Progress, challenges and future directions in marine organic-walled dinoflagellate cyst research: New insights from an international workshop

Abstract

Cysts are resistant life-cycle stages that play a key role in the survival and dispersal of some dinoflagellate species. Given their preservation and fossilisation potential, the organic-walled dinoflagellate cysts have been widely used as bioindicators of past and present environmental conditions. Living cysts are studied extensively due to their roles in bloom initiation, termination, and species adaptation. The use of cysts in various fields such as taxonomy, biogeography, evolution, (palaeo)ecology, and (palaeo)oceanography has expanded significantly in recent years. In this paper, we review recent developments, identify research needs, and outline future directions in marine organic-walled dinoflagellate cyst research based on round-table discussions held during the International Workshop on Dinoflagellate Cysts, which took place from 18 to 21 June 2024 in Vigo (Spain). Key priorities in taxonomy, evolution, and biogeography include the need to continue establishing connections between the cyst and motile forms along with their associated sequences, particularly for Harmful Algal Bloom (HAB) species, and updating reference databases for metabarcoding studies. Emerging molecular techniques, such as metabarcoding, provide complementary information on cyst diversity, distribution, and geographic connectivity, thereby aiding in the monitoring and reconstruction of HAB dynamics. Given the impacts of climate change on biogeographical ranges, cysts could serve as valuable indicators for tracking HAB shifts. Combining multi-omics with morphological methods could offer deeper insights into character evolution and support the construction of the dinoflagellate tree of life. Advances in the biogeochemical analysis of dinoflagellate cyst walls, particularly through the detailed study of dinosporin, are also promising for evolutionary research, as demonstrated by recent methodological advances in Fourier Transform Infrared (FTIR) and Raman spectroscopy. In palaeoceanography and palaeoecology, improving quantitative cyst-based reconstructions requires expanding the database of living cyst assemblages and their relationships with environmental variables, especially in underrepresented regions, notably in the Southern Hemisphere. Despite progress towards standardisation, there remains no universally adopted standardised methods for extracting and concentrating cysts from sediments or for quantifying cysts-essential steps for inter-site comparisons. Additionally, sediment trap studies and field observations of associated plankton are needed to complement surface sediment research and enhance our understanding of species ecology. The emerging field of palaeogenomics is promising as it complements cyst-based research. Finally, the integration of biological and geological studies to address key scientific questions is emphasised. For example, investigating the discrepancy between the accepted geological emergence of dinoflagellates and earlier suggestions from geochemistry, molecular analysis, and re-examination of acritarchs could help resolve the early phylogeny of the group.

Keywords: Dinoflagellate cysts; Ecology; Harmful Algal Blooms (HABs); Late Quaternary; Palaeoceanography; Palaeoclimatology; Palaeoecology; Palaeogenomics; Phylogeny.

Figure 1.

Haplontic life cycle in dinoflagellates. Thin-walled, usually haploid, cysts (pellicle cysts) (A) and thick-walled, usually diploid, cysts (resting cysts) (B) produced by some dinoflagellates. Resting cysts are mostly produced through sexual reproduction (hypnozygotes), involving the fusion of gametes and formation of motile zygotes (planozygotes) as a transitional phase (C). Cyst germination (excystment) generates new haploid vegetative cells, passing through a diploid transition phase called planomeiocyte (D) that undergoes meiosis. 2n=diploid, n=haploid. Adapted from Bravo and Figueroa 2014 (© Bravo and Figueroa, 2014, Towards an Ecological Understanding of Dinoflagellate Cyst Functions, https://doi.org/10.3390/microorganisms2010011, published in Microorganisms, MDPI Open Access Journals, under a CC BY 3.0 license).

Figure 2.

Illustration of the diversity within the genus Spiniferites in modern sediments: Spiniferites ramosus from Vilaine Bay (Bretagne, France) (A); Spiniferites belerius from Locquénolé (Bretagne, France), note trumpet-shaped antapical process (B); Spiniferites bentorii from South China Sea (SHG-CJ-2018), note apical boss (C); Spiniferites hainanensis from Kastela Bay (Croatia), note presence of intergonal processes (D); E. Spiniferites pachydermus from Izmir Bay (Turkey), note specific ornamentation (E); Spiniferites elongatus from offshore Spitzbergen (F). All specimens to scale. All images by Kenneth N. Mertens.

Figure 3.

Methodological approach linking the motile-defined Protoperidinium louisianense to the cyst-defined Trinovantedinium pallidifulvum through an incubation experiment and/or genetic sequences obtained through single-cell/cyst PCR. All images by Kenneth N. Mertens.

Figure 4.

Examples of hypothetical horizontal (A) and vertical (B) cyst profiles in sediments. The horizontal distribution of cysts in surface sediments (contour curves, A) is based on cyst mapping performed by García-Moreiras et al. (2021) on the Portuguese coast, NW Iberia (© 2021 García-Moreiras et al., https://doi.org/10.3389/fmars.2021.699483, published in Frontiers in Marine Science under a CC BY 4.0 license). The vertical distribution (sediment core, B) illustrates a peak of cysts in the subsurface layer (near the oxygenated surface layer), as it is commonly observed in some sediment cores (e.g., Anderson et al., 1982; Keafer et al., 1992). The grey shading within 0–3 cm indicates the recommended depth for counting (living) cysts in surface sediments, and the darker grey the presence of a hypothetical oxygenated surface (mixed) layer.

Figure 5.

Map showing locations of sediment traps that include studies of dinoflagellate cyst assemblages. For color references, see Table 1.

Figure 6.

Proposed sampling strategy using sediment traps (A) and water sampling (B) along a cross-shore transect to study lateral and vertical advection of dinoflagellate cysts. In panel B, similar colors indicate comparable dinoflagellate cyst assemblages: the pink samples indicate that vertical transport predominates over lateral transport, while the blue colour indicates a predominance of lateral transport; at station #3, different types of transport predominate depending on the depth in the water column (yellow, vertical transport; blue, horizontal transport).