Intracellular symbiosis of algae with possible involvement of mitochondrial dynamics

Chihong Song,Toshinobu Suzaki,Kazuyoshi Murata

doi:10.1038/s41598-017-01331-0

Chihong Song, Toshinobu Suzaki + Show 1 more

Open Access

https://doi.org/10.1038/s41598-017-01331-0

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Abstract

Algal endosymbiosis is widely present among eukaryotes including many protists and metazoans. However, the mechanisms involved in their interactions between host and symbiont remain unclear. Here, we used electron microscopy and three-dimensional reconstruction analyses to examine the ultrastructural interactions between the symbiotic zoochlorella and the organelles in the host Paramecium bursaria, which is a model system of endosymbiosis. Although in chemically fixed samples the symbiotic algae show no direct structural interactions with the host organelles and the perialgal vacuole membrane (PVM), in cryofixed P. bursaria samples the intimate connections were identified between the host mitochondria and the symbiotic algae via the PVM. The PVM was closely apposed to the cell wall of the symbiotic algae and in some places it showed direct contacts to the host mitochondrial membrane and the cell wall of the symbiotic algae. Further, the PVM-associated mitochondria formed a mitochondrial network and were also connected to host ER. Our observations propose a new endosymbiotic systems between the host eukaryotes and the symbionts where the benefiting symbiosis is performed through intimate interactions and an active structural modification in the host organelles.

Highlights

A number of algae live in cells of protists and invertebrates such as Porifera and Cnidaria[1, 2]
Transmission electron microscopy (TEM) observations of cryofixed samples revealed that the perialgal vacuole membrane (PVM) in P. bursaria was apposed closely to the cell wall of the symbiotic zoochlorella with a constant gap of approximately 20 nm
Preparation of P. bursaria using the conventional chemical fixation method caused an obvious shrinkage of the sample, resulting in detachment of the PVM from the cell wall of the symbiotic zoochlorella

Summary

Introduction

A number of algae live in cells of protists and invertebrates such as Porifera and Cnidaria[1, 2]. Aposymbiotic P. bursaria can be infected artificially with other microorganisms, including Scenedesmus (green algae), several species of yeast, and bacteria[15, 16] In light of these facts, mixotrophic ciliates such as P. bursaria are possible intermediates between producers and consumers. Similar studies demonstrated that intracellular algal cells in metazoa are normally surrounded by a symbiosomal membrane, which is thought to be equivalent to the PVM1–3 These membranes prevent digestion of the symbionts in the host’s cytoplasm and control the mutual exchange of various substances between the two partners[19,20,21,22]. Three-dimensional (3-D) ultrastructural EM analyses of cryofixed samples were employed to examine the structural relationships between the symbiotic zoochlorellae and the host organelles of P. bursaria These experiments revealed for the first time the presence of direct contacts between ER-networked mitochondria in P. bursaria and symbiotic zoochlorella cells through their surrounding PVMs

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