Cryptophyte farming by symbiotic ciliate host detected in situ
- aChinese Academy of Sciences Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;
- bDepartment of Marine Sciences, University of Connecticut, Groton, CT 06340
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Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved September 8, 2016 (received for review July 28, 2016)
Significance
Symbioses between marine plankton species are diverse and widespread both spatially and taxonomically. However, the nature and function of such relationships in natural assemblages are severely underexplored due to technical challenges. Consequently, as an example, the relationship between the ciliate Mesodinium rubrum and its observed cryptophyte endosymbiont is varied and debated, from enslaving chloroplasts to exploiting an organelle complex. Applying environmental transcriptomics and other methods to a natural bloom of M. rubrum revealed an unsuspected relationship, “host farming symbiont,” in which the host helps to transport nutrients from the environment, promotes symbiont cell proliferation, and benefits from the symbiont’s photosynthesis.
Abstract
Protist–alga symbiosis is widespread in the ocean, but its characteristics and function in situ remain largely unexplored. Here we report the symbiosis of the ciliate Mesodinium rubrum with cryptophyte cells during a red-tide bloom in Long Island Sound. In contrast to the current notion that Mesodinium retains cryptophyte chloroplasts or organelles, our multiapproach analyses reveal that in this bloom the endosymbiotic Teleaulax amphioxeia cells were intact and expressing genes of membrane transporters, nucleus-to-cytoplasm RNA transporters, and all major metabolic pathways. Among the most highly expressed were ammonium transporters in both organisms, indicating cooperative acquisition of ammonium as a major N nutrient, and genes for photosynthesis and cell division in the cryptophyte, showing active population proliferation of the endosymbiont. We posit this as a “Mesodinium-farming-Teleaulax” relationship, a model of protist–alga symbiosis worth further investigation by metatranscriptomic technology.
Footnotes
- ↵1To whom correspondence should be addressed. Email: senjie.lin{at}uconn.edu.
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Author contributions: D.Q. and S.L. designed research; D.Q. performed research; D.Q., L.H., and S.L. contributed new reagents/analytic tools; D.Q. analyzed data; and D.Q. and S.L. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
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Data deposition: The data reported in this paper have been deposited in the National Center for Biotechnology Information (NCBI) BioProject database (ID code PRJNA340945) and Sequence Read Archive (accession no. SRR4098290).
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This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1612483113/-/DCSupplemental.
Freely available online through the PNAS open access option.
