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BMC Evol Biol. 2017 Apr 11;17(1):98. doi: 10.1186/s12862-017-0930-2.

Tripartite species interaction: eukaryotic hosts suffer more from phage susceptible than from phage resistant bacteria.

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GEOMAR, Helmholtz Centre for Ocean Research, Evolutionary Ecology of Marine Fishes, Düsternbrooker Weg 20, 24105, Kiel, Germany.
GEOMAR, Helmholtz Centre for Ocean Research, Evolutionary Ecology of Marine Fishes, Düsternbrooker Weg 20, 24105, Kiel, Germany.
Present address: Max Planck Institute for Evolutionary Biology, Department of Evolutionary Ecology, August-Thienemann-Straße 2, 24306, Plön, Germany.
Institute of Natural Resource Sciences, Zurich University of Applied Sciences, School of Life Sciences and Facility Management, Campus Grüental, CH-8820, Wädenswil, Switzerland.
Institute for Microbiology and Genetics, Georg-August University Goettingen, Grisebachstr. 8, 37077, Goettingen, Germany.
Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Inhoffenstr. 7B, 38124, Braunschweig, Germany.



Evolutionary shifts in bacterial virulence are often associated with a third biological player, for instance temperate phages, that can act as hyperparasites. By integrating as prophages into the bacterial genome they can contribute accessory genes, which can enhance the fitness of their prokaryotic carrier (lysogenic conversion). Hyperparasitic influence in tripartite biotic interactions has so far been largely neglected in empirical host-parasite studies due to their inherent complexity. Here we experimentally address whether bacterial resistance to phages and bacterial harm to eukaryotic hosts is linked using a natural tri-partite system with bacteria of the genus Vibrio, temperate vibriophages and the pipefish Syngnathus typhle. We induced prophages from all bacterial isolates and constructed a three-fold replicated, fully reciprocal 75 × 75 phage-bacteria infection matrix.


According to their resistance to phages, bacteria could be grouped into three distinct categories: highly susceptible (HS-bacteria), intermediate susceptible (IS-bacteria), and resistant (R-bacteria). We experimentally challenged pipefish with three selected bacterial isolates from each of the three categories and determined the amount of viable Vibrio counts from infected pipefish and the expression of pipefish immune genes. While the amount of viable Vibrio counts did not differ between bacterial groups, we observed a significant difference in relative gene expression between pipefish infected with phage susceptible and phage resistant bacteria.


These findings suggest that bacteria with a phage-susceptible phenotype are more harmful against a eukaryotic host, and support the importance of hyperparasitism and the need for an integrative view across more than two levels when studying host-parasite evolution.


Bacteria-phage infection network; Prophages; Temperate phages; Tripartite interaction; Vibrio

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