequestered organelles is unknown
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