Abstract

Filamentous fungi asymptomatically colonize the inner tissues of macroalgae, yet their ecological roles remain largely underexplored. Here, we tested if metabolites produced by fungal endophytes might protect their host against a phylogenetically broad spectrum of protistan pathogens. Accordingly, the cultivable fungal endophytes of four brown algal species were isolated and identified based on LSU and SSU sequencing. The fungal metabolomes were tested for their ability to reduce the infection by protistan pathogens in the algal model Ectocarpus siliculosus. The most active metabolomes effective against the oomycetes Eurychasma dicksonii and Anisolpidium ectocarpii, and the phytomixid Maullinia ectocarpii were further characterized chemically. Several pyrenocines isolated from Phaeosphaeria sp. AN596H efficiently inhibited the infection by all abovementioned pathogens. Strikingly, these compounds also inhibited the infection of nori (Pyropia yezoensis) against its two most devastating oomycete pathogens, Olpidiopsis pyropiae, and Pythium porphyrae. We thus demonstrate that fungal endophytes associated with brown algae produce bioactive metabolites which might confer protection against pathogen infection. These results highlight the potential of metabolites to finely-tune the outcome of molecular interactions between algae, their endophytes, and protistan pathogens. This also provide proof-of-concept toward the applicability of such metabolites in marine aquaculture to control otherwise untreatable diseases.

Highlights

  • Macroalgae are important ecosystems engineers that contribute significantly to primary production in cold and temperate coastal seas and drive essential functions in nutrient cycling (Dayton, 1985)

  • 99 clonal isolates in total were purified from the 2,100 algae organs segments (Table 1), of which 30 were isolated from L. digitata (10 from Scotland and 20 from France), 17 from S. latissima in Oban, 49 strains from A. nodosum (5 from Scotland and 44 from France), and 3 from P. canaliculata

  • The taxonomic diversity was high but Molecular operational taxonomic units (MOTU) were mostly present as singletons (16 MOTU/17 isolates from S. latissima in Oban, 9 MOTU/10 isolates from L. digitata in Oban, 16 MOTU/20 isolates from L. digitata in Roscoff)

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Summary

Introduction

Macroalgae (seaweed) are important ecosystems engineers that contribute significantly to primary production in cold and temperate coastal seas and drive essential functions in nutrient cycling (Dayton, 1985). Human consumption represents 99% of the global algal market which keeps growing at an annual rate nearing 10% (Food and Agricultural Organization of the United Nations (FAO), 2014). Epiphytic bacterial communities are essential to the morphological development of certain green algae (Wichard et al, 2015) and numerous studies demonstrated the contribution of bacteria to nutrient acquisition or defense by the production of vitamins (Wichard and Beemelmanns, 2018). These multiple interactions led to define macroalgae and their associated microbiota as a “superorganism,” called the holobiont (Egan et al, 2013)

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