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Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A

An Erratum to this article was published on 23 January 2017

Abstract

Nitrogen fixation — the reduction of dinitrogen (N2) gas to biologically available nitrogen (N) — is an important source of N for terrestrial and aquatic ecosystems. In terrestrial environments, N2-fixing symbioses involve multicellular plants, but in the marine environment these symbioses occur with unicellular planktonic algae. An unusual symbiosis between an uncultivated unicellular cyanobacterium (UCYN-A) and a haptophyte picoplankton alga was recently discovered in oligotrophic oceans. UCYN-A has a highly reduced genome, and exchanges fixed N for fixed carbon with its host. This symbiosis bears some resemblance to symbioses found in freshwater ecosystems. UCYN-A shares many core genes with the ‘spheroid bodies’ of Epithemia turgida and the endosymbionts of the amoeba Paulinella chromatophora. UCYN-A is widely distributed, and has diversified into a number of sublineages that could be ecotypes. Many questions remain regarding the physical and genetic mechanisms of the association, but UCYN-A is an intriguing model for contemplating the evolution of N2-fixing organelles.

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Figure 1
Figure 2: Phylogenetic trees showing the evolutionary relationship between UCYN-A and other cyanobacteria, as well as the microdiversity of UCYN-A and known UCYN-A hosts.
Figure 3: Methods used to discover the UCYN-A unicellular symbiosis.
Figure 4: Visualizations of UCYN-A from key observations between 2012–2016 using a variety of techniques.
Figure 5: Protein comparisons across genomes of UCYN-A1, the Paulinella chromatophore and the E. turgida spheroid body.
Figure 6: Schematic depictions of plastid evolution and cellular structures in the Paulinella and E. turgida symbiotic associations, and the potential symbiotic interactions in UCYN-A.

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Acknowledgements

We thank J. Magasin for bioinformatics assistance and the personnel of the Hawaiian Ocean Time Series program. This work supported in part by a grant from the Simons Foundation (SCOPE Award ID 329108, J.P.Z.), and the NSF Center for Microbial Oceanography: Research and Education (C-MORE, DBI no. 0424599). M.M.M. is supported by a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme. H.M.F. is supported by the Swedish Research Council VR 637-2013-7502.

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J.P.Z. conceptualized and drafted the manuscript. I.N.S. performed genome comparisons and prepared accompanying figure. M.M.M. compiled photomicrographs, and prepared conceptual figures. K.T.K. performed phylogenetic analysis and prepared accompanying figure. J.P.Z., I.N.S., H.M.F., M.M.M. and K.T.K. drafted and edited the manuscript and figures. All authors read and approved the final manuscript.

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Correspondence to Jonathan P. Zehr.

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Zehr, J., Shilova, I., Farnelid, H. et al. Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A. Nat Microbiol 2, 16214 (2017). https://doi.org/10.1038/nmicrobiol.2016.214

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