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A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells

Nature Microbiology volume 2, pages 1446–1455 (2017)Cite this article

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Abstract

The major difference between viruses and plasmids is the mechanism of transferring their genomic information between host cells. Here, we describe the archaeal plasmid pR1SE from an Antarctic species of haloarchaea that transfers via a mechanism similar to a virus. pR1SE encodes proteins that are found in regularly shaped membrane vesicles, and the vesicles enclose the plasmid DNA. The released vesicles are capable of infecting a plasmid-free strain, which then gains the ability to produce plasmid-containing vesicles. pR1SE can integrate and replicate as part of the host genome, resolve out with fragments of host DNA incorporated or portions of the plasmid left behind, form vesicles and transfer to new hosts. The pR1SE mechanism of transfer of DNA could represent the predecessor of a strategy used by viruses to pass on their genomic DNA and fulfil roles in gene exchange, supporting a strong evolutionary connection between plasmids and viruses.

The discovery of the Archaea and this domain’s numerous sublineages has provided unique insight into the evolution of cellular life1,2,3. By comparison, the evolution of viruses, including their origin and relationship to other extrachromosomal elements (ECEs) and ancestral cellular life4,5, is less certain6. Archaeal viruses can possess morphologies, genomic content and interactions with their hosts that differ from viruses from Bacteria and Eukarya4,7 and therefore enhance the opportunity for researching viral evolution. So far, the majority of archaeal viruses have been sourced from hydrothermal or warm hypersaline environments, and those in the Earth’s dominant, cold biosphere have only just begun to be examined8.

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Fig. 1: Transmission electron micrographs of Hrr. lacusprofundi R1S1 VLPs.
Fig. 2: Plasmid map of pR1SE.
Fig. 3: Functional predictions of pR1SE proteins from region 2 that were detected in PVs.
Fig. 4: pR1SE derivatives in Hrr. lacusprofundi hosts.
Fig. 5: Overview of the PV ‘life cycle’: PV formation and infection, and pR1SE dissemination, integration and resolution.

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Acknowledgements

This work was supported by the Australian Research Council (DP150100244) and the Australian Antarctic Science program (project 4031). S.E. was supported by the EMBO Long-Term Fellowship ALTF 188–2014, which is co-funded by the European Commission (EMBOCOFUND2012, GA-2012-600394) and supported by Marie Curie Actions. Mass spectrometry results were obtained at the Bioanalytical Mass Spectrometry Facility (BMSF) and electron microscopy at the Electron Microscope Unit, both within the Analytical Centre of the University of New South Wales. Subsidized access to the BMSF is acknowledged. The authors thank the PRIDE team and ProteomeXchange for efficiently processing and hosting the mass spectrometry data. The authors thank A. Hancock for providing the image of Rauer 1 Lake, the Landsat Image Mosaic of Antarctica (LIMA) project for making satellite images available, S. Payne and A. Hancock for collecting Antarctic water samples, M. Allen for providing uncharacterized strains of Hrr. lacusprofundi, R. Kuchel for assistance with electron microscopy, D. Baker and I. Anishchanka for attempting structural predictions and T. Williams for comments about the manuscript.

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Authors and Affiliations

  1. School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales, 2052, Australia

    Susanne Erdmann, Bernhard Tschitschko & Ricardo Cavicchioli

  2. Bioanalytical Mass Spectrometry Facility, The University of New South Wales, Sydney, New South Wales, 2052, Australia

    Ling Zhong & Mark J. Raftery

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  1. Susanne Erdmann
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  2. Bernhard Tschitschko
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  5. Ricardo Cavicchioli
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Contributions

S.E. and R.C. conceived and led the study and performed the primary writing of the manuscript. S.E. performed all experimental work related to VLPs and host strains, including discovering the existence of PVs. B.T. assembled DNA sequence data and analysed metagenome data. L.Z. and M.J.R. performed the mass spectrometry. All authors participated in the analysis and interpretation of the data and contributed to the writing of the manuscript.

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Correspondence to Ricardo Cavicchioli.

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Supplementary Information

Supplementary Notes, Supplementary References, Supplementary Figures and Supplementary Tables.

Supplementary Data File 1

pR1SEDL18 contig with annotation

Supplementary Data File 2

All proteins detected in vesicle and membrane preparations.

Supplementary Date File 3

All proteins detected in PVs purified by CsCl gradient centrifugation.

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Erdmann, S., Tschitschko, B., Zhong, L. et al. A plasmid from an Antarctic haloarchaeon uses specialized membrane vesicles to disseminate and infect plasmid-free cells. Nat Microbiol 2, 1446–1455 (2017). https://doi.org/10.1038/s41564-017-0009-2

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