AUTOPHAGY IS A CENTRAL CELLULAR PROCESS IN THE INTERACTION BETWEEN BROWN ALGAE AND PARASITIC WATER MOULDS (OOMYCOTA)

Anisolpidium ectocarpii, an obligate oomycete pathogen of brown algae, was subjected to ultrastructural investigation towards understanding its interaction with the kelp Macrocystis pyrifera at a cellular level. Electron microscopy revealed that successful penetration into the host leads to the development of a walled Anisolpidium syncytium, which in optimal growth conditions fills the entire volume of the cell wall and accumulates lipid globules. Sometimes, and likely because of starvation, the Anisolpidium syncytium shrinks inside the space delimited by the cell wall, conspicuous plasmalemma invaginations appear in the pathogen’s periplasmic space, and some spore initials undergo autophagy, in a response that probably aims to rescue the development of a limited number of pathogen spores. In extreme cases, entirely abortive Anisolpidium syncytia show extensive evidence of uncontrolled autophagy despite the presence of lipid reserves. Besides cell wall reinforcements, infected algal cells exhibit many digestive vacuoles, some of them with Anisolpidium structures. Indeed, in vivo staining with monodansylcadaverin showed that over time, autophagy is induced in both the oomycete and the host. Autophagy, therefore is i) induced by the algal host as a local and possibly systemic defence to mobilise energy required to mount defences, and/or directly kill the intruder; ii) induced by the pathogen to adjust its sporulation to the level of resources it can retrieve from its host. We further hypothesise that iii) both the host and the pathogen may hijack their counterpart’s autophagic process: depending on the winner of the interaction, systemic algal autophagy may provide extra resources to the pathogen, or a last line of defence for the alga to induce the suicide of its parasite. Complementary observations performed on two other oomycetes A. rosenvingei and E. dicksonii and another alga, Pylaiella littoralis, suggest that this response is at least partially conserved with other brown algae and oomycetes.