Abstract

Breviatea form a lineage of free living, unicellular protists, distantly related to animals and fungi1,2. This lineage emerged almost one billion years ago, when the oceanic oxygen content was low, and extant Breviatea have evolved or retained an anaerobic lifestyle3,4. Here we report the cultivation of Lenisia limosa, gen. et sp. nov., a newly discovered breviate colonized by relatives of animal-associated Arcobacter. Physiological experiments show that the association of L. limosa with Arcobacter is driven by the transfer of hydrogen and is mutualistic, providing benefits to both partners. With whole-genome sequencing and differential proteomics, we show that an experimentally observed fitness gain of L. limosa could be explained by the activity of a so far unknown type of NAD(P)H-accepting hydrogenase, which is expressed in the presence, but not in the absence, of Arcobacter. Differential proteomics further reveal that the presence of Lenisia stimulates expression of known ‘virulence’ factors by Arcobacter. These proteins typically enable colonization of animal cells during infection5, but may in the present case act for mutual benefit. Finally, re-investigation of two currently available transcriptomic data sets of other Breviatea4 reveals the presence and activity of related hydrogen-consuming Arcobacter, indicating that mutualistic interaction between these two groups of microbes might be pervasive. Our results support the notion that molecular mechanisms involved in virulence can also support mutualism6, as shown here for Arcobacter and Breviatea.

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Acknowledgements

We thank T. Hargesheimer, D. Liu, G. Klockgether, P. Hach, R. Appel and I. Kattelmann for technical assistance, A. Simpson, G. Strous and Fulvio Reggiori for comments on electron micrographs, and C. Hubert, E. Ruff, S. Ahmerkamp and N. Dubilier for discussions. This study was supported by European Research Council starting grant MASEM 242635 (M.S., E.H., J.C.), the Campus Alberta Innovation Chair Program (M.S., E.H., X.D.), the Canadian Foundation for Innovation (M.S), the Alberta Small Equipment Grant Program (M.S.), the German Federal State Nordrhein-Westfalen (M.S.), the Max Planck Society, and the Natural Sciences and Engineering Research Council of Canada for a Banting fellowship to M.K. and a Discovery Grant to M.S.

Author information

Affiliations

  1. Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany

    • Emmo Hamann
    • , Halina E. Tegetmeyer
    • , Jianwei Chen
    •  & Marc Strous
  2. Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada

    • Emmo Hamann
    • , Manuel Kleiner
    • , Jianwei Chen
    • , Xiaoli Dong
    •  & Marc Strous
  3. Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany

    • Harald Gruber-Vodicka
  4. Institute for Genome Research and Systems Biology, Center for Biotechnology, University of Bielefeld, Universitätsstraße 25, 3615 Bielefeld, Germany

    • Halina E. Tegetmeyer
    •  & Marc Strous
  5. Max Planck Institute for Biophysical Chemistry, Am Faßberg 11, 37077 Göttingen, Germany

    • Dietmar Riedel
  6. Biogeochemistry Department, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany

    • Sten Littmann
    •  & Jana Milucka
  7. MARUM Centre for Marine Environmental Sciences, Bibliothekstraße 1, University of Bremen, 28359 Bremen, Germany

    • Bernhard Viehweger
    • , Kevin W. Becker
    •  & Kai-Uwe Hinrichs
  8. Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, 6299 South Street, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada

    • Courtney W. Stairs
    •  & Andrew J. Roger
  9. Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA

    • Matthew W. Brown

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Contributions

E.H. and J.C. performed sampling, cultivation and physiological experiments. M.K. performed proteomics and data analysis. D.R. performed transmission electron microscopy. S.L. and E.H. performed scanning electron microscopy. E.H. performed CARD-FISH imaging. H.T. performed next-generation sequencing, H.G.-V. performed read processing, assembly and binning. E.H. performed in silico processing of next-generation sequencing data with assistance from H.G.-V., X.D. and M.S. M.W.B., C.W.S. and A.J.R. analysed sequences for Arcobacter associated with S. tetraspora. E.H., B.V. and K.B performed chemical analysis with input from J.M, K.-U.H. and M.S. The experimental design was developed jointly by M.S., E.H., J.M., M.K. and K.-U.H. E.H. wrote the manuscript with input from all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Emmo Hamann or Marc Strous.

Extended data

Supplementary information

Excel files

  1. 1.

    Supplementary Table 1

    Accession numbers and per gene expression levels as determined with proteomics.

  2. 2.

    Supplementary Table 2

    Calculation of the thermodynamic and kinetic feasibility of hydrogen transfer between L. limosa and Arcobacter.

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Notes regarding the diagnosis of Lenisia limosa gen. et sp. Nov

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DOI

https://doi.org/10.1038/nature18297

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