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Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations

MPS-Authors
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Hamann,  Emmo
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Tegetmeyer,  Halina E.
HGF MPG Joint Research Group for Deep Sea Ecology & Technology, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Riedel,  Dietmar
Facility for Electron Microscopy, MPI for biophysical chemistry, Max Planck Society;
Department of Neurobiology, MPI for biophysical chemistry, Max Planck Society;

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Littmann,  Sten
Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Ahmerkamp,  Soeren
Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Chen,  Jianwei
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Hach,  Philipp F.
Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Strous,  Marc
Microbial Fitness Group, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Citation

Hamann, E., Tegetmeyer, H. E., Riedel, D., Littmann, S., Ahmerkamp, S., Chen, J., et al. (2017). Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL, 11(5), 1205-1217. doi:10.1038/ismej.2016.197.


Cite as: https://hdl.handle.net/21.11116/0000-0001-C1C1-A
Abstract
Most anoxic environments are populated by small (<10 mu m) heterotrophic eukaryotes that prey on different microbial community members. How predatory eukaryotes engage in beneficial interactions with other microbes has rarely been investigated so far. Here, we studied an example of such an interaction by cultivating the anerobic marine flagellate, Carpediemonas frisia sp. nov. (supergroup Excavata), with parts of its naturally associated microbiome. This microbiome consisted of so far uncultivated members of the Deltaproteobacteria, Bacteroidetes, Firmicutes, Verrucomicrobia and Nanoarchaeota. Using genome and transcriptome informed metabolic network modeling, we showed that Carpediemonas stimulated prokaryotic growth through the release of predigested biomolecules such as proteins, sugars, organic acids and hydrogen. Transcriptional gene activities suggested niche separation between biopolymer degrading Bacteroidetes, monomer utilizing Firmicutes and Nanoarchaeota and hydrogen oxidizing Deltaproteobacteria. An efficient metabolite exchange between the different community members appeared to be promoted by the formation of multispecies aggregates. Physiological experiments showed that Carpediemonas could also benefit from an association to these aggregates, as it facilitated the removal of inhibiting metabolites and increased the availability of prey bacteria. Taken together, our results provide a framework to understand how predatory microbial eukaryotes engage, across trophic levels, in beneficial interactions with specific prokaryotic populations.