Environmental Breviatea harbour mutualistic Arcobacter epibionts.
Breviatea form a lineage of free living, unicellular protists, distantly related to animals and fungi. This lineage emerged almost one billion years ago, when the oceanic oxygen content was low, and extant Breviatea have evolved or retained an anaerobic lifestyle. 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 infection, but may in the present case act for mutual benefit. Finally, re-investigation of two currently available transcriptomic data sets of other Breviatea 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 mutualism, as shown here for Arcobacter and Breviatea.
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.|Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada.
Emmo
E
Hamann
Symbiosis Department, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.
Harald
H
Gruber-Vodicka
Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada.
Manuel
M
Kleiner
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.|Institute for Genome Research and Systems Biology, Center for Biotechnology, University of Bielefeld, Universitätsstraße 25, 3615 Bielefeld, Germany.
Halina E
HE
Tegetmeyer
Max Planck Institute for Biophysical Chemistry, Am Faßberg 11, 37077 Göttingen, Germany.
Dietmar
D
Riedel
Biogeochemistry Department, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.
Sten
S
Littmann
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.|Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada.
Jianwei
J
Chen
Biogeochemistry Department, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.
Jana
J
Milucka
MARUM Centre for Marine Environmental Sciences, Bibliothekstraße 1, University of Bremen, 28359 Bremen, Germany.
Bernhard
B
Viehweger
MARUM Centre for Marine Environmental Sciences, Bibliothekstraße 1, University of Bremen, 28359 Bremen, Germany.
Kevin W
KW
Becker
Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada.
Xiaoli
X
Dong
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
CW
Stairs
MARUM Centre for Marine Environmental Sciences, Bibliothekstraße 1, University of Bremen, 28359 Bremen, Germany.
Kai-Uwe
KU
Hinrichs
Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA.
Matthew W
MW
Brown
Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, 6299 South Street, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.
Andrew J
AJ
Roger
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.|Department of Geoscience, University of Calgary, Calgary, 2500 University Drive Northwest, Alberta T2N 1N4, Canada.|Institute for Genome Research and Systems Biology, Center for Biotechnology, University of Bielefeld, Universitätsstraße 25, 3615 Bielefeld, Germany.
Marc
M
Strous
D020640:Arcobacter / Q000235:genetics / Q000502:physiology*; D056890:Eukaryota / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D056084:Genetic Fitness; D006859:Hydrogen / Q000378:metabolism*; D006864:Hydrogenase / Q000235:genetics / Q000378:metabolism; D009249:NADP / Q000378:metabolism; D040901:Proteomics; D013559:Symbiosis / Q000235:genetics; D059467:Transcriptome; D014774:Virulence / Q000235:genetics; D037521:Virulence Factors / Q000235:genetics / Q000378:metabolism
D037521:Virulence Factors; D009249:NADP; D006859:Hydrogen; D006864:Hydrogenase