The nature of the diatom Leptocylindrus mediterraneus (Bacillariophyceae), host of the enigmatic symbiosis with the stramenopile Solenicola setigera

Abstract:

The consortium between the colonial stramenopile Solenicola setigera and the centric chain-forming diatom Leptocylindrus mediterraneus is cosmopolitan throughout the world ocean yet rarely abundant. However, the nature of the association remains enigmatic. A mutualistic symbiosis requires a live diatom host, but the frustule of L. mediterraneus is apparently empty, lacking protoplasm and plastids. The parasitism requires free-living host cells to be infected, but there is no evidence of populations of the free-living diatom. During experiments attempting to culture the heterotrophic S. setigera, we successfully obtained a strain of the host diatom. In the small-subunit (SSU) rDNA phylogeny, L. mediterraneus was closely related to Dactyliosolen blavyanus and to a new sequence of Dactyliosolen sp. while distantly related to the genus Leptocylindrus. We proposed the reinstatement of L. mediterraneus in the genus Dactyliosolen as D. mediterraneus. Even under optimal growth conditions, the frustule was nearly empty with reduced protoplasm concentrated in the middle. When compared with congeneric species, D. mediterraneus showed a double-layered structure that acts as substrate for Solenicola. The free-living diatom lacked the convex walls that D. mediterraneus showed as host of Solenicola. The diatom in consortium with Solenicola maintained the photosynthetic machinery to eventually proliferate as a free-living organism. The ecological and morphological observations suggested that the diatom was successfully adapted to the mutualistic symbiosis with Solenicola. We discarded a parasitic relationship in this exceptional example of symbiosis.

Key Words::

• Bacillariophyta
• Dactyliosolen
• DNA bar coding
• Epibiosis
• Epibiont
• Molecular phylogenetics
• Phoresy commensalism
• Plankton
• Parasitism
• Rhizomonas
• SSU rDNA
• Symbiont
• Symbioses

ACKNOWLEDGEMENTS

This research is supported by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant numbers BJT 370646/2013–14 to F.G. and 402759/2012–5 and 311936/2013–0 to R.M.L.).