Chemical ecology of plankton parasitism in algae

2.1 What are the plankton parasites?

The classic definition of a parasite is an organism that lives on or within another organism and obtains nutrients at the expense of this host (Poulin 2007). Plankton parasites may be prone to rapid evolution, having short generation times. Their short generation times further imply the potential to generate large population sizes in short time periods, increasing the chances of sexual reproduction and dissemination in the host cells (Kochin et al. 2010). Throughout evolutionary history, plankton have been using cell-to-cell associations during one or more life cycle stages to increase survival and avoid the harsh environmental conditions of nutrient-depleted open waters (Picoche 2022). Phytoplankton and seaweeds utilize photosynthesis to sustain their nutritional needs, rendering them suitable hosts for plankton parasites. Opportunistic microorganisms, such as single-cell eukaryotes (namely protists), can infect algae and feed on their metabolites for growth and reproduction during their life cycle stages, impacting their host’s fitness, metabolism, and associated microbiome (Figure 1). Other microorganisms, such as bacteria and viruses, can also cause infectious diseases and parasitize algae, and are equally important marine pathogens in oceans (Gachon et al. 2010). Parasitic bacteria may inhabit the algal membranes of dinoflagellates such as Alexandrium tamarense and can induce cell wall degradation using β-glucosidase and chitinase (Wang et al. 2010). The most studied pathogens of algae are viruses, which usually have a narrow host range and can control their host populations by infecting the most abundant species (Brussaard 2004).

Figure 1:

Plankton parasites and their diverse effects on their algal hosts. Parasites can influence their host’s growth, fitness, metabolism, and reproduction, leading to symptoms of disease in seaweeds and bloom termination of microalgae due to the death of the population. The herd control of algae maintained by plankton parasites also has a positive outcome, supporting a population equilibrium in aquatic ecosystems.

Among the groups of protists reported as parasites of algae is the clade of Alveolata, which contains the perkinsids, a sister group to dinoflagellates, that can infect algae, bivalves, fishes, and amphibians (Itoïz et al. 2022). Another dinoflagellate group from the Syndiniales, also referred to as marine alveolates, comprises many obligate parasites of phytoplankton. Syndiniales parasites can significantly reduce carbon flux via host cell lysis by increasing the sinking rate of infected hosts or zoospores on particles (Anderson et al. 2023). According to genome sequencing analysis, Syndiniales parasites are critical players in ocean surface waters, including sea-ice environments (Clarke et al. 2019). Syndinian and perkinsid parasites can infect toxic, harmful dinoflagellates, thus accelerating their bloom termination and the succession of algal species (Chambouvet et al. 2008; Jephcott et al. 2016).

The Oomycetes, a stramenopile group once classed as Fungi, are plankton parasites responsible for top-down control of phytoplankton hosts such as diatoms (Hanic et al. 2009). Several oomycete species are obligate biotrophic pathogens, but other members can also use host-jumping to evolve followed by radiation, specialization, and speciation (Thines 2019). These processes are well studied in the terrestrial environment for parasites of plants, but not yet for plankton parasites of algae. Several marine oomycete parasites have been established in cultures as laboratory models, including the specialist Lagenisma coscinodisci that infects the diatom genus Coscinodiscus (Buaya et al. 2019), and the generalist Ectrogella sp. that targets diatoms such as the pennate diatom Licmophora (Garvetto et al. 2020). Remarkably, marine oomycetes are stramenopiles, a heterotrophic sister group of brown algae and diatoms, which are the targeted hosts of these parasites (Thines et al. 2015). These oomycetes possess cellulosic cell walls, contrasting with Fungi and their chitinaceous cell walls (Scholz et al. 2014). Stramenopile parasites have reduced, smaller genomes than their host, possibly due to the simplification and reduction of the genomes during evolution (Wolf and Koonin 2013). Consequently, these parasites might hijack the host biosynthetic machinery to produce metabolites during infection and cellular invasion.

Oomycetes infect macroalgal species and planktonic diatoms and could shift from one host to another (Scholz et al. 2014). This infection strategy is shared by many generalist parasites of algae, such as the perkinsid Parvilucifera that can target multiple dinoflagellate species and therefore can thrive and survive if one host disappears (Garcés et al. 2013a). Generalist plankton parasites usually prefer the most susceptible host available, given that reproductive success depends on their ability to infect a host, and use chemical cues to detect the host’s presence (Garcés et al. 2013b). Parasitic organisms from aquatic environments can also be specialists for single algal species, emerging from long co-evolutionary histories (Anderson and May 1981). Many plankton parasites of phytoplankton can be specialists or generalists, and some are parasitoids, i.e., living at their host’s expense and inducing the death of infected cells (Mills 2009).

The kingdom of Fungi also encompasses unicellular eukaryotes that infect algae. By definition, marine fungi include any fungus repeatedly recovered from marine habitats that can (i) grow and reproduce in marine environments, (ii) form symbiotic relationships with other organisms during their life cycle, or (iii) adapt and evolve at the genetic level or is metabolically active in a marine environment (Rédou et al. 2016). The kingdom of Fungi (Opisthonkonta) includes the chytrids that can infect diatoms in both freshwater (Ibelings et al. 2004) and marine (Gutiérrez et al. 2016) environments. One established model of chytrids is Dinomyces arenysensis, which was isolated from a toxic bloom of Alexandrium minutum (Lepelletier et al. 2014a). The chytrid Dinomyces can infect a wide range of dinoflagellates, with a preference for Alexandrium species under culture conditions (Lepelletier et al. 2014a). Strikingly, chytrids are found in terrestrial soils, where they can live without a host as free-flagellate zoospores thriving on a film of surface water (Shearer et al. 2007). Due to their wide distribution across climatic regions, including freshwater and marine ecotypes, and their potential as generalist opportunistic pathogens, chytrids have been a topic of rising interest in recent years (Frenken et al. 2017). Their biology and ecology have been reviewed by Ilicic and Grossart (2022) and Rasconi et al. (2014). The predominant ecological role of chytrids and other fungus-like organisms infecting algae might be their contribution to carbon cycling and food web dynamics by channeling carbon flow to the food chain in freshwater ecosystems (Klawonn et al. 2021).

Osmotrophic and saprotrophic eukaryotes can also be counted among the plankton parasites, and they usually acquire their nutrients through the direct uptake of dissolved organic substrates (Richards and Talbot 2018). The Labyrinthulomycetes, which include labyrinthulids and thraustochytrids, are another stramenopile group that parasitizes algae and uses osmotrophy as a nutrition mode. They are commonly found in marine snow (Bochdansky et al. 2017) and sediments (Rodríguez-Martínez et al. 2020). Thraustochytrids are also detected during decaying blooms of coccolithophores (e.g. Emiliana huxleyi) and might contribute to the termination of the bloom (Vincent et al. 2021). These organisms are considered parasitic due to extracellular digestion via lysotrophy (also chemoheterotrophy), which involves the secretion of enzymes into the environment to break down larger substrates such as polymers (e.g., cellulose, lignin) into their building blocks (e.g., sugars, fatty acids, amino acids), that will serve for nutrition (Richards et al. 2006).

The Oomycetes, Hypochytriomycetes, and Labyrinthulomycetes all use osmotrophy in one or more life stages and prey on coastal planktonic diatoms, hence contributing to total long-term organic carbon sequestration (Armbrust 2009). Diatoms such as Fragilariopsis and the domoic acid toxin producer Pseudo-nitzschia are Tychoplankton, as they can alternate between benthic and pelagic waters (Cahoon 2016). Due to this versatile lifestyle, these algae could be responsible for transferring plankton parasites from one environment to another. At the same time, the symbionts can use a hitchhiking or piggybacking strategy to colonize new host cells. Indeed, pathogens can become a new parasite species for algae by host jumping, leading to species diversification (Thines 2019). Remarkably, diverse protists and fungi from the same taxonomic clades as plankton parasites of algae were found in marine invertebrates (Holt et al. 2022), raising the question of whether the same organisms are infecting a wide array of hosts. This process has been shown for the genus Labyrinthula, which can infect various seagrass species and is associated with other algae and phytoplankton (Bower et al. 1998).

2.2 Ecological roles of plankton parasites of algae

Plankton parasites are abundant in aquatic ecosystems and impact host populations by modifying the interspecific competition between hosts and other species (Van Donk 1989). Plankton parasites adapted and co-evolved with their hosts in terms of metabolite production and use, as well as gene expression and catalytic function due to their long-term presence and adaptation to marine habitats (Alacid et al. 2017; Blanquart et al. 2016).

Parasites are considered integral components of co-evolved microbial communities and can be assessed to determine the health and functioning of aquatic ecosystems (Drew et al. 2021). Parasite diversity is connected to the health of aquatic communities, and itself plays a direct role in shaping and modulating algal populations (Deng et al. 2022b). Remarkably, plankton parasites can selectively prey on weaker individuals, as shown by the widespread aquatic thraustochytrids exploiting the diatom genus Chaetoceros (Laundon et al. 2021). The preferential infection of unhealthy algal cells promotes the overall health of the host population without impacting its density, a phenomenon typically associated with animal predators and their prey. Parasite-alga interactions are thus not always detrimental to the host population, and these dynamics were coined as healthy herd selection. Hence, host and parasite abundances are not always in phase, with a lag between the host and parasite cell densities akin to the temporal dynamics of predator-prey interactions.

Field studies showed that parasites are usually present in their host from 5 to 18 % by cell number in the algal population, and high competitive pressure exists between infective free-living zoospores of different species (Alacid et al. 2017). Hence, plankton parasites in oceans are presumably involved in more diverse and complex microbial interactions than expected (Bjorbækmo et al. 2020). Strikingly, parasitic infections of phytoplankton can also modify the microbiome surrounding the host cells in laboratory cultures, which may favor opportunistic organisms that prey upon algae (Klawonn et al. 2021). The changes in host-microbiome composition might also potentially disrupt co-evolved relationships between hosts and their symbionts, leading to disease emergence (Llewellyn et al. 2017).

Plankton parasites might have more ecological roles beyond the top-down control of the algal population and a number of examples has been reported for freshwater environments. The transfer of inaccessible organic matter from large, inedible hosts, such as the freshwater diatom Asterionella, to zooplankton is enabled through predation on the zoospores, a process framed as the “mycoloop”, which has been shown for chytrids infecting freshwater diatoms (Kagami et al. 2014). Furthermore, the fungal shunt, i.e., photosynthetic carbon being diverted from the microbial loop to fungal parasites, promotes zooplankton-mediated remineralization (Klawonn et al. 2021). In laboratory studies, freshwater plankton parasites possess a significant capacity to structure the plankton community by increasing the trophic chain length and channeling the carbon flow (Klawonn et al. 2021). Freshwater parasitic fungi could hence shunt 20 % of the total diatom-derived photosynthetic carbon as they themselves are being grazed by copepods, leading to an increase in carbon transfer to higher trophic levels and the bypass of the microbial loop (Klawonn et al. 2021). Parasite-infected algal cells and free-living flagellated parasitic zoospores contain a high amount of polyunsaturated fatty acids (PUFAs) and sterols, which represent a nutrient-rich food source for grazers and zooplankton (Gerphagnon et al. 2019). Further studies should focus on whether similar processes, i.e., the fungal shunt and the “mycoloop”, also occur in the oceans.

2.3 Life cycles, infection stage, and cellular invasion

The shared property among plankton parasites of algae is their ability to produce small, free-living zoospores to ensure dispersal in the water column during their life cycles (Cachon and Cachon 1987). The zoospores might require chemical cues to find new hosts, and swimming might be directed by chemoattraction, i.e., an active movement in response to a chemical gradient. Generally, symbiotic relationships rely on nutrient acquisition from recruited microbial partners, and the active migration towards, and colonization is often driven by chemotaxis (Raina et al. 2019). Chemotaxis governs the movement of marine microbes, particularly prokaryotes, towards phytoplankton-derived compounds, as demonstrated in field assay experiments (Raina et al. 2022). Positive correlations were found between marine bacteria and compounds such as the sugar alcohol erythritol and aminopiperidin-2-one, which were investigated in laboratory-based chemotaxis assays. More than half of the tested compounds induced a positive chemotactic response and are commonly used by marine bacteria to support their growth. For alga-bacterium interactions, bacterial chemotaxis has been investigated in laboratory-controlled models (Sonnenschein et al. 2012). The role of dimethylsulfoniopropionate (DMSP) as a general, broad, and relatively non-specific chemical cue of the marine microbial food web has been found in phytoplankton and bacteria (Seymour et al. 2010). However, in the case of eukaryotic marine parasites of algae, few studies have been conducted to identify the chemoattractant released by susceptible hosts. In cultures of the dinoflagellate Alexandrium minutum, DMSP is hydrolyzed into dimethylsulfide (DMS), which led to the maturation of the parasite Parvilucifera, enabling the transition from the immature to the mature sporont that releases free-living zoospores (Garcés et al. 2013b). Genes of signaling pathways involving proteases and transporters were overexpressed, suggesting that the free-living parasitic zoospores can perceive and sense chemical cues (Farhat et al. 2018).

The chemo-attractive properties of metabolites were investigated by exogenous addition to cultures of plankton parasites. For instance, the ectoparasite dinophyte Paulsenella sp. is attracted to glucose and mannose, common sugars released by the centric diatom Streptotheca thamesis, and the attraction was lower in the dark period (Schnepf and Drebes 1986). Several studies have focused on the chemoattracting cues sensed by aquatic chytrid parasites. For instance, free-living flagellated chytrids were found to be attracted by whole-cell extracts of stressed hosts and a combination of carbohydrates in solution (Scholz et al. 2017). Furthermore, the marine chytrid species Rhizophydium is positively attracted to amino acids and carbohydrates, both being photosynthetic by-products (Muehlstein et al. 1988). Investigating the volatiles released by infected and non-infected hosts revealed different metabolic profiles, with a decrease in anti-fungal beta-ionone in chytrid-infected cells (Yoneya et al. 2021). Hosts might release diverse organic compounds that can serve as food and habitat-finding cues for grazers, defense against herbivores, and microbial interactions during the algal bloom (Saha and Fink 2022).

While parasite chemotaxis has been as yet insufficiently investigated in marine and freshwater environments due to the challenges in laboratory cultivation, the chemical exchange that facilitates and influences parasite infection in plants is well-researched. Plant exudates, i.e., volatiles, sugars, and amino acids, can accelerate the germination of terrestrial oomycetes. Zoospores of terrestrial oomycetes can be attracted to specific compounds released by plants, such as prunetin, daizein, and genistein (Judelson and Ah-Fong 2018). These isoflavones possess multifunctional roles and can influence encystment and germ tube orientation (Morris et al. 1998). Exogenous addition of sesquiterpenes, such as abscisic acid, attracts the zoospores of the parasitic oomycete Plasmopara viticola, which infects many plants (Kiefer et al. 2002). Abscisic acid is a known plant signaling molecule mediating seed dormancy, growth, and adaptation to environmental stresses (Hauser et al. 2011). In microalgae, this compound and several other phytohormones have been detected in a broad spectrum of microalgal lineages, including diatoms (Lu and Xu 2015), but it is not yet established how or whether they relate to plankton parasites. Notably though, adding phytohormones to microalgal cultures induces lipid production and promotes cell growth, which might play a role in the interactions with parasites (Yang et al. 2023). In plants, the chemotaxis of the oomycete parasites involves G-proteins (Judelson and Ah-Fong 2018). A G-protein coupled receptor was identified in unicellular marine eukaryotes, including 81 diatom and 24 dinoflagellate groups (Mojib and Kubanek 2020). Another study revealed that four diatoms share genes related to G protein-coupled receptors (Port et al. 2013). This evidence suggests that analogous receptor proteins and signaling pathways might be involved in the attraction and attachment of marine oomycetes and other parasites of algae. Furthermore, a repertoire of extracellular proteins is encoded within genomes of parasitic alveolates, suggesting a connection with cell wall degradation (Templeton and Pain 2016).

Pathogen-associated molecular patterns (PAMPs) are small molecular motifs conserved in pathogenic microbes (Mogensen Trine 2009). Many molecules can serve as PAMPs, including glycans and glycoconjugates. Multiple receptors, such as toll-like and pattern-recognition receptors, have been investigated in plants and animals but not yet in plankton parasites. However, to date, no studies have demonstrated whether marine plankton parasites of algae employ these molecular patterns. The latest whole-genome sequencing efforts might however reveal whether these receptors are present in plankton parasites and symbionts (Faktorová et al. 2020).

In terrestrial plants, pathogenic effectors can induce the modulation of immune responses (Dodds and Rathjen 2010). PAMPs are recognized by receptor proteins, also called pattern recognition receptors, that, once stimulated, lead to PAMP-triggered immunity. In seaweeds, such as the brown alga Macrocystis pyrifera, a local, inducible, autophagic mechanism serves in the defense against the marine oomycete Anisolpidium ectocarpii (Murúa et al. 2020). Phytoplankton hosts, i.e., unicellular photosynthetic eukaryotes, might not have evolved such elaborate molecular mechanisms to modulate immunity but might counteract cell invasion using other basal processes, such as programmed cell death and autophagy. These processes determine cell fate and can be triggered by various abiotic and biotic factors (Bidle 2016). Autophagy is also the hallmark of other pathogenic infections in the coccolithophore E. huxleyi, such as during the lytic phase induced by coccolithoviruses (Schatz et al. 2014). The coccolithoviruses manipulate their host lipid metabolism and alter glycosphingolipid production, regulating cell fate via programmed cell death (Vardi et al. 2012). Algal resistance might thus be modulated via the control of the programmed cell death machinery required for successful viral replication. It is unknown whether these processes are involved in the infection caused by eukaryotic parasites.

Due to the diversity of morphology and physiology of the algal species, distinct strategies of cellular invasion depending on the targeted host are expected. For instance, diatom hosts possess frustules, i.e., an external, siliceous part of the cell wall, which parasites encounter during cell invasion. Algicidal bacteria can attack diatoms by attaching and releasing enzymes to degrade this diatom matrix (Furusawa et al. 2003). Coincidentally, co-existing eukaryotic parasites might use this bacterial action to invade and infect the algal cells alongside.

2.4 Parasite reproduction and dissemination

Plankton parasites share a similar pattern of reproduction and dissemination, alternating from a free-living phase (zoospore) and an intracellular parasitic phase (trophont and sporont) (Cachon and Cachon 1987). Generalist plankton parasites can also have a more complex life cycle that involves two or more hosts used for reproduction (Alacid et al. 2016).

Plankton parasites are characterized by these distinct infection stages, which involve specific metabolic pathways associated with growth and reproduction. Transcriptomics analysis of infective stages during Amoebophrya infection in the dinoflagellate host Alexandrium highlighted the diversification of transcribed metabolic pathways (Lu et al. 2014). Genes related to oxidative pathways, cell division, and proliferation were expressed during the maturation of the parasite-infected host cells. At the initial host encounter and penetration stage, the parasitic syndinian Amoebophrya induces genes related to cytoskeleton organization and signal transduction, including genes coding for G protein and guanine nucleotide-binding proteins (Lu et al. 2014).

In Amoebophrya parasitism, the host chloroplast and mitochondria remain fully functional after the cell invasion, stressing the importance of photosynthesis for parasite reproduction (Kayal et al. 2020). This occurrence contrasts with many plankton parasites, such as Parvilucifera, that kill their host before digesting them, which prevents cells from evolving resistance mechanisms in the course of the infection. By keeping the host cell alive with physiological functions, parasites such as Amoebophrya enable parasite reproduction quickly and efficiently. Moreover, Amoebophrya-infected cells remain motile, unlike Parvilucifera parasites that induce loss of motility in dinoflagellates at the initial cell invasion stage (Decelle et al. 2022). This phenomenon would serve the parasite by enabling dissemination to new environments while being protected inside its host. These features might have evolved multiple time in the Alveolates, as Perkinsids and Syndinians exhibit extracellular proteins to enable cell invasion (Templeton and Pain 2016). The metabolism of Amoebophrya parasites is sustained by the continuous carbon production of the host, a metabolic process shared by more distantly related apicomplexan parasites such as Toxoplasma and Plasmodium that infect human cells (Decelle et al. 2022). Strikingly, Colpodella, a predatory alveolate and close cousin to human parasites from Apicomplexa clade, as well as the intracellular fish-parasite Perkinsus, have developed apical complexes and secretion systems that are indeed used during cellular infection (Brugerolle 2002).

Plankton parasites of algae employ a low-cost energy scavenging and harvesting strategy by altering the host’s metabolism. The marine oomycete Lagenisma coscinodisci can hijack the algal metabolism by overexpressing two beta-carboline alkaloids (Figure 2), which are responsible for diatom cell division arrestment and conversely speed up the infection rate in the population (Vallet et al. 2019). This finding is also an example of plankton parasites counteracting the host defense by inhibiting host cell division and using the host machinery. However, the beta-carbolines constitute a group of alkaloids with antioxidant properties (Moura et al. 2007), and they may play a more diverse role in Lagenisma infection by mitigating the effect of oxidative stress induced by cell invasion and metabolic reshuffling.

Figure 2:

Life stages of the plankton parasitoids Parvilucifera rostrata (#) and Lagenisma coscinodisci (*) that infect the dinoflagellate Alexandrium minutum and the diatom Coscinodiscus granii, respectively. Biological functions involved in alga-parasite interactions (in blue) and the two metabolites DMS and β-carboline contributing to the infection processes are highlighted. Images reproduced from Lepelletier et al. (2014b) and Vallet et al. (2019), with permission.

Another example of a host metabolite serving in the reproduction of plankton parasites is the volatile compound DMS (Figure 2). This chemical cue mediates the transition from the trophont to the mature reproduction stage in the intracellular phase, i.e., the sporont. DMS was added exogenously to laboratory cultures of the dinoflagellate Alexandrium minutum infected with the alveolate parasite Parvilucifera sinerae, and induced the activation and maturation into the sporont (Garcés et al. 2013b). DMS effectively caused the release of the free-living zoospores, which could infect new surrounding host cells (Figure 2). Whether this compound has a broad-spectrum induction activity in other algal hosts has not yet been investigated.

Parasitic and pathogen infections in algae are often characterized by programmed cell death and the induction of reactive oxygen species, for example, during the viral infection of the coccolithophore Emiliana huxleyi (Vardi et al. 2012). On the one hand, plankton parasites of algae have sex and use meiosis to conduct genetic intermixing and evolve. These processes also occur after the cellular invasion and maturation of the trophont into the sporont (Jephcott et al. 2016). On the other hand, alga-parasite and alga-predator interactions are subjected to the Red Queen dynamics, defined as a long-term co-evolutionary motion in which species must constantly adapt, evolve, and proliferate to survive (Råberg et al. 2014; Van Valen 2014). Hence, sex is maintained as it creates novel genotypes with a selective advantage. This hypothesis was investigated in the predator-prey system of rotifer-alga Brachionus-Chlamydomonas. Sex rates were high in changing environmental conditions, increasing selection pressure on these organisms (Felpeto et al. 2013). In more constant conditions, predators evolved rapidly to lower sex levels, indicating that selection pressure can shift a phenotypic trait. High potential for Red Queen dynamics has been demonstrated in plankton parasites when challenging clones of the dinoflagellate A. minutum with P. sinerae (Råberg et al. 2014). These winnerless coevolution dynamics characterize parasitic chytrids (Kyle et al. 2015) and marine viruses (Avrani et al. 2012) in aquatic environments. More insights into the molecular mechanisms involved in plankton parasite reproduction are expected from recent whole-genome and transcriptome sequencing and analysis (Faktorová et al. 2020).

2.5 Effect of abiotic factors on alga-parasite interactions

Plankton parasites are influential in aquatic ecosystems as they facilitate energy flows through the food web and control the population of algal species (Deng et al. 2022b; Park et al. 2021). The changes in environmental factors, such as significant modification of light, temperature, salinity, and nutrient levels, can conceivably impact the algal hosts and their associated microbiota (Menaa et al. 2020). For instance, increased sea surface temperature might lead to modulation of parasitism in aquatic ecosystems (Wood et al. 2023). A study using 1000-L indoor mesocosm showed that a +4 °C warming treatment accelerated parasitic infections and the bloom termination of the diatom Synedra (Frenken et al. 2016). Conversely, in a laboratory-based infection assay conducted with the perkinsid Parvilucifera targeting two bloom-forming dinoflagellates, the toxin-producer Alexandrium minutum and non-toxic Heterocapsa triquetra, the parasite favored one or the other host species depending on the incubation temperature (Schmitt et al. 2022). Remarkably, higher infection rates of A. minutum were recorded at higher temperatures, while a lower temperature decreased the overall infection rates in both algal hosts. This is also because Parvilucifera, similar to Amoebophrya, forms a resting stage in its host to survive the winter months (Chambouvet et al. 2011; Lepelletier et al. 2014a). Hence, plankton parasites and their algal hosts will employ different adaptation responses to a temperature variation, and some species will be negatively impacted while others will thrive.

Other abiotic factors, such as salinity, can affect host susceptibility and parasite infectivity. For instance, Parvilucifera parasites thrive at lower salinity, promoting sporangial germination and higher infection rates (Figueroa et al. 2008). Concurrently, higher salinity correlates with losing fungal diversity in coastal waters (Rojas-Jimenez et al. 2019). Meanwhile, the algal hosts cope with a salinity increase by accumulating lipids to strengthen their membranes and enhance the production of osmoprotectant metabolites such as zwitterions (Fenizia et al. 2020, 2021). The change of these abiotic factors, such as temperature and salinity, might cause generalist plankton parasites to attempt a jump from one host to another. Environmental refugees were also proposed for plankton parasites, enabling the parasite or the host to subsist under global change (Gsell et al. 2023). Due to the tolerance range and sensitivity of many species to environmental factors, the outcome of alga-parasite interactions can be affected by abiotic changes. Non-specific generalist parasites can flourish in new hosts, while specialist parasites relying on one host species may face a higher risk of extinction. Hence, the persistence of plankton parasites in aquatic ecosystems will be determined also by the susceptibility of the algal hosts and their ability to defend themselves, and the resilience of the free-living forms of parasites that infect new cells (Sures et al. 2023).

4.1 Interaction with larger predators

Grazers can preferentially prey on infected phytoplankton cells, hence sustaining the growth of the predators during an algal bloom (Evans and Wilson 2008; Rasconi et al. 2014). Conversely, another study showed that viral infection could also deter grazing by copepods (Vermont et al. 2016). These contrasting findings indicate the complexity of grazers’ interactions with algae and their parasites. DMS, produced by the algal hosts, is a key player in the global sulfur cycle and performs multiple functions in marine microbial interactions (Mahajan et al. 2015; Yoch 2002). Remarkably, DMS has a role in parasitic infection and can serve as a chemoattractant for diverse protist grazers that prey on phytoplankton hosts (Shemi et al. 2021). Plankton parasites and grazers compete and sometimes target the same algal species, thus acting as a critical top-down control of the host populations in aquatic ecosystems (Lima-Mendez et al. 2015).

The predation on infected cells has been shown for several algal host species and their plankton parasites. For instance, grazers can interfere with host-parasite interactions by feeding on infected cells, as demonstrated during the bloom of Planktothrix rubescens parasitized by chytrids (Frenken et al. 2020). Ingestion of parasite-infected algae is not restricted to the diet of copepods, as Parvilucifera-infected cells of the bloom-forming dinoflagellate Akashiwo sanguinea were rapidly ingested by the algal predator Luciella masanensis (Park et al. 2021). In this laboratory-based assay, the parasitoid presence led to its co-occurrence with both prey and predator, suggesting that parasites play a role as a mediator in planktonic predator-prey interactions. Furthermore, in cultures, grazers ingested the infective zoospores, which can lead to an 80 % decrease in parasite infection of Akashiwo sanguinea (Johansson and Coats 2002). These findings did not fully translate into alga-virus interactions, as the predator Oxyrrhis marina did not ingest more virus-infected cells than healthy ones (Goode et al. 2019). In diatom hosts, chytrid-infected cells of the host Asterionella formosa were not grazed by the copepods. Still, the survival rate of the predator increased following a diet of infected cells, suggesting that the predators were feeding on the free-living parasitic zoospores instead (Kagami et al. 2011). Grazers could also function as a transmission vector for parasites of algae, as shown for coccolithoviruses (Frada et al. 2014).

4.2 Interactions with bacteria

Marine bacteria, including the most abundant clade, SAR11, are significant third-party microorganisms in alga-parasite interactions, as they are ubiquitous in oceans and found in association with all known algal hosts targeted by plankton parasites (Giovannoni 2017). In particular, many pathogenic bacteria are naturally more abundant during the decline phase of the diatom blooms (Branscombe et al. 2024). A unique bacterial consortium is usually present in the near surroundings of the algae, a process termed microbial gardening. For instance, the green macroalga Ulva enriches its environment with metabolites that attract and stimulate the growth of microorganisms necessary for algal morphogenesis (Wichard et al. 2015). These bacteria associated with phytoplankton and seaweeds can encounter plankton parasites in their free-living or host-associated form. Questions arise about whether algae possess a core bacterial microbiome that can be detected regardless of geographical location, environmental conditions, and physiological status (Dittami et al. 2021). The study of bacterial microbial communities associated with the brown alga Saccharina latissima demonstrated a high species variability (Tourneroche et al. 2020).

Further, the microorganisms were organized and partitioned according to the algal tissues. This observation was also made for green macroalgae, where the host releases DMSP, recruiting specific bacteria associated with the rhizoid and supporting the algal morphogenesis (Kessler et al. 2018). In turn, some thallus-specific bacteria release the osmoprotectant ectoine that protects the host during salinity stress (Vallet et al. 2021).

In multicellular algae living with epiphytic and endophytic microorganisms, bacterial symbionts might serve to protect against plankton parasites by producing bioactive molecules, and this might be a similar host strategy to that of mosquitoes harboring Wolbachia bacterial symbionts that protect against Dengue virus (Hoffmann et al. 2011). In amphibians, defensive bacteria associated with the skin can reduce their host susceptibility against chytrids (Bletz et al. 2013). These examples in terrestrial organisms suggest that bacterial symbionts can contribute to the host’s defense against parasites, which will also vary according to the environmental conditions (Hopkins et al. 2017).

Marine bacteria can produce and release compounds used by the algal host (Amin et al. 2012, 2015), potentially affecting plankton parasites. Indeed, marine bacteria are well known for QS signaling, which enables the production of specific signaling molecules based on the cell population density and regulates functions such as virulence, niche colonization, biofilm formation, and toxin production (Atkinson and Williams 2009). Hence, marine bacteria and their chemical signaling might have a cryptic but significant role in algal hosts that are parasitized by plankton parasites.

Bacterial QS signaling is also involved in the induction of virulence factors in pathogen-host associations (Zhou et al. 2016), for instance increasing the mortality of the alga Emiliania huxleyi (Harvey et al. 2016). Conversely, another study revealed that the bacterial QS compound 2-heptyl-4-quinolone protects the alga E. huxleyi from viral attacks (Pollara et al. 2021). Algal cells could get infected with viral entry, but replication and release were inhibited. Further studies should focus on testing the role of QS molecules in the infectivity of plankton parasites to provide insights into their potential influence on alga-parasite interactions.

Remarkably, marine bacteria have evolved lifestyle strategies that enable them to shift from mutualistic to pathogenic towards their algal hosts, which is sustained by the production of bioactive metabolites that serve the new role. The most outstanding example is an α-proteobacterium from the Roseobacter clade, Phaeobacter gallaeciensis, which promotes the growth of its algal host E. huxleyi by secreting auxins (Seyedsayamdost et al. 2011) at first. In response to the senescent host releasing p-coumaric acid, this bacterium switches to a pathogenic lifestyle by producing roseobactericides, which lyse E. huxleyi at a concentration of 2.2 µM. Another α-proteobacterium, Sulfitobacter, becomes a pathogen of E. huxleyi in the presence of algal DMSP (Barak-Gavish et al. 2023). Sulfitobacter can compete with pathogenic Phaeobacter species and protect E. huxleyi in laboratory cultures (Beiralas et al. 2023). These observed contrasting effects on algae might explain the diverse and complex multi-species plankton interactions (Deng et al. 2022a).

Other marine bacteria, such as Kordia algicida, are primary pathogens of algae, causing a rapid decline of algal populations due to the excretion of specific proteases that lyse algal membranes (Paul and Pohnert 2011). They also coexist with plankton parasites, as they arise together with eukaryotic plankton parasites at the collapse of algal blooms (Deng et al. 2022b).

During indoor enclosure experiments, algicidal bacteria were found to induce the bloom termination of the diatom Chaetoceros socialis, leading to the rise of an algal competitor, Phaeocystis, which is resistant to the bacterial lytic activity (Bigalke et al. 2019). This occurrence might hinder plankton parasites that target Chaetoceros, i.e., thraustochytrids, whose existence would also be threatened by these co-occurring natural bacteria. Considering that thraustochytrids can infect Chaetoceros senescent cells (Laundon et al. 2021), the actual effect of algicidal bacteria on eukaryotic plankton parasites can be questioned. Indeed, as these bacteria target and co-exist with the same algal host that plankton parasites prey on, further studies using tripartite interactions are needed to reveal their potential role in parasitic infection and host defense.

Furthermore, during parasitic infection on phytoplankton cells, bacterial colonization is significantly promoted in fungal-infected cells in comparison to non-infected cells in the cultured model diatom Synedra infected by Zygophlyctis (Klawonn et al. 2023). In this laboratory-based study, fungal infections also reduced the formation of aggregations of algal cells and consequently modified the bacterial microbiome’s abundance in the surrounding cells (Klawonn et al. 2023). In four freshwater algal species infected by the parasite Amoeboaphelidium protococcarum cultivated in photobioreactor systems, the overall bacterial diversity increased, with species-specific differences being observed over time (Höger et al. 2021). In another laboratory-based assay, the infection by the chytrid Rhizophydiales could also modify the bacterial species composition surrounding its diatom host Asterionella (Klawonn et al. 2021). The shift in the bacterial community composition upon viral infection was also detected in large-scale mesocosm experiments, followed by an increase in the extracellular release of acidic polysaccharides that contributed to the ocean carbon sink (Vincent et al. 2023). These examples indicate that bacteria interact with plankton parasites, and their presence is modulated during parasitic infection of algae.

4.3 Interactions with other unicellular eukaryotes

Chemical interactions between plankton eukaryotic parasites and other protists most likely occur in oceans. Still, as they are often short-lived, however, plankton parasites might not appear in large-scale field surveys recorded at specific locations and times. The species composition of the plankton communities can be derived from whole microbiome analysis studying microbial interactions in laboratory-based co-culture assays (Bjorbækmo et al. 2020). However, few studies have yet surveyed the role of single-cell eukaryotes on alga-parasite exchanges – future exploration using multipartite interactions in laboratory-based experiments is needed. Competitive and interdependent interactions might emerge within the algal population as novel species of plankton parasites are continuously being discovered (Buaya et al. 2021; Garvetto et al. 2019; Reñé et al. 2021; Van den Wyngaert et al. 2017). Since taxonomically different parasites can target and infect the same clade of algal hosts, we can expect highly competitive interactions between the co-existing microbes, with different chemical cues used for host foraging and cell attachment. During cross-infection studies, the perkinsid parasite Parvilucifera corolla could infect the chlorophyte Pyramimonas without developing its complete life cycle by producing zoospores (Rodríguez-Martínez et al. 2020). The authors hypothesized that parasites might attempt to infect co-existing algae belonging to a completely distinct clade, leading to a parasite population sink, i.e., enabling parasite speciation and radiation to other, less frequent hosts. Hence, host specificity allows parasite speciation, which might be influenced by environmental and geographic factors (Brunner and Eizaguirre 2016).

Plankton parasites may alter the outcome of host-species interactions, such as competition, mutualism, and predation. In a meta-analysis based on phylogenetic studies, parasites adversely affected host-species interactions in aquatic habitats but conversely provided beneficial effects for terrestrial hosts (Hasik et al. 2023). These findings consolidate that an organism can be a parasite in one environment while shifting to a mutualistic or commensal lifestyle in another as it encounters other host species. Microsporidia from the kingdom of Fungi are common endoparasites infecting Daphnia, small aquatic crustaceans that prey on microalgae (Valois and Poulin 2015). When grazing predators were infected, they exhibited reduced fecundity under scarce resources and without the presence of virulent parasitic individuals. However, when more virulent parasites were present in the host, the infected grazer was more fecund (Rogalski et al. 2021). Another member of the fungal kingdom, Aspergillus pseudoglaucus, was isolated from a microalgal culture and cultivated in the presence of the dinoflagellate Prorocentrum lima (Berry et al. 2023). While in close physical contact with the fungus, the dinoflagellate released higher concentrations of toxins, including okadaic acid and dinophysistoxin 1, which might suggest a potential role in the algal defense. Remarkably, the alkaloid saxitoxin produced by the dinoflagellate genus Alexandrium was detected in higher amounts in Amoebophrya-infected cultures than in healthy cells but was not found in the free-living zoospore stage of the parasite (Kim and Park 2016). The function of toxins produced by bloom-forming harmful algae in the infection process has yet to be revealed. Future studies could explore the influence of third-party microbes on parasite infectivity during different bloom phases and whether they are beneficial or detrimental to the infection success of algae.