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New three-way symbiosis: an eukaryotic alga, a blue mussel, and an endolithic cyanobacteria

Abstract

In several parts of the world, mytilid mussels, Mytilus spp., are infected with pathogenic, single-celled, photosynthetic algae belonging to the genus Coccomyxa. The posterior shell edge of heavily infected mussels becomes considerably thickened with an extra shell material. Also, the external shell surface is usually eroded as a result of the microboring activity of endolithic cyanobacteria. We compared the number of bioeroded shells, the bioerosion degree, and the number of badly eroded shells, in uninfected and Coccomyxa-infected Mytilus spp. from the Lower St. Lawrence Estuary, Québec, Canada. The thickness of prismatic and nacreous layers was measured. The epibionts (pink calcareous algae, crustose brown algae, and barnacles) which encrusted surface of studied shells, were counted. Epibionts did not occur frequently and their possible relationship with the partners of a three-way symbiosis, Coccomyxa sp. – Mytilus spp. – endolithic cyanobacteria, has been neglected. We suggest that the mussel provides the alga Coccomyxa a protected space and metabolic carbon for photosynthesis. The alga stimulates shell thickening, and this protects mussel against ocean acidification and predators. The endolithic cyanobacteria remove black-colored periostracum providing the mussel and alga with an increased ability to survive during sunny days when exposed at low tide. The eroded shells become more translucent which encourages alga photosynthesis. However, shell degradation caused by endolithic cyanobacteria is a possible reason for the death of the Coccomyxa-infected mussels at the studied sites.

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References

  • Darienko T, Gustavs L, Eggert A, Wolf W, Pröschold T (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA bar-coding with further implications for the species identification in environmental samples. PLoS One 10:e0127838. https://doi.org/10.1371/journal.pone.0127838

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Fitzer SC, Vittert L, Bowman A, Kamenos NA, Phoenix VR, Cusack M (2015) Ocean acidification and temperature increase impact mussel shell shape and thickness: problematic for protection? Ecol Evol 21:4875–4884

    Article  Google Scholar 

  • Gehman A-LM, Harley CDG (2019) Symbiotic endolithic microbes alter host morphology and reduce host vulnerability to high environmental temperatures. Ecosphere 10(4):e02683. https://doi.org/10.1002/ecs2.2683

    Article  Google Scholar 

  • Kaehler S, McQuaid CD (1999) Lethal and sub-lethal effects of phototrophic endoliths attacking the shell of the intertidal mussel Perna perna. Mar Biol 135:497–503

    Article  Google Scholar 

  • Laihonen P, Furman ER (1986) The site of settlement indicates commensalism between bluemussel and its epibiont. Oecologia (Berlin) 71:38–40

    CAS  Article  Google Scholar 

  • Leclerc R (1987) Guide d’identification des algues marines de l’estuaire du Saint-Laurent, ed. Groupe d’animation en sciences naturelles du Québec, 180 p

  • Mortensen S, Harkestad LS, Stene R-O, Renault T (2005) Picoeucaryot alga infecting blue mussel Mytilus edulis in southern Norway. Dis Aquat Org 63:25–32

    Article  Google Scholar 

  • Nash TH (2008) Lichen biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ponnudurai R, Heiden SE, Sayavedra L, Hinzke T, Kleiner M, Hentschker C, Felbeck H, Sievert SM, Schlüter R, Becher D, Schweder T, Markert S (2020) Comparative proteomics of related symbiotic mussel species reveals high variability of host–symbiont interactions. ISME J 14:649–656. https://doi.org/10.1038/s41396-019-0517-6

    CAS  Article  PubMed  Google Scholar 

  • Richardson DHS, Jackson Hill D, Smith DC (1968) Lichen physiology. XI. The role of the alga in determining the pattern of carbohydrate movement between lichen symbionts. New Phytol 67:469–486

    CAS  Article  Google Scholar 

  • Rossbach S, Saderne V, Anton A, Duarte CM (2019) Light-dependent calcification in Red Sea giant clam Tridacna maxima. Biogeosciences 16:2635–2650. https://doi.org/10.5194/bg-16-2635-2019

    CAS  Article  Google Scholar 

  • Sokolnikova Y, Magarlamov T, Stenkova A, Kumeiko V (2016) Permanent culture and parasitic impact of the microalga Coccomyxa parasitica, isolated from horse mussel Modiolus kurilensis. J Invetebr Pathol 140:25–34

    Article  Google Scholar 

  • Zardi GI, Nicastro KR, McQuaid CD, Gektidis M (2009) Effects of endolithic parasitism on invasive and indigenous mussels in a variable physical environment. PLoS One 4(8):e6560. https://doi.org/10.1371/journal.pone.0006560

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Zuykov M, Tanaka K, Shirai K, Anderson J, McKindsey CW, Deng Y, Spiers G, Schindler M (2019) New insight into light-enhanced calcification in mytilid mussels, Mytilus sp., infected with photosynthetic algae Coccomyxa sp.: δ13C value and metabolic carbon record in shells. J Exp Mar Biol Ecol 520. https://doi.org/10.1016/j.jembe.2019.151211

  • Zuykov M, Belzile C, Lemaire N, Gosselin M, Dufresne F, Pelletier E (2014) First record of the green microalgae Coccomyxa sp. in blue mussel Mytilus edulis (L.) from the lower St. Lawrence estuary (Québec, Canada). J Invertebr Pathol 120:23–32

    Article  Google Scholar 

  • Zuykov M, Anderson J, Archambault P, Dufresne F, Pelletier E (2018a) Mytilus trossulus and hybrid (M. edulis-M. trossulus) – new hosts organisms for pathogenic microalgae Coccomyxa sp. from the estuary and northwestern gulf of St. Lawrence, Canada. J Invertebr Pathol 153:145–146

    Article  Google Scholar 

  • Zuykov M, Anderson J, Pelletier E (2018b) Does photosynthesis provoke formation of shell deformity in Coccomyxa-infested wild mytilid mussels Mytilus spp.? - a conceptual model and research agenda. J Exp Mar Biol Ecol 505:9–11

    Article  Google Scholar 

  • Zuykov M, Allam B, Gosselin M, Archambault P, Spiers G, Schindler M (2020) First report of signs of infection by Coccomyxa-like algae in wild blue mussels, Mytilus spp., in the Gulf of Maine (USA, Maine). J Fish Dis 00:1–4. https://doi.org/10.1111/jfd.13172

    Article  Google Scholar 

  • Zuykov M, Kolyuchkina G, Spiers G, Gosselin M, Archambault P, Schindler M (2021) Pre-exposure to Cu2+ and CuO NPs leads to infection of caged blue mussels, Mytilus edulis L., by pathogenic microalga: pilot study in the lower St. Lawrence estuary (Québec, Canada). Mar Pollut Bull 166. https://doi.org/10.1016/j.marpolbul.2021.112180

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Acknowledgements

The authors thank Drs. W. Adey and M. Cusson for epibionts identification, T. Goto for assistance with shell section preparation. We appreciate Sidney Pierce’s, David Richardson’s, and two anonymous reviewers support during manuscript revision. MZ was supported by Japan Society for the Promotion of Science (JSPS) Fellowship (PE20004) and the Queen Elizabeth II Graduate Scholarships in Science and Technology (QEII-GSST). MS was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) discovery grant.

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This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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MZ, JA, MG and PA contributed to the study conception and design, and performed the field research; MZ wrote the first version of the manuscript; GK, LZ and KS analyzed the data and worked with the literature; MG, PA and MS administrated the project. All the authors edited the manuscript.

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Correspondence to Michael Zuykov.

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Zuykov, M., Anderson, J., Kolyuchkina, G. et al. New three-way symbiosis: an eukaryotic alga, a blue mussel, and an endolithic cyanobacteria. Symbiosis 84, 163–169 (2021). https://doi.org/10.1007/s13199-021-00777-1

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  • DOI: https://doi.org/10.1007/s13199-021-00777-1

Keywords

  • Symbiosis
  • Blue mussels
  • Photosynthetic algae
  • Endolithic cyanobacteria
  • Bioerosion