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Journal of Applied Phycology

, Volume 31, Issue 2, pp 1239–1250 | Cite as

Novel species of the oomycete Olpidiopsis potentially threaten European red algal cultivation

  • Yacine Badis
  • Tatyana A. Klochkova
  • Martina Strittmatter
  • Andrea Garvetto
  • Pedro Murúa
  • J. Craig Sanderson
  • Gwang Hoon Kim
  • Claire M. M. GachonEmail author
Article

Abstract

The rapid growth of marine macroalgal cultivation amplifies the potential impacts of seaweed diseases. Here, we combine microscopy and molecular analysis to describe two novel European species, Olpidiopsis palmariae and O. muelleri spp. nov., that infect the commercially important red algae Palmaria and Porphyra, respectively. A Scottish variety of Olpidiopsis porphyrae, a devastating pathogen of Pyropia previously thought to be restricted to Japanese seaweed farms, is also described as O. porphyrae var. scotiae. In the light of their destructiveness in Asian farms, together with the global expansion of algal cultivation and pertaining seed trade, Olpidiopsis pathogens should be treated as a serious threat to the sustainability of red algal aquaculture. Our findings call for the documentation of seaweed pathogens and the creation of an international biosecurity framework to limit their spread.

Keywords

Aquaculture Algal disease Algal parasite Barcoding Biosecurity Olpidiopsis Oomycete Rhodophyte 

Notes

Author contributions

CMMG, GHK, YB and TAK designed the experiments; CMMG and GHK supervised the research; YB, CMMG, GHK and JCS conducted the fieldwork; YB, TAK, MS, AG and PM conducted the laboratory work YB and CMMG wrote the manuscript with contributions from all co- authors. All authors gave final approval for publication.

Funding information

This work was financially supported by the UK NERC IOF Pump-priming + scheme (NE/L013223/1 – Y.B./C.M.M.G.), the European Union’s Horizon 2020 research and innovation (ALFF No 642575 – A.G./C.M.M.G; EMBRIC No 654008 – C.M.M.G.), the Genomia fund (HERDIR – M.S), and a MASTS Visiting Fellowship Scheme (J.C.S.). P.M. was funded by Conicyt (BecasChile No. 72130422) for PhD studies at the University of Aberdeen, and by the NERCIOF Pump-priming (scheme NE/L013223/1) for activities at the Scottish Association for Marine Sciences. This work was partially supported by a National Research Foundation of Korea Grant (NRF-2015M1A5A1041804) funded to G.H.K. We are also grateful Duncan Smallman and Philip Kerrison for providing Palmaria specimens.

Supplementary material

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References

  1. Arasaki S (1947) Studies on the rot of Porphyra tenera by a Pythium. J Jap Soc Fish 74–90Google Scholar
  2. Arasaki S (1960) A chytridean parasite on the Porphyra. Bull Jpn Soc Sci Fish 543–548Google Scholar
  3. Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol 57:792–808CrossRefGoogle Scholar
  4. Cottier-Cook EJ, Nagabhatla N, Badis Y, Campbell ML, Chopin T, Dai W, Fang J, He P, Hewitt CL, Kim GH, Huo Y, Zengjie Jiang GK, Li X, Liu F, Liu H, Liu Y, Lu Q, Luo Q, Mao Y, Msuya FE, Rebours C, Shen H, Stentiford GD, Yarish C, Hailong W, Yang X, Zhang J, Zhou Y, Gachon CM (2016) Safeguarding the future of the global seaweed aquaculture industry. United Nations University (INWEH) and Scottish Association for Marine Science Policy Brief. ISBN 978-92-808-6080-1Google Scholar
  5. Craigie JS, Correa JA (1996) Etiology of infectious diseases in cultivated Chondrus crispus (Gigartinales, Rhodophyta). Hydrobiologia 326:97–104CrossRefGoogle Scholar
  6. Dick MW (2001) Straminipilous fungi: systematics of the peronosporomycetes, including accounts of the marine straminipilous protists, the plasmodiophorids, and similar organisms. Springer, Dordrecht, pp 362–366CrossRefGoogle Scholar
  7. Ding H, Ma J (2005) Simultaneous infection by red rot and chytrid diseases in Porphyra yezoensis Ueda. J Appl Phycol 17:51–56CrossRefGoogle Scholar
  8. Fletcher K, Uljevic A, Tsirigoti A, Antolic B, Katsaros C, Nikolic V, van West P, Kupper FC (2015) New record and phylogenetic affinities of the oomycete Olpidiopsis feldmanni infecting Asparagopsis sp. (Rhodophyta). Dis Aquat Org 117:45–57CrossRefGoogle Scholar
  9. Gachon CM, Strittmatter M, Badis Y, Fletcher KI, Van West P, Müller DG (2017) Pathogens of brown algae: culture studies of Anisolpidium ectocarpii and A. rosenvingei reveal that the Anisolpidiales are uniflagellated oomycetes. Eur J Phycol 52:133–148CrossRefGoogle Scholar
  10. Kim GH, Klochkova TA, Lee DJ, Im SH (2016) Chloroplast virus causes green-spot disease in cultivated Pyropia of Korea. Algal Res 17:293–299CrossRefGoogle Scholar
  11. Kim GH, Moon K-H, Kim J-Y, Shim J, Klochkova TA (2014) A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae 29:249–265CrossRefGoogle Scholar
  12. Klochkova TA, Jung S, Kim GH (2017a) Host range and salinity tolerance of Pythium porphyrae may indicate its terrestrial origin. J Appl Phycol 29:371–379CrossRefGoogle Scholar
  13. Klochkova TA, Kwak MS, Kim GH (2017b) A new endoparasite Olpidiopsis heterosiphoniae sp. nov. that infects red algae in Korea. Algal Res 28:264–269CrossRefGoogle Scholar
  14. Klochkova TA, Shin YJ, Moon K-H, Motomura T, Kim GH (2016) New species of unicellular obligate parasite, Olpidiopsis pyropiae sp. nov., that plagues Pyropia sea farms in Korea. J Appl Phycol 28:73–83CrossRefGoogle Scholar
  15. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  16. Kwak MS, Klochkova TA, Jeong S, Kim GH (2017) Olpidiopsis porphyrae var. koreanae, an endemic endoparasite infecting cultivated Pyropia yezoensis in Korea. J Appl Phycol 29:2003–2012CrossRefGoogle Scholar
  17. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320CrossRefGoogle Scholar
  18. Loureiro R, Gachon CM, Rebours C (2015) Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace. New Phytol 206:489–492CrossRefGoogle Scholar
  19. Park CS, Kakinuma M, Amano H (2001) Detection and quantitative analysis of zoospores of Pythium porphyrae, causative organism of red rot disease in Porphyra, by competitive PCR. J Appl Phycol 13:433–441CrossRefGoogle Scholar
  20. Saunders GW, Moore T (2013) [Review] Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28:31–43CrossRefGoogle Scholar
  21. Sekimoto S, Klochkova TA, West JA, Beakes GW, Honda D (2009) Olpidiopsis bostrychiae sp. nov.: an endoparasitic oomycete that infects Bostrychia and other red algae (Rhodophyta). Phycologia 48:460–472CrossRefGoogle Scholar
  22. Sekimoto S, Yokoo K, Kawamura Y, Honda D (2008) Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, straminipiles), a unicellular obligate endoparasite of Bangia and Porphyra spp. (Bangiales, Rhodophyta). Mycol Res 112:361–374CrossRefGoogle Scholar
  23. Stentiford GD, Lightner DV (2011) Cases of White Spot Disease (WSD) in European shrimp farms. Aquaculture 319:302–306CrossRefGoogle Scholar
  24. Stentiford GD, Sritunyalucksana K, Flegel TW, Williams BAP, Withyachumnarnkul B, Itsathitphaisarn O, Bass D (2017) New paradigms to help solve the global aquaculture disease crisis. PLoS Pathog 13:e1006160CrossRefGoogle Scholar
  25. Strittmatter M, Gachon CM, Muller DG, Kleinteich J, Heesch S, Tsirigoti A, Katsaros C, Kostopoulou M, Kupper FC (2013) Intracellular eukaryotic pathogens in brown macroalgae in the Eastern Mediterranean, including LSU rRNA data for the oomycete Eurychasma dicksonii. Dis Aquat Org 104:1–11CrossRefGoogle Scholar
  26. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 9:678–687Google Scholar
  27. West JA, Klochkova TA, Kim GH, Loiseaux-de Goër S (2006) Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: host species susceptibility. Phycol Res 54:72–85CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Yacine Badis
    • 1
  • Tatyana A. Klochkova
    • 2
  • Martina Strittmatter
    • 1
    • 3
  • Andrea Garvetto
    • 1
  • Pedro Murúa
    • 1
    • 4
  • J. Craig Sanderson
    • 5
  • Gwang Hoon Kim
    • 6
  • Claire M. M. Gachon
    • 1
    Email author
  1. 1.The Scottish Association for Marine ScienceScottish Marine InstituteObanUK
  2. 2.Kamchatka State Technical UniversityPetropavlovsk-KamchatskyRussia
  3. 3.Roscoff Biological StationPlace Georges TeissierRoscoffFrance
  4. 4.Aberdeen Oomycete Laboratory, College of Life Sciences and MedicineUniversity of AberdeenAberdeenUK
  5. 5.Institute of Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  6. 6.Department of BiologyKongju National UniversityKongjuSouth Korea

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