Limits to the cellular control of sequestered cryptophyte prey in the marine ciliate Mesodinium rubrum


The marine ciliate Mesodinium rubrum is famous for its ability to acquire and exploit chloroplasts and other cell organelles from some cryptophyte algal species. We sequenced genomes and transcriptomes of free-swimming Teleaulax amphioxeia, as well as well-fed and starved M. rubrum in order to understand cellular processes upon sequestration under different prey and light conditions. From its prey, the ciliate acquires the ability to photosynthesize as well as the potential to metabolize several essential compounds including lysine, glycan, and vitamins that elucidate its specific prey dependency. M. rubrum does not express photosynthesis-related genes itself, but elicits considerable transcriptional control of the acquired cryptophyte organelles. This control is limited as light-dependent transcriptional changes found in free-swimming T. amphioxeia got lost after sequestration. We found strong transcriptional rewiring of the cryptophyte nucleus upon sequestration, where 35% of the T. amphioxeia genes were significantly differentially expressed within well-fed M. rubrum. Qualitatively, 68% of all genes expressed within well-fed M. rubrum originated from T. amphioxeia. Quantitatively, these genes contributed up to 48% to the global transcriptome in well-fed M. rubrum and down to 11% in starved M. rubrum. This tertiary endosymbiosis system functions for several weeks, when deprived of prey. After this point in time, the ciliate dies if not supplied with fresh prey cells. M. rubrum represents one evolutionary way of acquiring photosystems from its algal prey, and might represent a step on the evolutionary way towards a permanent tertiary endosymbiosis.

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Fig. 1: Light micrographs of Teleaulax amphioxeia and Mesodinium rubrum with corresponding cartoons.
Fig. 2: Workflow and transcriptome features of Teleaulax amphioxeia and Mesodinium rubrum.
Fig. 3: Global transcriptome features of M. rubrum.
Fig. 4: Changes in gene expression of Teleaulax amphioxeia genes in response to sequestration.
Fig. 5: Changes in light- and time-controlled gene expression of free-swimming T. amphioxeia and after sequestration by M. rubrum.
Fig. 6: Transcriptional changes in M. rubrum upon sequestration in different light conditions.

Data availability

The raw sequencing reads produced in this study are deposited in the CNGB Nucleotide Sequence Archive (CNSA) [62, 63] with accession number CNP0000925. The nucleotide sequences and functional annotations of the reference gene sets for Teleaulax amphioxeia and Mesodinium rubrum are deposited in the figshare repository under the link 10.6084/m9.figshare.12360836.


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This project was supported by the Danish Council for Independent Research (Grant number 4181–00484 to PJH), the Major scientific and technological projects of Hainan Province (ZDKJ2019011), the National Key Research and Development Program of China (2018YFC0308401), and the Carlsberg Foundation (2012_01_0515 to LG-C). We acknowledge the China National GeneBank (CNGB) for support with computing resources.

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PJH, NL, UJ, and AA conceived the work. AA, KD, MK, and LG-C did the culturing; AA and LG-C extracted RNA; QL, YZ, and XZ did the sequencing; HC, AA, and QL analyzed the data under the supervision of SL and NL; AA, HC, and QL drafted the manuscript. All authors contributed to writing of the final version of the manuscript.

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Correspondence to Shuaicheng Li or Nina Lundholm.

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Altenburger, A., Cai, H., Li, Q. et al. Limits to the cellular control of sequestered cryptophyte prey in the marine ciliate Mesodinium rubrum. ISME J (2020).

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