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Home , Cyanotoxin, Cylindrospermopsin

Harmful 98 (2020) 101894

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Harmful Algae

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Review producers and the catalytic decomposition T process: A review. ⁎ Michal Adamskia, , Konrad Wołowskia, Ariel Kaminskib, Alica Hindákovác a Department of Phycology, W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, 31-512 Kraków, Poland b Department of Plant Physiology and Development, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland c Department of Cryptogams, Institute of Botany, Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 23 Bratislava, Slovak Republic

ARTICLE INFO ABSTRACT

Keywords: Cylindrospermopsin (CYN) is a toxic produced by several freshwater species of cyano- . Its high chemical stability and wide biological activity pose a series of threats for human and animal Cylindrospermopsin morbidity and mortality. The biggest risk of CYN exposure for human organism comes from the consumption of contaminated water, fish or seafood. Very important for effective monitoring of the occurrence of CYNinaquatic Catalytic decomposition environment is accurate identification of cyanobacteria species, that are potentially able to synthesize CYN.In this review we collect data about the discovery of CYN production in cyanobacteria and present the morpho- logical changes between all its producers. Additionally we set together the results describing the catalytic de- composition of CYN.

1. Introduction Moreira et al. 2013, Flores-Rojas et al. 2019). CYN is an (C15H21N5O7S; 415.43 Da) with a tricyclic gua- Harmful algal blooms (HABs) occurring all over the world constitute nidine moiety, a group and a ring (Fig. 1) (Ohtani et al. serious ecological problems and contribute to biodiversity decline in 1992). The biological activity of this compound is wide and includes aquatic environments. The massive development of cyanobacteria or disruptions of several metabolic pathways. Primarily, CYN is an effec- algae radically worsens conditions in water reservoirs due to the ex- tive inhibitor of biosynthesis in both animal and plant cells cessive use of , increases the of water and disrupts (Harada et al. 2004, Metcalf et al. 2004, De la Cruz et al. 2013). The trophic networks (Huisman et al. 2018, Krztoń et al. 2019, results of many studies have shown that the influence of CYN leads to Hipsher et al. 2020). damage to nucleic acids and carcinogenesis (Pichardo et al. 2017). CYN It is believed that human activity, such as the production of sewage, also increases the concentration of free oxygen radicals and causes waste and high intensity agriculture, has the greatest impact on the oxidative stress (Štraser et al. 2013). Moreover, it was demonstrated to intensification of these phenomena (Pereira et al. 2017, drastically disrupt the proliferation of animal cells and reduce the mi- Park et al. 2017, Zuo 2019). Consequently, increased concentrations of totic index (Humpage et al. 2005, Moreira et al. 2013). biogenic chemical elements and the creation of favorable conditions for The above information clearly indicated that CYN is one of the most cyanobacteria or algae growth are observed. Moreover, many re- dangerous compounds synthesized by cyanobacteria. Therefore, it is a searchers have linked the formation of optimal conditions for cyano- serious threat to organisms that live in ecological niches similar to bacteria or algae in places where blooms have not occurred so far with cyanobacteria and to people using aquatic reservoirs in which HABs climate change and global warming (Mazard et al. 2016, occur. To date, many researchers have made efforts to broaden the Visser et al. 2016, Yan et al. 2017). knowledge about the fate of CYN in the environment and to develop HABs are particularly dangerous and require attention due to pro- effective methods to remove CYN from water. In recent decades, many duce toxic secondary metabolites, called cyanotoxins, that are released interesting and innovative results on this topic have been published. into the water (De la Cruz et al. 2013, Adamski et al. 2014, González- However, in these papers, information about cyanobacteria that are Pleiter et al. 2020). In recent years, cylindrospermopsin (CYN) has been able to synthesize CYN is limited. A summary of data characterizing one of the most commonly studied cyanotoxins (Merel et al. 2013, CYN producers could be helpful in future studies and potentially

⁎ Corresponding author. E-mail address: [email protected] (M. Adamski). https://doi.org/10.1016/j.hal.2020.101894 Received 24 February 2020; Received in revised form 18 August 2020; Accepted 22 August 2020 Available online 01 September 2020 1568-9883/ © 2020 Elsevier B.V. All rights reserved. M. Adamski, et al. Harmful Algae 98 (2020) 101894

was recorded in the Danube estuary, Don rivers and Swedish reservoirs (Wu et al. 2010, Komárek 2013). Schembri et al. (2001) studied the Australian A. bergii strain ANA283A. They confirmed that the genes responsible for CYN production (PKS and PS) are present in the genome of this cyanobacterium and determined that PKS and PS have different restriction fragment length polymorphisms (RFLPs) compared to other CYN-producing genes in organisms such as C. raciborskii. However, the nucleotide sequences and composition after expression were Fig. 1. of CYN: A – sulfate group, B – tricyclic similar (Schembri et al. 2001). moiety, C – uracil ring. In the same year, CYN was also extracted from Raphidiopsis curvata Fritsch et. Rich 1929 (Nostocales) cells (Fig. 2E) (Li et al. 2001). This contribute to a better assessment of the risks caused by CYN in water species is present in warm climates in areas such as Africa, and reservoirs where cyanobacteria blooms will develop. In this paper, we , where it lives in lentic freshwater reservoirs (Komárek 2013, described in detail the history of the discovery of CYN production in Aguilera et al. 2018). R. curvata has been described as a CYN producer, cyanobacteria. We collected all important morphological features of and R. curvata HB1 was isolated from a fish pond in Wuhan (China). species classified as CYN producers to date. This collate will be helpful The CYN concentration detected in cyanobacterial material was 0.56 µg for the rapid assessment of the potential of cyanobacteria g−1 dry weight. The authors also indicated that R. curvata synthesized forming blooms in natural aquatic environments. deoxy-CYN (1500 mg kg−1 dry weight), a toxic analog of CYN. This CYN has high chemical stability, and its rate of decomposition is research was also the first report of CYN and deoxy-CYN production in slow due to the influence of abiotic factors present in China (Li et al. 2001). (Chiswell et al. 1999, Wörmer et al. 2010, Adamski et al. 2016 a and b). In 2006, Preußel et al. published results indicating the ability of However, the results obtained by several research groups showed that flos-aquae Ralfs ex Bornet & Flahault 1886 (Nostocales) very promising methods of CYN decay involve catalysts. In (Fig. 2F) to produce CYN. This species is common and is present in all this review, we also collected results describing the catalytic decom- climate zones in eutrophic freshwater reservoirs with low turbidity. It is position of this published in the last decade. often a dominant microorganism in the microbial community, accom- panied by a high biodiversity of (Dean and Sigee 2006, Komárek 2013). A. flos-aquae strains studied by Preußel et al. (2006) 2. Cylindrospermopsin producers were isolated from two German lakes: Melangse (Eastern Brandenburg) and Heiliger See (Potsdam). They belonged to the three strains 10E6, For the first time, CYN was isolated from Cylindrospermopsis raci- 10E9 (from Melangse) and 22D11 (from Heiliger See). The CYN con- borskii (= Raphidiopsis raciborskii) (Woloszynska) Seenayya and Subba centrations detected in strains 10E6, 10E9 and 22D11 were 2.3, 3.2 and Raju 1972 (Fig. 2A), a cyanobacterium of the order Nostocales (Ohtani 6.6 mg g−1 dry weight, respectively (Preußel et al. 2006). et al. 1992). This species is present in the of mesotrophic or In the same year, the Finnish-Scottish research team identified CYN eutrophic freshwater, including large rivers. It originates from the in the extract from lapponica Borge 1913 (Nostocales) fila- tropical region but has high invasive potential; in , it develops in ments (Fig. 2G) (Spoof et al. 2006). This cyanobacterium has a the summer season, in waters as far north as Finland worldwide distribution and is common in Central and Eastern Europe, (Wilson et al. 2000, Komárek 2013). Drinking water from the Aus- , Japan, Brazil and Kerguelen Islands (Komárek 2013). tralian reservoir Solomon Dam (Queensland), in which blooms of C. Spoof et al. (2006) determined the CYN production ability of strain 966 raciborskii developed in 1979, caused illness in 148 people, mainly isolated from Lake Takajärvi (Southern Finland). The total amount of children. This incident, called the Palm island mystery disease, was CYN in cyanobacterial material was 242 µg g−1 dry weight (Spoof et al. classified as similar to hepatoenteritis based on the symptoms (Hawkins 2006). et al. 1985). At that time, data about the structure and toxicity of CYN Seifert et al. (2007) reported, for the first time, evidence for the were not available; therefore, the concentration of toxin in the water production of CYN by wollei (Farlow ex Gomont) Speziale and was not detected. Dyck 1992 (Oscillatoriales) (Fig. 2H). This cyanobacterium lives in Fifteen years later, Harada et al. (1994) purified CYN from Umezakia clean lentic or flowing freshwater reservoirs. Usually, it attaches to natans Watanabe 1987 (Nostocales) (Fig. 2B) isolated from Lake Mikata submersed stones and water plants. It is a dominant species in the (Fukui Prefecture). To date, this species has been described only in south-east USA and is widely present in southern Europe. Moreover, it large freshwater lakes in Japan (Niiyama et al. 2011). is present in the tropical zones of and India (Komárek and Later, CYN was purified from Aphanizomenon ovalisporum Forti 1911 Anagnostidis 2007, Kenins 2017). Samples of L. wollei analyzed by (Fig. 2C) (Nostocales) (Banker et al. 1997). This planktonic species lives Seifert et al. (2007) were collected from two rivers: Yabba Creek and in both freshwater and slightly saline reservoirs due to its high toler- Brisbane River (both southeast Queensland). The maximal detected ance to water conductivity. In Europe, this cyanobacterium has been concentration of CYN was 20 µg g−1 dry weight (Seifert et al. 2007). recorded in many countries, including the Czech Republic, Greece, Later, Wiedner et al. (2008) reported significant correlations be- Hungary and Italy. It is also widely distributed in Central Asia tween the particulate CYN concentrations and Aphanizomenon gracile (Zapoměllova et al. 2012, Komárek 2013). A. ovalisporum studied by Lemmermann 1907 (Nostocales) (Fig. 2I) biovolume in Langer See Lake Banker et al. (1997) was isolated from Lake Kinneret (Israel). Samples (Germany). This note is the first description of CYN production by this were collected from blooms formed during summer and autumn in cyanobacterium. A. gracile is a common species that is present in the 1994 (4000 trichomes per mL in October), but only once. In other years, whole zone. A. gracile usually lives in small lakes or ponds A. ovalisporum did not form intensive blooms in Lake Kinneret; the and is an element of plankton (Willame et al. 2006, Komárek 2013). cyanobacterial community was composed of the dominant taxa Micro- The maximum CYN concentration detected by Wiedner et al. (2008) in cystis aeruginosa and/or M. flos-aquae. Langer See was 1.8 µg L−1. However, it should be mentioned that the Another species described as a CYN producer was Anabaena bergii microbial community of these lakes was also composed of C. raciborskii (= Chrysosporum bergii) Ostenfeld 1908 (Nostocales) (Fig. 2D) and Aph. flos-aquae, other CYN producers (Wiedner et al. 2008). (Schembri et al. 2001). This cyanobacterium lives in the plankton layer In 2009, the production of CYN by Anabaena planctonica of warmer waters (above 20°C). A. bergii is present in brackish and salty Brunnthaler 1903 (Nostocales) (Fig. 2J) was confirmed (Brient et al. reservoirs, especially in Central and Eastern Asia. In Europe, A. bergii 2009). This species is present in the whole temperature zone in the

2 M. Adamski, et al. Harmful Algae 98 (2020) 101894

Fig. 2. Cyanobacteria able to synthesized CYN: A – Cylindrospermopsis raciborskii,B– Umezakia natans (after © Niyama et al. 2011), C – Aphanizomenon ovalisporum,D – Anabaena bergii,E– Raphidiopsis curvata (a – akinetes; after © Li et al. 2001, modified), F – Aphanizomenon flos-aquae,G– Anabaena lapponica,H– Lyngbya wollei after © Husk and Nieuwenhuis 2019). Fig. 2. cont. Cyanobacteria able to synthesized CYN: I – Aphanizomenon gracile,J– Anabaena planctonica (after © Hindák 2008), K – Oscillatoria sp., L – Raphidiopsis mediterranea.

3 M. Adamski, et al. Harmful Algae 98 (2020) 101894 plankton of lentic small waterbodies (Thomazeau et al. 2010). Brient and valuable for the removal of this toxin. Highly effective CYN de- et al. (2009) described CYN concentrations in eleven reservoirs in composition was observed in natural water matrices (from lakes and western France. A. planctonica was a dominant species at two sites: rivers to drinking water treatment plants) due to the influence of 2− − Boulet and Vern sur Seiche. The detected CYN concentrations in Boulet S2O8 , HSO5 or H2O2 excited by UV-254 nm. The obtained results −1 −1 2− and Vern sur Seiches were 1.95 µg L and 1.88 µg L , respectively. suggest that of the studied radicals, UV-254 nm/S2O8 was the most However, in addition to A. planctonica, other species able to synthesize efficient in CYN removal (He et al. 2014). This reaction also proceeded CYN, including Aph. flos-aquae or Oscillatoria sp., were also present in in the presence of natural organic matter (NOM) and nitrate, which these reservoirs (Brient et al. 2009). confirms the value of this method (He et al. 2014).

Next, CYN production ability was confirmed by completely se- CYN decomposition by a photocatalyst composed of TiO2 was also quencing the gene cluster responsible for the biosynthesis of the toxin in described by Zhang et al. (2014). They used a heteronanostructure Oscillatoria sp. Vaucher ex Gomont 1892 (Oscillatoriales) (Fig. 2K) catalyst (66% anatase, 22% brookite, 12% rutile) with a high surface strain PCC 6506 (Mazmouz et al. 2010). Moreover, in the study of area (207 m2 g−1) and small size (~5 nm) functioning during Mazmouz et al., it was documented that other strains of this genus are UV-VIS irradiation. Decomposition of CYN proceeded with high effi- also able to synthesize CYN (Mazmouz et al. 2010). Oscillatoria is pre- ciency; the total CYN concentration (1 µM) decreased within 20 min at sent all over the world except in cold climate zones, it forms blue-green all studied pH values (from pH 4 to 10.5). However, the influence of mats on the bottom of lakes and ponds (Komárek and Anagnostidis NOM (10 mg L−1) was very significant; NOM inhibited the reaction by 2007, Mühlsteinová et al. 2018). The intracellular and extracellular 95% compared to clean water (Zhang et al. 2014). Similar results were concentrations of CYN produced by Oscillatoria sp. strain PCC 6506 obtained for the tailored synthesis of anatase-brookite heterojunction detected by Mazmouz et al. (2010) were 0.10 and 0.11 µg per mg of dry TiO2 (ABH) photocatalysts under UV-VIS (El-Sheikh et al. 2017). The weight, respectively. anatase/brookite ratio was 61.8:38.2%, and the TiO2 nanoparticles To date, the last species characterized as a CYN producer is have mesostructures with highly active surface areas (maximum of Raphidiopsis mediterranea Skuja 1937 (Nostocales) (Fig. 2L) 62.3 m2 g−1). The studied catalyst decomposed CYN with high per- (McGregor et al. 2011). This planktonic cyanobacterium is usually formance (100% within 15 min, the 1st order reaction rate was 175 µM present in slightly eutrophic, shallow reservoirs. It lives in warm ha- min−1)(El-Sheikh et al. 2017). bitats sporadically outside the tropical climate zone (Komárek 2013, Commercially available TiO2 photocatalysts were also tested as Aguilera et al. 2018). R. mediterranea studied by McGregor et al. (2011) potential CYN removal factors. Fotiou et al. (2015) studied CYN de- was isolated from Lake Clarendon (Queensland, Australia) and belongs composition by Degussa P25 or Kronos vlp-7000 catalysts under the to strain FSS1-150/1. The concentration of CYN in dry weight was influence of UV-A, solar light or visible light. Both Degussa P25and 917 µg g−1. Kronos vlp-7000 contributed to complete CYN destruction under UV-A Morphological changes among all cyanobacteria known to synthe- (after 15 and 40 min, respectively) and solar light (after 40 and size CYN to date are presented in Table 1. 120 min, respectively). Kronos vlp-7000 activated by visible light was able to decompose but with relatively weak efficiency (15% 3. Catalytic CYN decomposition within 10 h). Under visible light, Degussa P25 did not induce a similar reaction. However, during UV-An irradiation, this catalyst performed The high chemical stability of CYN under the influence of abiotic CYN decomposition with complete toxin mineralization. The CYN de- factors such as pH, high temperature, photosynthetic active radiation composition pathway proposed by Fotiou et al. 2015 includes mod- (PAR) and UV radiation is a serious barrier in the effective removal of ifying the toxin structure by isomerization, removing a sulfate group, CYN from drinking water or food products made from fish or seafood breaking the hydroxymethyluracil ring or cleaving the tricyclic guani- (Chiswell et al. 1999, Wörmer et al. 2010, Adamski et al. 2016 a and b, dine moiety. The most likely attack of hydroxyl radicals on different Guzmán-Guillén et al. 2017, Maisanaba et al. 2018). Classically, sites of the CYN molecule was the main factor initiating its decay. The common methods used in drinking water treatment plants, such as proposed CYN decomposition pathway includes eighteen compounds destratification, filtration or methods with activated carbon, arecom- with m/z values ranging from 449.12 to 194.13. Some of them are si- paratively ineffective in CYN removal (De La Cruz et al. 2013, milar to products described after CYN chlorination or radiolysis (eight Moreira et al. 2013). Moreover, problems with toxin that compounds with m/z range from 319.08 to 447.11). Other products are remain on membranes or carbon layer during these processes can occur. characteristic of TiO2 photocatalytic reactions (ten byproducts with m/ In the last decade, many scientists have tried to broaden the knowledge z range from 194.13 to 449.12) (Fotiou et al. 2015). Zhang et al. (2015) on how to allow efficient and safe removal of CYN from water intended also characterized the reaction pathway of CYN destruction by TiO2 for consumption (De la Cruz et al. 2013, Moreira et al. 2013). Relatively photocatalysts (commercial Degussa P25 or lab synthesized PM-TiO2) new and feasible methods for the removal of cyanotoxins from water and described the decomposition products formed during this process. involve catalysts, especially photocatalysts (Antoniou and Andersen Hydroxyl radical attack of the CYN molecule was indicated as the main 2015, Antoniou et al. 2018). mechanism involved in toxin decomposition. •OH breaks the C–H bonds Pelaez et al. (2012) studied the stability of CYN after contact with and forms carbon-centered radicals that next react with oxygen and/or

NF-TiO2-P25 composite films under visible or UV light at pH 3.They hydroxyl radicals. As a consequence, , acid or are described weak CYN adsorption for these films and low degradation formed. Hydroxyl radicals also interfere with C]C double bonds and under visible light under the applied conditions. However, irradiation disrupt the structure of the guanidine moiety or cause the sulfate group with UV-VIS contributed to the better activation of films and more ef- to break. The CYN decomposition products described by fective CYN decomposition, which was 100% after 4 h Zhang et al. (2015) had an m/z range from 466.12 to 290.08 m/z. (Pelaez et al. 2012). The removal of dissolved CYN from water after reaction with hybrid It has been proven many times that the influence of the free radicals photocatalytic composites (HPCs) was described as satisfactory created during catalytic CYN decomposition is the main mechanism (Chae et al. 2019). HPCs prepared and described by Chae et al. (2019) causing effective toxin disintegration. It was documented that hydroxyl comprise carbon nanotubes on the surface of TiO2 nanotubes. The di- radicals (•OH) or sulfate radicals formed by UV-254 nm activation of mensions of TiO2 nanotubes formed on porous Ti foil were as follows: Di 2− peroxide (H2O2), peroxydisulfate (S2O8 ) and perox- ≈ 103 nm, Do ≈ 150 nm, L ≈ 7.6 nm, ≈ 49% porosity. Synthesized − ymonosulfate (HSO5 ) could effectively destroy toxin molecules HPCs have various amounts of ferrocene (0–100 mg) and have been (He et al. 2013). Research on the fate of CYN in natural water samples characterized by different carbon nanotube contents (maximally ≈ showed that advanced oxidation processes (AOPs) seem to be promising 9 mg−1 cm−2), contact angles as fabricated (maximally ≈139°),

4 .Aasi tal. et Adamski, M. Table 1 Morphological changes between cyanobacteria species able to synthesize CYN (based on: Dean and Sigee 2006, Komárek and Anagnostidis 2007, Wu et al. 2010, Niiyama et al. 2011, Zapomělova et al. 2012, Komárek 2013, Aguilera et al. 2018).

Species Trichom Cells Heterocytes Akinetes

Cylindrospermopsis Free-floating, solitary, cylindrical, slightly Cylindrical to barrel-shaped, 2.5–12 (16) × (1.7) Terminal at one or both trichome ends, drop-like, Near the ends of the trichomes, adjacent to heterocytes raciborskii tapering towards ends, straight or slightly 2–2.4 µm. Apical cells conically narrowed and rounded-pointed. or separate from them by one or few vegetative cells, bent, sometimes irregular screw-like coiled, rounded. solitary or rarely more than 3 in row, cylindrical-oval, notably and irregularly constricted at the (7) 8.5–18 (22) × (2.4) 3–5 (5.5). cross-walls, pale blue-green.

Umezakia natans Filaments solitary, free-floating, simple, Cylindrical to barrel-shaped, sometimes Spherical to elongated. Present only in environment Single or few in row, ellipsoidal, thick-walled, with a straight or slightly curved, in some cases with ellipsoidal, with aerotopes, longer than wide, with low concentration,7-9 × 6–8 µm. smooth surface, 10.5–8.7 × 7.4–1.0 µm. true branches (T-type), with tick, indistinct Apical cells with few or without aerotopes. End mucilaginous sheath. Trichomes attenuated cells rounded and cylindrical. at the ends, constricted or not constricted at the cross-walls, short (~50 µm) or long (> 3 cm), (4) 5–7 (8) µm wide, in apical part 2.5–3.5 µm wide.

Aphanizomenon Free-floating, solitary, straight or slightly Cylindrical, isodiametric, with poorly marked wall Spherical to ellipsoidal, (4.4) 6.1–12 × (4.8) Oval, usually separate from heterocytes, rarer joined to ovalisporum arcuate, slightly to distinctly constricted at and aerotopes, pale blue-green, (2.5) 3.5 up to 5–8.5 µm. them, yellow or brownish (13.6) the cross-walls, with attenuated ends, more 15 × (2.4) 3–5.1 µm. Terminal cells narrowed, 18–27.8 × 10.8–15.1 µm. than 1.5 mm. with rounded-pointed ends, 30 × 3–5 µm.

Anabaena bergii Free-floating, solitary, straight or slightly Isodiametric (sometimes shorter than wide), Solitary, intercalary, spherical, 8–10.2 µm in Solitary, intercalary, widely oval, with thick and arcuate, narrow toward ends, constricted at barrel-shaped, spherical or hemispherical, with diameter. colourless exospores, distant from heterocytes, the cross-walls, indistinct mucilaginous aerotopes, 4–8 × 8 µm in the centre of trichome. 21–24 × 10–20 µm.

5 envelopes is present. Apical cells narrowed. End cells elongated, conical-rounded, 6–8 µm long.

Raphidiopsis curvata Free-floating, solitary or in small clusters, With aerotopes, pale blue-green, (1.5) 2–4.5 µm ̶ Develop 1–2 aside. Subapically or in the middle of the usually sigmoidally coiled or irregularly wide, 1.5–2.5 times longer than wide. Terminal trichomes, barely-shaped or cylindrical-oval, with circular, rarely almost straight, not cells elongated, hyaline and pointed, long (up to truncate or rounded ends, sometimes slightly curved, constricted at the cross-walls. 20 µm). granular, yellowish, 10–16.1 × 3.9–5.2 (7.2) µm.

Aphanizomenon flos- Free-floating, straight or bent, cylindrical, Cylindrical to slightly barrel-shaped, isodiametric, Usually one in a trichome (sometimes up to 3), Intercalary, long, cylindrical, 40–220 × 6-10.8 µm. aquae slightly constricted at the cross-walls, with aerotopes, olive-green, 4–12.1 × 4.4–8 µm. solitary, intercalary, cylindrical 10–18 × 5–8.5 µm. isopolar, cylindrical rounded. Long terminal Apical cells elongated with remains of cytoplasm cells at the both ends. Aggregated in parallel, in lengthwise string form, almost hyaline, >24 µm elongated, band-like colonies, >2 × 3 mm. long.

Anabaena lapponica Filaments usually solitary, sometimes in Spherical or almost slightly citriform, very short Solitary, intercalary, spherical, associated at the Solitary, cylindrical, with rounded ends, with thick, small cluster, cylindrical, straight or slightly cross-walls, blue-green, 7–9.5 µm wide. both side with akinetes, 8–10.5 µm in diameter. smooth exposure, colourless, 75–85 × 11.5–13 (21) µm. flexuous, not attenuated towards ends, deeply constricted at the cross-walls.

Lyngbya wollei Filaments woolly, entangled, straight or Very short, discoid, with finely granular ̶ ̶

variously curved, with black-green to yellow- cytoplasm, 4–9 µm long. Apical cells rounded, Harmful Algae98(2020)101894 green tufts. Pseudo branches mostly solitary, without calyptra or thickened outer wall. breaking obliquely, hyaline to golden-yellow sheaths. Trichomes not constricted at the ungranulated cross-walls, dark blue-green or yellowish green, 28–47 µm wide. Aphanizomenon gracile Free floating, solitary, isopolar, Isodiametrical or a little longer than wide, Solitary, intercalary, usually just 1 or 2 in a Solitary (or few in row), short-cylindrical, in a subsymmetric, straight or slightly arcuate or cylindrical to slightly barrel-shaped, with trichome, separate by few vegetative cells from subsymmetric position in a trichome, (6.4) 7.8–14.7 coiled, cylindrical, with distinctly constrict at irregularly placed aerotopes, blue-green, (2) akinetes, 3.5–7.8 (9.8) × (2.5) 3–5.9 µm. (16.7–30) × (2.9) 3.9–5.9 (8) µm.

(continued on next page) .Aasi tal. et Adamski, M. Table 1 (continued)

Species Trichom Cells Heterocytes Akinetes

the cross-walls, slightly and continually 2.8–6.4 (8) × (2) 2.6–3.1 (4) µm in the central narrowed towards ends. part are. Terminal cell slightly elongated and narrowed, (3.6) 4.3–6.4 (12) × 1.5–2.1 (2.8). Apical cells rounded, often slightly capitate at the end.

Anabaena planctonica Free-floating, solitary, straight or slightly Shortly barel-shaped, with dark numerous Intercalary, solitary rounded, nearly spherical Intercalary, solitary (rarely in pairs or three in row), oval coiled, constricted at the cross-walls, not aerotopes, (3.2) 4–10 (13) × (7.7) 8–15 µm, blue- (sometimes slightly oval), (8) 9.4–15 (16) µm in or wide cylindrical, with rounded ends, always distant attenuated towards end, with indistinct green. End cells spherical and rounded. diameter. from heterocytes, colourless, 15-37 × 9–21 µm. mucilaginous envelopes. 2–3 terminal cells slightly narrower than other.

Oscillatoria sp. Thallus macroscopic, creates smooth, layered Short, discoid (in many cases 3-11 times shorter ̶ ̶ or sometimes leathery mats, rarely in solitary than wide) with homogenous or high granulated trichomes. Trichomes cylindrical, straight or cytoplasm, lacking aerotopes. slightly waved, in some cases screw-like coiled at the ends, not constricted or constricted at the cross-walls, rarely with sheaths (it occurs only in stressed conditions), motile. 6.8–70 µm wide.

Raphidiopsis Free-floating, solitary, straight, slightly bent Cylindrical, poses homogenous or optionally with ̶ Intercalary, solitary or few in row, cylindrical, long mediterranea or coiled, usually short but sometimes shaped solitary, elongated aerotopes, ends narrowed and ellipsoid or barrel-shaped, with granular cytoplasm and long (up to 2 mm), not or very less elongated with sharply pointed, light or greyish rounded or flattened ends, with smooth, colourless or constricted at the cross-walls, with pointed blue-green, mostly 2–5 (10) × longer than wide, brownish exposure, pale blue-green and granular

6 and narrow ends. At one or both ends free (0.8) 1–2.5 (3.3) µm wide in the middle. content, ends rounded or flattened, (5.5) 6.5–16 rounded segments. (32) × (2) 2.5–5.2 (6.4) µm. Harmful Algae98(2020)101894 M. Adamski, et al. Harmful Algae 98 (2020) 101894 diameters of carbon nanotubes (maximally ≈ 55 nm) and BET surface the bond between the uracil ring and guanidine moiety to break, and areas (maximally ≈ 17 m−2 g−1). HPCs have been used in combination consequently, compounds with m/z 319.3 and 275.5 were formed. The with commercially available nanofiltration (NF) membranes (NF 270, decomposition of the uracil ring finally led to the formation of a small with a molecular weight cutoff of 200–400 Da). The highest overall compound with two amino groups and m/z 85.9 (Wang et al. 2014). −1 efficiency of removing CYN (100 µgL ) was 70% within 2 hours and Sudrajat (2017) studied the delta phase of δ-Bi2O3 (without dopant) was obtained for HPC characterized as follows: carbon nanotube con- as a potential photocatalyst in CYN removal under UV light. The ob- tent (5.2 ± 0.4 mg cm−2), contact angle as fabricated (120 ± 4°), tained results suggest the high efficiency of this reaction system: the diameter of carbon nanotubes (38.0 ± 2.4 nm) and BET surface area initial CYN concentration (5 mg L−1) decreased by 98% within 20 min. (10.0 ± 0.5 m−2 g−1). The efficiency of CYN decomposition per- A very satisfactory reaction rate was achieved through a high level of formed under the applied conditions depended on size exclusion and catalyst crystallinity, high energy of the band gap and good efficiency of adsorption because of the relatively high of CYN. Hydro- ROS action. The advantage of this catalyst is its reusability and simple philic groups contained in the CYN structure cause less efficient re- bismuth recovery (Sudrajat 2017). moval of this toxin in comparison to more hydrophobic cyanotoxins The most important factor affecting CYN decomposition in both ti- (Chae et al. 2019). Chae et al. (2019) showed that optimized HPCs tanium- and bismuth-containing catalysts is ROS efficiency in toxin could be a good alternative for the removal of CYN from water. structure modification. He et al. (2014) described in detail the influence

The high performance of CYN removal via catalysts using TiO2 was of free radicals on CYN molecules during UV irradiation of H2O2. They also proven by applying the synthetic model compound 6-hydro- indicated that CYN decomposition can proceed through three main xymethyl uracil (6-HOMU) (Zhao et al. 2014a). Decomposition of CYN pathways. The first is the reaction of ROS with hydroxymethyl uracil was performed with several nonmetal-doped TiO2 materials: nitrogen ring leading to hydroxyl addition, dihydroxylation or secondary alcohol and fluorine-TiO2 (NF-TiO2); phosphorus and fluorine-TiO2 (PF-TiO2); oxidation. Byproducts with m/z range from 450 to 290 are formed in and sulfur-TiO2 (S-TiO2). The reaction was studied under the influence these reaction pathways. The second pathway of CYN molecule de- of visible or radiation. All studied catalysts showed high composition is the attack of ROS on the tricyclic guanidine moiety and effectiveness in CYN molecule disintegration during UV irradiation. The the formation of compounds with m/z range from 496 to 200. The high initial toxin amount was completely reduced within ≈30 min, 60 min m/z ratio of some products in this pathway is connected to the lack of and 120 min for S-TiO2, PF-TiO2 and NF-TiO2, respectively. Under an open guanidine moiety and the addition of hydroxyl groups, oxygen visible light, NF-TiO2 contributed to CYN decomposition (≈60% after or both. The last pathway includes separation of the sulfate group and 240 min), whereas S-TiO2 and PF-TiO2 did not induce similar reactions. insertion of the hydroxyl group, oxygen or both (byproducts with m/z The authors indicated that alkalization accelerated CYN breakdown by ratios from 334 to 432). Authors have suggested that in natural aquatic 2+ 3+ NF-TiO2 with visible light, while humic acid and ions (Ca and Fe ) environments, the influence of radicals such as carbonate radicals, did not influence this process. Analyses of several roles of ROShave singlet oxygen, and triple state natural organic matter and hydroxyl shown that superoxide is the most important factor in visible light NF- radicals could be important in CYN decomposition (He et al. 2014). The

TiO2 action (Zhao et al. 2014a). This research proved that NF-TiO2 collection of papers describing the catalytic systems used in the CYN activated by visible light could be a good alternative in all situations in decomposition process is presented in Table 2. which UV irradiation is undesirable. Under visible light, nitrogen-doped TiO2 (N-TiO2) has a satisfactory efficiency for C. raciborskii whole cell catalytic degradation. 4. Summary Jin et al. (2019) demonstrated the complete destruction of C. raciborskii 6 −1 −1 cells (5 × 10 cells mL ) by N-TiO2 (200 mg mL ) under visible light. Cyanobacterial blooms are important and common in the aquatic Cell lysis in the first step of degradation resulted in the release ofin- environment, often significant to humans. The good and correct as- ternal compounds, including CYN. The authors indicated that 96% of sessment of the risks caused by potentially toxic cyanobacteria growing released CYN (6.6 µg mL−1) was disintegrated under the applied con- in blooms is a very important issue. Knowledge of the morphological ditions. Similarly, 90% of the total organic matter was also destroyed changes and ecological niches of cyanobacteria could greatly contribute during the photocatalytic reactions (Jin et al. 2019). Some limitations to the study of the potential presence of cyanotoxins in aquatic re- of the described catalytic system seem to be the time needed to destroy servoirs. Consequently, there is an urgent need for effective monitoring cyanobacterial cells and decrease the CYN concentration (20 h). Hence, the action of N-TiO2 under visible light could be an interesting alter- Table 2 native in both cyanobacterial cells, and CYN degrades in places where List of catalytic systems used for CYN decomposition close artificial water reservoirs are treated by the continuous impact of Catalytic system References these factors (i.e., sewage treatment plants). Other types of catalysts studied for their function in CYN removal TiO2/UV Senogles et al. 2000 TiO2/UV Senogles et al. 2001 from included those containing bismuth oxide. NF-TiO2-P25 Pelaez et al. 2012 2 − − Wang et al. (2014) estimated CYN decomposition by bismuth oxybro- S2O8 /UV ; HSO5 /UV; H2O2/UV He et al. 2013 mide (BiOBr) under visible light (420 nm) or UV radiation. The action H2O2/UV He et al. 2014 of BiOBr irradiated by UV caused a decrease in the initial CYN con- BiOBr/UV-ViS Wang et al. 2014 PM-TiO /UV-Vis Zhang et al. 2014 centration (2 mg L−1) by 87% within 12 h, whereas complete toxin 2 NF-TiO2/UV; PF-TiO2/UV; S-TiO2/UV Zhao et al. 2014a cleavage was observed under visible light within 3.5 h. Similar results TiO2/UV Chen et al. 2015 were obtained for photolysis of the uracil ring; the decomposition of the TiO2/UV-A/Vis/solar light Fotiou et al. 2015 2− − uracil ring by this catalyst occurred more effectively under visible light. S2O8 /UV; HSO5 /UV; H2O2/UV He et al. 2014 It should be indicated, however, that the faster decay of CYN under TiO2/solar light Pinho et al. 2015 TiO2/UV-Vis Zhang et al. 2015 visible light probably caused a higher applied intensity than that under TiO2/ozonation Wu et al. 2015

UV light. Taking into account the harmful effects of UV irradiation and Carbon doped TiO2 (C–TiO2) Fotiou et al. 2016 the lack of visible light, BiOBr working evenly at a high intensity of Anatase–brookite heterojunction TiO2 (ABH) El-Sheikh et al. 2017 visible light could be a good alternative to other catalysts used in CYN Hybrid photocatalytic composites (HPCs) comprising Chae et al. 2019 carbon nanotubes on TiO nanotubes removal, i.e., in systems with a living organism. CYN decomposition 2 N-doped TiO2 (N-TiO2) Jin et al. 2019 products formed during BiOBr action under visible light resulted in the Fe3O4-R400/H2O2 Munoz et al. 2019 formation of three compounds. Oxidation of the toxin molecule caused

7 M. Adamski, et al. Harmful Algae 98 (2020) 101894 of the occurrence of cyanobacteria able to synthesize CYN. The high Anabaena flos-aquae (Cyanophyta): A synchrotron-based Fourier-transform infrared toxic potential of CYN and its wide biological activity has increased the study of lake micropopulations. Eur. J. Phycol. 41 (2), 201–212. https://doi.org/10. 1080/09670260600645907. attention of scientists willing to study this compound. It is crucial to El-Sheikh, S.M., Khedr, T.M., Zhang, G., Vogiazi, V., Ismail, A.A., O'Shea, K., Dionysiou, find a good method of removing this toxin from water, especially in D.D., 2017. Tailored synthesis of anatase–brookite heterojunction photocatalysts for sewage treatment plants. Catalyst decomposition of CYN often takes degradation of cylindrospermopsin under UV-Vis light. Chem. Eng. J. 310, 428–436. https://doi.org/10.1016/j.cej.2016.05.007. place during UV irradiation and seems to be a good way to efficiently Flores-Rojas, N.C., Esterhuizen-Londt, M., Pflugmacher, S., 2019. Uptake, growth, and decay this molecule. In recent years, the most popular and studied CYN pigment changes in Lemna minor L. exposed to environmental concentrations of photodecomposition catalysts have containing titanium in their struc- cylindrospermopsin. Toxins 11 (11), 650. https://doi.org/10.3390/toxins11110650. tures. Definitely, the short time needed to completely damage thetoxin Fotiou, T., Triantis, T., Kaloudis, T., Hiskia, A., 2015. Photocatalytic degradation of cy- lindrospermopsin under UV-A, solar and visible light using TiO2. Mineralization and is an advantage of these products. However, knowledge of the toxicity intermediate products. Chemosphere 119, S89–S94. https://doi.org/10.1016/j. of the decomposition products formed after catalysis must be enhanced. chemosphere.2014.04.045. Similarly, research on the fate of CYN in the natural environment, in- Fotiou, T., Triantis, T.M., Kaloudis, T., O'Shea, K.E., Dionysiou, D.D., Hiskia, A., 2016. Assessment of the roles of reactive oxygen species in the UV and visible light pho- cluding its degradation, should be undertaken. tocatalytic degradation of cyanotoxins and water and odor compounds using C- TiO2. Water Res. 90 (2016), 52–61. https://doi.org/10.1016/j.watres.2015.12.006. Declaration of Competing Interest González-Pleiter, M., Cirés, S., Wörmer, L., Agha, R., Pulido-Reyes, G., Martín-Betancor, K., Rico, A., Leganés, F., Quesada, A., Fernández-Piñas, F., 2020. Ecotoxicity as- sessment of from freshwater samples using a bioluminescent cyano- The authors declare that they have no known competing financial bacterial bioassay. Chemosphere 240. https://doi.org/10.1016/j.chemosphere.2019. 124966. interests or personal relationships that could have appeared to influ- Guzmán-Guillén, R., Maisanaba, S., Prieto Ortega, A.I., Valderrama-Fernández, R., Jos, Á., ence the work reported in this paper. Cameán, A.M., 2017. Changes on cylindrospermopsin concentration and character- ization of decomposition products in fish muscle (Oreochromis niloticus) by boiling and steaming. Food Control 77, 210V220. https://doi.org/10.1016/j.foodcont.2017. Acknowledgments 02.035. Harada, K.ichi, Ohtani, I., Iwamoto, K., Suzuki, M., Watanabe, M.F., Watanabe, M., Terao, We feel privileged to be able to honor the memory of Professor K., 1994. Isolation of cylindrospermopsin from a cyanobacterium Umezakia natans František Hindák, a magnificent phycologist and author of some photos and its screening method. Toxicon 32 (1), 73–84. https://doi.org/10.1016/0041- 0101(94)90023-X. presented in this article. 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