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Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum.

ABSTRACT: BACKGROUND: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 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. METHODS:We 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. RESULTS:At 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. CONCLUSIONS:Major 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.

SUBMITTER: Lasek-Nesselquist E

PROVIDER: S-EPMC4609049 | biostudies-literature | 2015 Oct

REPOSITORIES: biostudies-literature

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Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum.

Lasek-Nesselquist Erica E Wisecaver Jennifer H JH Hackett Jeremiah D JD Johnson Matthew D MD

BMC genomics 20151016

<h4>Background</h4>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 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 gen ...[more]

PMID: 26475598

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Project description:The development of Dinophysis populations, producers of diarrhetic shellfish toxins, has been attributed to both abiotic (e.g., water column stratification) and biotic (prey availability) factors. An important process to consider is mixotrophy of the Dinophysis species, which is an intensive feeding of the Mesodinium species for nutrients and a benefit from kleptochloroplasts. During the feeding process, the nutritional status in the environment changes due to the preference of Mesodinium and/or Dinophysis for different nutrients, prey cell debris generated by sloppy feeding, and their degradation by micro-organisms changes. However, there is little knowledge about the role of the bacterial community during the co-occurrence of Mesodinium and Dinophysis and how they directly or indirectly interact with the mixotrophs. In this study, laboratory experiments were performed to characterize the environmental changes including those of the prey present, the bacterial communities, and the ambient dissolved nutrients during the co-occurrence of Mesodinium rubrum and Dinophysis acuminata. The results showed that, during the incubation of the ciliate prey Mesodinium with its predator Dinophysis, available dissolved nitrogen significantly shifted from nitrate to ammonium especially when the population of M. rubrum decayed. Growth phases of Dinophysis and Mesodinium greatly affected the structure and composition of the bacterial community. These changes could be mainly explained by both the changes of the nutrient status and the activity of Dinophysis cells. Dinophysis feeding activity also accelerated the decline of M. rubrum and contamination of cultures with okadaic acid, dinophysistoxin-1, and pectenotoxin-2, but their influence on the prokaryotic communities was limited to the rare taxa (<0.1%) fraction. This suggests that the interaction between D. acuminata and bacteria is species-specific and takes place intracellularly or in the phycosphere. Moreover, a majority of the dominant bacterial taxa in our cultures may also exhibit a metabolic flexibility and, thus, be unaffected taxonomically by changes within the Mesodinium-Dinophysis culture system.

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Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum.

Publications

Insights into transcriptional changes that accompany organelle sequestration from the stolen nucleus of Mesodinium rubrum.

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