Seafoams associated with phaeocystis sp. bloom accumulate saprophytic and parasitic microorganisms from terrestrial origin

DOI : 10.54563/asgn.2668

Abstract

The community composition, structure, origin, and trophic functions of eukaryotic microorganisms on seafoam deposits (N = 30) and adjacent seawater (N = 32) were explored at the beach of Wimereux (North of France) during the Phaeocystis globosa spring bloom (March-May 2023), using high throughput sequencing of 18S rRNA marker gene. Our results notably showed that eukaryotic communities trapped in seafoams were different from communities in adjacent seawater. In particular, seafoams were rich in ASVs affiliated to saprobes and parasites compared to seawater, with a terrestrial origin for most of them.

Outline

Text

Context, material and methods

Seafoams, often associated with decaying marine algal blooms, are ubiquitous and increasingly acknowledged as a potential environmental issue (Lancelot 1995, Spilmont et al. 2009, Schilling & Zessner 2011, Peperzak and van Wezel 2023, Das et al. 2024, Seuront et al. 2024, Cazalis-Henry et al. 2025). The composition, structure, origin, and trophic functions of eukaryotes community trapped in seafoams are still, however, largely unexplored (Schilling & Zessner 2011, Das et al. 2024). Yet, such knowledge is essential for assessing the role of foams in the ecosystem functioning of the aquatic environment.

On the seashore of the eastern English Channel and North Sea during the spring bloom of Phaeocystis globosa (Haptophyte), a recurrent phenomenon of massive seafoam accumulation following agitated seawater and crashing waves is well documented (Lancelot 1995, Blaw et al. 2010, Peperzak and van Wezel 2023). Besides unpleasant visuals and odors (Lancelot 1995, Blaw et al. 2010), these seafoam deposits may concentrate pollutants (The Guardian 2023, Castagno 2025), various microorganisms (Schilling & Zessner 2011), and may provoke sediment anoxia (Spilmont et al. 2009). In addition, recent studies have reported that seafoams impair the behavior and metabolism of intertidal gastropods and are avoided by these organisms, which led to the identification of a new taxis, i.e. aphrotaxis, coined from the ancient Greek word aphrós, ‘seafoam’ (Seuront et al. 2024, Cazalis-Henry et al. 2025).

Figure 1

Figure 1

The different steps of the 18S rRNA gene Next Generation Sequencing.
Les différentes étapes du 18S rRNA gene Next Generation Sequencing.
ASV: Amplicon Sequence Variant, DNA: Deoxyribonucleic acid, PCR: Polymerase Chain Reaction.

In this study, we analyzed the community composition of eukaryotic microorganisms using high throughput sequencing of 18S rRNA marker gene on seafoam deposits (N = 30) and adjacent seawater (N = 32) at the beach of Wimereux (North of France) collected over the duration of the phytoplankton spring bloom, i.e. March-May 2023 (Fig. 1). A comparative analysis was performed to investigate differences between seafoam and seawater samples in microbial diversity, community structure, potential microbes origin along a seawater-land gradient, and trophic modes (e.g. autotroph, mixotroph, phagotroph, saprotroph, parasite). The origin and trophic modes were assessed according to available scientific literatures. Samples were also examined by light microscopy (Nikon Eclipse TE2000-S) and scanning electron microscopy (LEO 438 VP).

Results and discussion

Our results notably showed that eukaryotic communities trapped in seafoams were different from communities in adjacent seawater. Indeed, only 10 % of Amplicon Sequence Variants (ASVs, the molecular equivalent of species) were common between the two habitats (Fig. 2A). The result of diversity analysis showed that seafoams accommodate a greater richness of eukaryotic ASVs compared to seawater. These results support the hypothesis that seafoam is a transition habitat and is strongly influenced by interactions with (i) seawater and wave action, (ii) sands during seafoam formation and accumulation, and (iii) the continent under the action of winds, precipitation and animals (Gobet et al. 2012, Whitman et al. 2014, Probandt et al. 2018, Okamoto et al. 2022). In addition, seafoams act as a sticky, sponge-like matrix trapping enormous organic contents.

Figure 2.

Figure 2.

Comparison of eukaryotic communities between seafoam and adjacent seawater.
Comparaison des communautés eukaryotiques dans la mousse marine et l’eau de mer.
A. Venn diagram showing the number of shared and unique ASVs (Amplicon Sequence Variant) among seafoam and seawater; and B&C. The mean proportion (%) in seafoam of the different trophic modes of the eukaryotic ASVs and sources of saprobes and parasites (sea-continent gradient). Comparison between seafoam and seawater: (Mann-Witney test). *p<0.05, **p<0.005, ***p<0.0001.

More importantly, when considering the trophic modes of microorganisms, seafoams have 7-fold more ASVs affiliated to saprobes and parasites (corresponding to 53% of all ASVs, Fig. 2B) compared to seawater. However, considering the predominant land-origin of saprobes and parasites (i.e. associated to trees, lichens, plants including vegetables, soil, human gut and skin, and fresh water; 87% of the total ASVs, Fig. 2C), their viability in the intertidal zone and seafoam remain unknown. Such unknown also apply to about 25% of auto- mixotrophs, including pollen and remains of wild and cultivated terrestrial plants. Interestingly, certain fungi, amoeba, Rhizaria, dinoflagellates, ciliates, pollen, euglenid, chlorophytes and diatoms were present only in seafoams (Fig. 3), which may indicate that seafoam acts as selective filters accumulating species and taxa otherwise present at very low concentration in the bulk phase seawater, hence below the detection limits of our analytical approach.

Figure 3

Figure 3

Example of abundant eukaryotic organisms found exclusively in seafoam deposits on the Wimereux beach.
Exemples d’eucaryotes abondants recensés uniquement dans la mousse déposée sur la plage de Wimereux.
Fungal conidia (A-J) of AAlternaria sp. (Dothideomycetes), B&CAlatospora acuminata and Tetracladium. maxilliforme (Leotiomycetes), DAmniculicola longissima (Dothideomycetes), ECladosporium sp. (Dothideomycetes), FNeopestalotiopsis clavispora (Sordariomycetes), GNeohelicosporium griseum  (Dothideomycetes), H-Ioomycete parasitoids, J: Chytrid-like in the diatom Amphiprora; K: Micractinium pusillum (Trebouxiophyceae, Chlorophyta); L-M: Dinophyceae (L: Sinophysis sp. ; M: Apicoporus glaber), N-Q: Cercozoa (Rhizaria) (N: Cryothecomonas sp. in the diatom Guinardia delicatula, O: Cryomonadida, P: Silicofilosea, and Q: Ebria tripartita); R: naked amoeba (Amoebozoa) ; S: Zoothamnium sp. (Peritrichia, Ciliata); TStrombidium sp. (Oligotrichea, Ciliata); U: Euglenid; V: Chlamydomonas sp. (Chlamydomonadaceae, Chlorophyta) ; W: Pollen grain of Betula_papyrifera (Archaeplastida), and X-AB: the diatoms (Stramenopile, XNavicula perminuta, Y: N. gregaria, Z: N. veneta, AAParlibellus delognei, and ABAttheya armata). Not at scale.

Conclusion

Eukaryotic communities in seafoams are distinct from those in adjacent seawater. Given that seafoams typically occur at the sea-land interface, the seafoam-trapped eukaryotic communities were enriched by organisms originating from land, especially saprobes and parasites. Future studies are needed to investigate their variability as well as their biological activity in a habitat different from the ones they originated from.

Bibliography

Blauw A N., Los F J, Huisman J & Peperzak L (2010).- Nuisance seafoam events and Phaeocystis globosa blooms in Dutch coastal waters analyzed with fuzzy logic. Journal of Marine Systems, 83(3‑4):115‑126.

Castagno P. (2025).- https://portcitydaily.com/local-news/government/2025/03/25/nc-state-researcher-finds-high-pfas-concentrations-in-sea-foam-along-local-beaches/ (USA).

Cazalis-Henry S, Spilmont N, Breton E, Elias F & Seuront L (2025).- Seafoam avoidance is driven by both chemosensory and contact cues and points towards the presence of soft-surface thigmotaxis in the intertidal gastropod Littorina littorea, Journal of Experimental Marine Biology and Ecology 583:152085.

Das R, Chanakya H & Lakshminarayana R (2024).- Insights on foaming in surface waters: A review of current understandings and future directions, Chemical Engineering Journal, 493: 152472,

Gobet A, Böer S I, Huse S M, Van Beusekom J E E, Quince C, Sogin, M L, Boetius A & Ramette A. (2012).- Diversity and dynamics of rare and of resident bacterial populations in coastal sands. The ISME Journal, 6(3); 542‑553.

Lancelot C. (1995).- The mucilage phenomenon in the continental coastal waters of the North Sea. Science of The Total Environment, 165(1‑3): 83‑102

Okamoto N, Keeling P J, Leander B S & Tai V. (2022).- Microbial communities in sandy beaches from the three domains of life differ by microhabitat and intertidal location. Molecular Ecology, 31: 3210–3227.

Peperzak L & van Wezel R (2023).- Human fatalities related to a Phaeocystis harmful algal bloom in the North Sea, Harmful Algae, 130:,102545.

Probandt D, EickhorstT., Ellrott A. et al. (2018).- Microbial life on a sand grain: from bulk sediment to single grains. ISME Journal, 12: 623–633.

Schilling K & Zessner M (2011).- Seafoam in the aquatic environment. Water Research, 45(15), 4355‑4366.

Seuront L, Henry S, Breton E, Spilmont N, & Elias F (2024).- Marine seafoams impede metabolic and behavioural traits in the rough periwinkle Littorina saxatilis. Marine Environmental Research, 197, 106486.

Spilmont N, Denis L, Artigas L F, Caloin F, Courcot L, Créach A, Desroy N, Gevaert F, Hacquebart P, Hubas C, Janquin M-A, Lemoine Y, Luczak C, Migné A, Rauch M & Davoult D (2009).- Impact of the Phaeocystis globosa spring bloom on the intertidal benthic compartment in the eastern English Channel : A synthesis. Marine Pollution Bulletin, 58(1), 55‑63.

Whitman R, Harwood VJ, Edge TA, Nevers M, Byappanahalli M, Vijayavel K, Brandão J, Sadowsky MJ, Alm EW, Crowe A, Ferguson D, Ge Z, Halliday E, Kinzelman J, Kleinheinz G, Przybyla-Kelly K, Staley C, Staley Z & Solo-Gabriele HM (2014).- Microbes in Beach Sands: Integrating Environment, Ecology and Public Health. Reviews in Environmental Science and Bio/technoly (The Netherlands). 13(3): 329-368

Illustrations

  • Figure 1

    Figure 1

    The different steps of the 18S rRNA gene Next Generation Sequencing.
    Les différentes étapes du 18S rRNA gene Next Generation Sequencing.
    ASV: Amplicon Sequence Variant, DNA: Deoxyribonucleic acid, PCR: Polymerase Chain Reaction.

  • Figure 2.

    Figure 2.

    Comparison of eukaryotic communities between seafoam and adjacent seawater.
    Comparaison des communautés eukaryotiques dans la mousse marine et l’eau de mer.
    A. Venn diagram showing the number of shared and unique ASVs (Amplicon Sequence Variant) among seafoam and seawater; and B&C. The mean proportion (%) in seafoam of the different trophic modes of the eukaryotic ASVs and sources of saprobes and parasites (sea-continent gradient). Comparison between seafoam and seawater: (Mann-Witney test). *p<0.05, **p<0.005, ***p<0.0001.

  • Figure 3

    Figure 3

    Example of abundant eukaryotic organisms found exclusively in seafoam deposits on the Wimereux beach.
    Exemples d’eucaryotes abondants recensés uniquement dans la mousse déposée sur la plage de Wimereux.
    Fungal conidia (A-J) of AAlternaria sp. (Dothideomycetes), B&CAlatospora acuminata and Tetracladium. maxilliforme (Leotiomycetes), DAmniculicola longissima (Dothideomycetes), ECladosporium sp. (Dothideomycetes), FNeopestalotiopsis clavispora (Sordariomycetes), GNeohelicosporium griseum  (Dothideomycetes), H-Ioomycete parasitoids, J: Chytrid-like in the diatom Amphiprora; K: Micractinium pusillum (Trebouxiophyceae, Chlorophyta); L-M: Dinophyceae (L: Sinophysis sp. ; M: Apicoporus glaber), N-Q: Cercozoa (Rhizaria) (N: Cryothecomonas sp. in the diatom Guinardia delicatula, O: Cryomonadida, P: Silicofilosea, and Q: Ebria tripartita); R: naked amoeba (Amoebozoa) ; S: Zoothamnium sp. (Peritrichia, Ciliata); TStrombidium sp. (Oligotrichea, Ciliata); U: Euglenid; V: Chlamydomonas sp. (Chlamydomonadaceae, Chlorophyta) ; W: Pollen grain of Betula_papyrifera (Archaeplastida), and X-AB: the diatoms (Stramenopile, XNavicula perminuta, Y: N. gregaria, Z: N. veneta, AAParlibellus delognei, and ABAttheya armata). Not at scale.

References

Electronic reference

Elsa Breton, Sébastien Monchy, Luen-Luen Li, Florence Elias, Lucie Courcot, Gabin Dumaine, Solène Henry, Juliette Michaud, Catherine Rafin, Nicolas Spilmont, Léna Zig and Laurent Seuront, « Seafoams associated with phaeocystis sp. bloom accumulate saprophytic and parasitic microorganisms from terrestrial origin », Annales de la Société Géologique du Nord [Online], 32 | 2025, Online since 30 juin 2025, connection on 14 juillet 2025. URL : http://www.peren-revues.fr/annales-sgn/2668

Authors

Elsa Breton

Univ. Littoral Côte d’Opale, CNRS, Univ. Lille, IRD, UMR 8187 LOG, F-62930 Wimereux, France

Sébastien Monchy

Univ. Littoral Côte d’Opale, CNRS, Univ. Lille, IRD, UMR 8187 LOG, F-62930 Wimereux, France

Luen-Luen Li

Univ. Littoral Côte d’Opale, CNRS, Univ. Lille, IRD, UMR 8187 LOG, F-62930 Wimereux, France

Florence Elias

Laboratoire de Physique et Mécanique des Milieux Hétérogènes, UMR 7636, ESPCI–PSL–Sorbonne Université–Université de Paris Cité, F-75005 Paris, France

Lucie Courcot

Univ. Littoral Côte d’Opale, CNRS, Univ. Lille, IRD, UMR 8187 LOG, F-62930 Wimereux, France

Gabin Dumaine

Univ. Littoral Côte d’Opale, CNRS, Univ. Lille, IRD, UMR 8187 LOG, F-62930 Wimereux, France

Solène Henry

Univ. Lille, CNRS, Univ. Littoral Côte d’Opale, IRD, UMR 8187 LOG, Station Marine de Wimereux, F‐59000 Lille, France

Juliette Michaud

Laboratoire de Physique et Mécanique des Milieux Hétérogènes, UMR 7636, ESPCI–PSL–Sorbonne Université–Université de Paris Cité, F-75005 Paris, France

Catherine Rafin

Univ. Littoral Côte d’Opale, UCEIV, UR 4492, MREI 1, F-59140 Dunkerque, France

Nicolas Spilmont

Univ. Lille, CNRS, Univ. Littoral Côte d’Opale, IRD, UMR 8187 LOG, Station Marine de Wimereux, F‐59000 Lille, France

Léna Zig

Laboratoire Matières et Systèmes Complexes, UMR 7057 MSC, Université de Paris Cité

F-75013 Paris, France

Laurent Seuront

Univ. Lille, CNRS, Univ. Littoral Côte d’Opale, IRD, UMR 8187 LOG, Station Marine de Wimereux, F‐59000 Lille, France ; Department of Marine Resources and Energy, Tokyo University of Marine Science and Technology, Tokyo, Japan ; Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa

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