Hidden diversity in the oomycete genus Olpidiopsis is a potential hazard to red algal cultivation and conservation worldwide

ABSTRACT

Marine species of the oomycete genus Olpidiopsis that infect cultivated red macroalgae, most notably Pyropia spp., are one of the main causes of economic loss in the Asian seaweed industry. We recently described novel Olpidiopsis species infecting red algae in Scotland, and thus hypothesized that this genus is more abundant and widespread than previously recognized.

Here, we show that the eukaryotic microbiome of macroscopically healthy Porphyra umbilicalis thalli frequently contains marker genes closely related to Olpidiopsis. Thanks to a custom pipeline that allows for de novo OTU and biogeography discovery, and the recovery of precomputed OTUs from large-scale metabarcoding campaigns, we unveil more than 20 unknown Olpidiopsis taxa with a worldwide distribution. Additionally, laboratory-controlled cross-infection experiments show that a Scottish variety of O. porphyrae is virulent on the most commonly cultivated Pyropia yezoensis cultivar in Korea and that conversely, a Korean strain of O. porphyrae successfully infects wild Bangia sp. strains isolated from Scotland. These results provide proof-of-concept that a native Olpidiopsis pathogen may threaten an introduced crop or that an Olpidiopsis pathogen potentially introduced alongside a non-native crop might cross-infect a native European alga.

Thus, we draw parallels with several current biosecurity crises, where major risks to native floras and faunas, as well as crops, are caused by the inadvertent introduction of poorly known pathogens through the agricultural and horticultural trades. Therefore, we express concern that the rapid growth of algal cultivation worldwide, linked to international movement of seaweed seed and the absence of biosecurity monitoring or reulation pertaining to this trade, potentially lays the ground for grave ecological and economic crises in the marine environment.

KEYWORDS:

• Algal disease
• aquaculture
• biosecurity
• metabarcoding
• Olpidiopsis
• Oomycete
• Rhodophyta

Acknowledgements

We are grateful to Juliet Brodie (National History Museum, London, UK), Helena Abreu (ALGAPlus, Ílhavo, Portugal) and Susan Brawley (University of Maine, Orono, USA) for collection of wild P. umbilicalis blades. We would like to acknowledge the contribution of the Marine Microbes consortium in the generation of data used in this publication.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary information

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2019.1664769

Supplementary notes S1. MOULINETTE Pipeline – usage and script

Supplementary notes S2. MOULINETTE Pipeline – commentary

Supplementary notes S3. Fasta sequences of all Olpidiopsis OTUs gathered in this study.

Supplementary table S1. Detailed information for Olpidiopsis sequences and bibliographic records.

Supplementary table S2. Summary table of all metabarcoding datasets/campaigns processed in this study.

Supplementary table S3. OTUs calling and abundance in all sampled P. umbilicalis blade (Pumb iTag V4 Data).

Supplementary table S4. MOULINETTE – Run Information for each of the 1127 SRA runs processed.

Supplementary table S5. MOULINETTE - Per-read blast scores for best matching SRA-OTUs and reciprocal best hit in the nr Database.

Supplementary table S6. MOULINETTE - SRA-OTUs retrieved by the pipeline, with corresponding reads and SRA run numbers.

Supplementary table S7. MOULINETTE - Biogeography data for each SRA-OTUs.

Supplementary fig. S1. 18S Phylogenetic tree featuring v9 barcodes gathered in this study.

Supplementary figs S2–S13. Biogeography of individual OTUs detected by the MOULINETTE pipeline.

Author contributions

C.M.M. Gachon, G.H. Kim, M. Ostrowski, Y. Badis and T.A. Klochkova designed the experiments; C.M.M. Gachon and G.H. Kim supervised the research; Y. Badis, C.M.M. Gachon and J. Brakel conducted the fieldwork; Y. Badis, T.A. Klochkova, J. Brakel and P. Arce conducted the laboratory work; S.G. Tringe designed and conducted the metabarcoding of P. umbilicalis; Y. Badis designed code, conducted data analysis and drafted the initial manuscript; Y. Badis and C.M.M. Gachon finalized the manuscript with contributions from all co-authors. All authors gave final approval for publication.

Additional information

Funding

This work was supported through the UK NERC IOF Pump-priming + scheme (NE/L013223/1 – YB/CMMG), the European Union’s Horizon 2020 research and innovation (ALFF No 642575; EMBRIC No 654008 – CMMG) and a UKRI GCRF award (GlobalSeaweed-STAR, BB/P027806/1 to JB and CMMG). This work was partially supported by a National Research Foundation of Korea Grant (NRF-2015M1A5A1041804) funded to GHK. Metabarcoding of P. umbilicalis was performed in the frame of the Porphyra Research Coordination Network (NSF RCN 0741907). Sequencing and analysis were performed under the Community Science Program, CSP-926, and used resources at the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility supported under Contract No. DE-AC02-05CH11231. The Marine Microbes project was supported by funding from Bioplatforms Australia through the Australian Government National Collaborative Research Infrastructure Strategy (NCRIS) in partnership with the Australian research community.