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Protistology 16 (3): 149-160 (2022) | doi:10.21685/1680-0826-2022-16-3-l PPOtÎStOlOây
Perspectives
Studies of cellular and molecular mechanisms coupled with physico-chemical and ecological prerequisites of harmful algal blooms secure advanced research prospects in planktonology
Irena V. Telesh1'* and Sergei O. Skarlato2
1 Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia
2 Institute of Cytology of the Russian Academy of Sciences, St. Petersburg, Russia
| Submitted September 2, 2022 | Accepted October 3, 2022 |
Summary
Harmful algal blooms (HABs) in aquatic ecosystems constitute one of the topical research issues in modern planktonology. Currently, HABs have intensified in many freshwater basins and marine coastal regions of the world because of the increasing anthropogenic loads enhanced by climate change. Aftereffects of these events reduce water quality and deteriorate the environment, fisheries and aquaculture, flora, fauna, and human health. Harmful blooms are most prominently expressed in coastal ecosystems and semi-closed brackish-water seas. However, HAB patterns in the highly variable brackish coastal environments are seriously understudied; therefore, research and forecasting of these events is still hindered. The article presents an overview of recent studies using multidisciplinary approach, which allows for applying modern molecular-genetic, cellular-biological, biochemical and biophysical techniques, bioinformatics, and methods ofaquatic ecology for obtaining the most urgently needed new biological data and their inclusion into prognostic mathematical models. These topical issues were addressed in details and widely discussed at the IV All-Russian Conference "Frontiers in Plankton Research" held in Svetlogorsk (Kaliningrad Region, Russia) on 25—30 September 2022.
Key words: Baltic Sea, coastal ecosystems, cyanobacteria, dinoflagellates, harmful algal blooms, Frontiers in Plankton Research
Harmful algal blooms — a topical research issue in planktonology
Harmful algal blooms (HABs) in aquatic ecosystems constitute one of the topical research issues in present-day planktonology. Climate change, enhanced inflow of anthropogenic nutrients, intense desalination of inland seas and extension of HAB
https://doi.org/10.21685/1680-0826-2022-16-3-1
© 2022 The Author(s)
Protistology © 2022 Protozoological Society Affiliated with RAS
regions are the greatest environmental problems nowadays that can cause disastrous consequences in the nearest future (Gobler et al., 2017; Paerl, 2018; Brown et al., 2020; Burford et al., 2020; Glibert, 2020; Paerl and Barnard, 2020; Telesh et al., 2021; Skarlato, 2022). Outbursts of toxic or potentially toxic prokaryotic and eukaryotic microorganisms in marine coastal waters often induce poisoning of
*Corresponding author: Irena V. Telesh. Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb., 1, 199034 St. Petersburg, Russia; Irena.Telesh@zin.ru
aquatic organisms by algal secondary metabolites or toxins causing significant harm to flora and fauna in natural ecosystems and aquaculture, as well as spoiling industrial fishery, tourism, and human health (Li et al., 2015; Anderson et al., 2019; Glibert, 2020; Sakamoto et al., 2021). Moreover, hazardous blooms of microorganisms can be considered as additional powerful facilitators of climate change that cause significant transformations of freshwater, marine, and coastal brackish-water ecosystems (Griffit and Gobler, 2020). However, although many studies deal with toxic blooms of microorganisms (reviewed by: Carstensen et al., 2020; Glibert, 2020; Plaas and Paerl, 2021), still the complete understanding of these devastating events is lacking and descriptions of their sustainable patterns are scarce.
Coastal ecosystems host the majority of HABs
HABs are most deleterious in coastal marine ecosystems and semi-closed brackish-water seas — for example, the Baltic Sea (Carstensen et al., 2015, 2020; Olli et al., 2015; Skarlato et al., 2018a, 2018b; Anderson et al., 2019; Wasmund et al., 2019; Olofsson et al., 2020; Zilius et al., 2021). The Baltic coastal ecosystems host highly diverse microplankton communities (Telesh et al., 2011, 2013, 2015). Also, generally they are characterized by the enhanced hydrodynamic instability, structural and functional complexity, and high dynamism (Schubert and Telesh, 2017), as well as by non-linearity ofprocesses therein that govern the specific features ofpopulation dynamics ofaquatic organisms in space and time (Beninca et al., 2008, 2015; Boeing, 2016; Telesh et al., 2019, 2021). The type of this dynamics is featured by the complex effects of various external ecological triggers and internal cellular and molecular-genetic drivers on organisms and their populations (Telesh et al., 2019, 2021). However, the mechanisms behind those processes that determine the causality within populations and communities of aquatic organisms remain poorly studied (Gobler et al., 2017; Hillebrand et al., 2018; Brown et al., 2020). This hinders modeling of ecosystems' resistance to external stressors, including those stimulating harmful blooms ofmicroorganisms, and prevents development ofmethods for controlling these hazardous events. Meanwhile, HABs are most dangerous in the coastal ecosystems of seas in the economically important regions of the world where the nearshore territories are densely populated (Liu
et al., 2018; Anderson et al., 2019; Glibert, 2020). The example ofthe eastern Baltic Sea coastal regions demonstrates perfectly well that calm weather, surface warming and reduced turbulent mixing of the water column are among key abiotic factors that promote HABs, including cyanobacterial blooms (Fig. 1).
Recently, the large-scale meta-analysis of data from 86 coastal and estuarine regions in Europe and North America revealed that, unlike in marine and freshwater ecosystems, in brackish coastal seawaters the regularities of HABs development are still significantly understudied (Carstensen et al., 2015). This analysis showed that the community characteristics and phytoplankton dynamics in the ocean and marine coastal waters differ considerably. Moreover, the succession of dominant species in coastal ecosystems can be very abrupt and variable in timing (Winder and Cloern, 2010). Therefore, the forecasting of harmful blooms in these unstable environments is particularly complicated (Carstensen et al., 2015; Telesh et al., 2021).
Modern ecological, cellular and molecular data are needed to improve HABs forecasting
The standard monitoring ofphytoplankton communities and physico-chemical characteristics of the environment often cannot provide the sufficient data that are necessary for prognostic purposes. For comprehensive understanding of blooms of certain phytoplankton species, it is crucial to update the knowledge of their life cycles and reproduction features (Sarno et al., 2010; Berdieva et al., 2020, 2021; Berdieva and Paliy, 2022; Kalinina et al., 2020, 2022), resting stages' maturation (Shikata et al., 2008), allelopathy and intra-species mutualism (Smayda and Reynolds, 2001). Thus, the necessity of studies of the ecological, population, cellular and molecular-genetic mechanisms that back up HABs arises as the most urgent need (Skarlato, 2022). The ecological niche dimensions (i.e., the ranges of the basic physico-chemical characteristics of the environment, including water salinity, temperature, irradiance, nutrient concentrations and other factors that accompany massive proliferation of these organisms) of the principal bloom-forming species, calculated using methods ofmathematical statistics, are supposed to serve as potent predictors of harmful blooms (Telesh, 2022).
The population dynamics of microorganisms largely determines their bloom-forming capacities.
Fig. 1. Cyanobacterial bloom in the coastal waters of the Eastern Gulf of Finland, the Baltic Sea (August 20, 2022). Photos: I.V. Telesh.
At the same time, life cycles of microorganisms from different taxonomic groups are characterized by a number of unique features that define the rules for their population dynamics (Sarno et al., 2010; Figueroa et al., 2018). However, irrespective ofhigh importance of knowledge of the life cycles of bloom-forming species for the development of preventive measures against HABs in aquatic ecosystems, at present life cycles are known only for less than 1% of all described species of microorganisms (Tang et al., 2021). Specifically, life cycle of the potentially toxic dinoflagellates Prorocentrum cordatum (Ostenfeld) Dodge, 1975 that regularly form blooms in the Baltic Sea, is insufficiently studied, and its regulation triggers are not unveiled yet (Berdieva et al., 2020, 2021; Berdieva and Paliy, 2022). Meanwhile, the data on the life cycle stages, patterns of their alternation, and the ecological niches occupied by organisms at those stages are of key importance for understanding the mechanisms of the microorganisms' dispersion and reasons for HABs formation.
One of the hypotheses about the initiation and regulation of protistan HABs, which still requires experimental approval at the cellular and molecular levels, is the suggestion that mixotrophic metabolism of many protists, especially dinoflagellates, plays the key role in the eutrophic natural waters (Heisler et al., 2008; Li et al., 2015; Stoecker et al., 2017; Flynn et al., 2019). The physiological capacities of dinoflagellates, including their tolerance to wide salinity range and mixotrophic feeding strategy, have
been broadly discussed by the international scientific community during the recent years (reviewed by: Skarlato et al., 2018b). Earlier, the ability of dinoflagellates to obtain nitrogen not only from inorganic substrates but also from organic substances like urea and amino acids was demonstrated experimentally (Solomon et al., 2010). Moreover, there are data showing that those organisms can utilize also carbon from dissolved organic substances, although in rather small amounts (Matantseva et al., 2018; Mulholland et al., 2018). Of special interest are the so far rare studies demonstrating the balance of autotrophy and heterotrophy of dinoflagellates in the environment where several different organic and inorganic substrates are present. In particular, the intra-population heterogeneity of the dinoflagellates P. cordatum consuming ions of nitrate and bicarbonate during the mixotrophic nutrition was disclosed experimentally by using the dissolved organic and inorganic sources of nitrogen and carbon (Matantseva et al., 2016).
The combination of phagotrophy (i.e., feeding on other organisms, organic particles, etc.) and photosynthesis in mixotrophic dinoflagellates is even less studied. This combination is likely common in nature, including the periods of algal blooms, and it is highly relevant to both dinoflagellates and ecosystems in general (Stoecker, 1999). However, the successful and efficient studies of phagotrophy and its role in nutrition of mixotrophic microorganisms, similarly to investigation of transmembrane trafficking of inorganic ions, are possible only at the
Fig. 2. Participants ofthe IV All-Russian Conference "Frontiers in Plankton Research" (Svetlogorsk, Kaliningrad Region, Russia; 25—30 September 2022). Photo: K.A. Podgorny.
cell level using the laborious single-cell approach; therefore, these studies are utterly rare so far. Recently, the NanoSIMS technique was used to obtain data on the balance of autotrophy and phagotrophy in some representatives of Haptophyta and Chrysophyta algae (Terrado et al., 2017; Carpenter et al., 2018). However, bloom-forming dinoflagellates have not yet been studied in this respect, and the information about the effects of phagotrophy on the transmembrane ionic transport into their cells is lacking.
Ionic transport plays a crucial role in the interactions of microorganisms with the environment (Taylor et al., 2011; Pozdnyakov et al., 2014; Echevarria et al., 2016; Helliwell et al., 2021). Ion channels are transmembrane protein complexes that are key components ofionic transport (Hille, 2001). The transmembrane transport of inorganic ions in cells of the model bloom-forming dinoflagellate species, studied by means ofbioinformatics and cell biology methods, could shed light on adaptation of these flagellates to changing salinity as well as on their nutrition modes and intra-population
metabolic heterogeneity (Matantseva et al., 2016, 2018; Skarlato et al., 2018a; Pozdnyakov et al., 2021; Skarlato, 2022). Moreover, usage ofbioinformatics and the molecular phylogeny methods in the ion channel studies affords drawing important conclusions about both functions and roles of certain components of the ionic transport system in bloom regulation, and about cell physiology of dinoflagellates in general (Pozdnyakov and Skarlato, 2015; Pozdnyakov et al., 2018, 2020, 2021).
Protistological studies contribute substantially to present-day planktonology
A wide spectrum of topical protistological questions and hot issues of aquatic microbiology and HAB studies were addressed in many details and widely discussed at the IV All-Russian Conference "Frontiers in Plankton Research" held in Svetlogorsk (Kaliningrad Region, Russia) on 25—30 September 2022 (Figs 2—5). Four out of 7 plenary lectures at the conference dealt with protistological topics (57%). The similar proportion held true for the overall
Fig. 3. Irena Telesh, the Chairperson of the IV All-Russian Conference "Frontiers in Plankton Research", and Denis Tikhonenkov, the plenary lecturer presenting the discovery of microbial predators from a new supergroup of eukaryotes. Photo: K.A. Podgorny.
Fig. 4. Sergei Skarlato (left), Editor-in-Chief of the Journal "Protistology" and the Scientific Committee member; Maria Smirnova (center), member of the Organizing Committee, and Elena Naumenko (right), Vice-Chairperson of the IV All-Russian Conference "Frontiers in Plankton Research". Photo: K.A. Podgorny.
number of protistological and microbiological presentations (29 out of altogether 53 presentations at the conference). In particular, two plenary lectures reviewed the ecological and physico-chemical prerequisites of HABs (Telesh, 2022) and highlighted cellular and molecular mechanisms responsible for harmful blooms of algae and cyanobacteria in the Baltic Sea coastal waters (Skarlato, 2022). New spatial distribution models of692 species oftintinnid ciliates in different regions of the World Ocean were presented in another plenary talk (Gavrilova and Dovgal, 2022). But the culmination of the plenary session was the presentation of a new supergroup of eukaryotes — the predatory flagellated protists discovered recently in different habitats of remote marine regions, including coral reefs of Curaçao (continental shelf of South America), coastal bottom sediments in the Black and Red seas, water column in the SE Pacific and Arctic oceans (Tikho-nenkov, 2020). The newly described fascinating microbial predators resemble Ancoracysta morphotype, but become much smaller, about 3 ^m long, ifthey starve in the absence of eukaryotic prey. These predatory flagellates have wide geographic distribution and likely belong to the recently discovered deep branches of the eukaryotic tree (Tik-honenkov, 2020).
Different aspects of spatial distribution, range expansion and invasiveness, seasonality in development, peculiarities of morphology, functional and taxonomic diversity of protists in a variety of water
bodies of dissimilar types and origin were discussed at the conference sessions. Session 1 covered the issues of taxonomy and identification of planktonic organisms, Session 2 discussed biodiversity and trophic interactions in plankton, and Session 3 — planktonic invasive species and their role in aquatic ecosystems. Session 4 ("Harmful phytoplankton blooms in marine, brackish and freshwater ecosystems") served a good platform for highlighting the importance of using multidisciplinary approach for studying HABs. In particular, the urgent need for identifying and monitoring the concentrations of dangerous cyanobacterial toxin microcystin in the Baltic lagoons and adjacent coastal lakes and ponds was brightly demonstrated in a series of recent studies (Sulcius et al., 2015; Smirnova and Ezhova, 2022). Additionally, the necessity of revealing the microcystin-producing cyanobacteria and investigation of their interactions within pelagic ecosystems ofthe arctic lakes and other water basins was timely stressed (Berezina et al., 2022).
Importantly, it was also shown that results of field studies and nature observations thrive when they are verified by usage ofmolecular, phylogenetic, biochemical, biophysical, and other alternative methods. A good example of such focused research is the first discovery of a new protistan species from the genus Rhizochromulina in the arctic waters (the White Sea), which involved the studies of cell morphology and ultrastructure coupled with phylogenetic analysis of this peculiar organism
Fig. 5. Participants of the Plenary Session of the IV All-Russian Conference "Frontiers in Plankton Research" (Svetlogorsk, Kaliningrad Region, Russia; 26 September 2022). Photos: K.A. Podgorny.
capable of amoeboid/flagellated states' transition (Safonov et al., 2022). These and other results prove that today only the combination of classical ecological and modern molecular techniques is capable of generating data that could provide robust species identification, unveil the origin of these species and their evolutionary relationships, and allow for predicting the functional role of the newly discovered organisms in aquatic communities. This cumulative knowledge advances hydrobiological studies securing their fundamental value and high
quality that are essential for mathematical modeling of the key ecological processes, to be used further for the purposes of environmental management and nature protection.
Outlook: Filling the gaps for the improved HABs modeling
Usage of the data on physiological peculiarities ofmicroorganisms, their high adaptive potential and intrapopulation variability for ecological modeling
has been discussed repeatedly in scientific literature (Smayda and Reynolds, 2001; Kreft et al., 2013; Hellweger et al., 2016; Schubert et al., 2017; Burford et al., 2020; Telesh et al., 2021, etc.) and at the professional forums (Podgorny and Dmitrieva, 2022). However, the practical application of this approach for the prognostic modeling of harmful blooms of, for example, dinoflagellates and cyanobacteria, is hampered by scarcity of the robust experimental numerical data on molecular and cellular features and intrapopulation heterogeneity of these microorganisms. In addition, the information on ecological niche dimensions of the HAB species is limited, being very scanty even for the toxic, most harmful and best studied species (Telesh et al., 2016). Besides, until recently, only very rare attempts have been undertaken to model the role of mixotrophy in primary productivity of ecosystems; moreover, those attempts were based mostly on hypotheses rather than on experimental data (Hammer and Pitchford, 2005). Indeed, the experimental investigation of mixotrophy regulation is impeded by methodological shortcomings; therefore, such studies are scarce (Burkholder et al., 2008; Moorthi et al., 2009; Gast et al., 2018). Meanwhile, the challenges ofprotistan mixotrophic strategy explains one of the greatest gaps in the ecosystem models (Flynn et al., 2019). In particular, the evaluation of consumption of organic nutrient substrates by planktonic microorganisms, as well as the reliable data on the balance of autotrophy and phagotrophy in mixotrophic nutrition of dinoflagellates, are required to fill up this gap in the future mathematical models.
Due to a number of impartial reasons, HABs modeling is complicated even in the closed experimental systems and lakes, not to mention the open coastal and estuarine ecosystems (Burford et al., 2020; Behrenfeld et al., 2021). Laboratory investigations that provide data for models most often admit that algal cells are distributed regularly and, therefore, the turbulent water flows and water retention rates are largely underscored. However, water mixing processes are crucial in natural ecosystems (Bauer et al., 2013), as well as prolonged abiotic stability is critical for HABs initiation (Telesh et al., 2021). Besides, the models often ignore trophic interactions of microorganisms in plankton communities (Khanaychenko et al., 2019). They also tend to disregard stochastic events like extreme weather conditions acting as external HAB triggers, as well as the nonlinear internal drivers of blooms
(Benincà et al., 2008, 2015; Boeing, 2016; Hellweger et al., 2016; Liu et al., 2018; Telesh et al., 2019, 2020, 2021; Burford et al., 2020). At the same time, the recent publications repeatedly stress the necessity of actual mathematical models ofpopulation dynamics of dominant bloom-forming algal species targeted at forecasting their hazardous outbursts in marine coastal waters (Zvalinsky and Tishchenko, 2016; Burford et al., 2020).
Thus, the development of mechanistic mathematical models allowing for HABs forecasting can be considered as a pressing research priority in planktonology. Ideally, such models have to (1) base on fundamental principles of population ecology of aquatic organisms, ecological physiology and production hydrobiology (Alimov et al., 2013); (2) take into account the ecological niche dimensions of the blooming species (Telesh et al., 2016); (3) recognize the basic rules of chaotic oscillations of microorganisms' populations (Huisman and Weissing, 1999); and (4) consider the knowledge of their metabolism (Stoecker et al., 2017; Leles et al., 2018), cellular-molecular features and life cycles (Figueroa et al., 2018). Therefore, the above-mentioned research directions can be viewed as the major prospects in modern HAB studies (Travin et al., 2020; Behrenfeld et al., 2021; Wells et al., 2021), as well as in planktonology and aquatic ecology in general (Fig. 6). The advanced methods for the forecasting of harmful algal blooms, based on the present-day knowledge of ecological requirements, functional modes, feeding strategies and cellular-molecular organization of microorganisms, will promote the understanding of bloom patterns and support the effective environmental management aimed at reducing the deteriorating effects of HABs on aquatic biocenoses, fisheries, human well-being and quality of the environment.
Acknowledgements
This research was supported by the Russian Science Foundation project # 22-14-00056.
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