Occurrence in Water Environments

Anatoxin-a has a worldwide distribution that includes temperate, tropical and cold climatic regions (Fristachi &c Sinclair, 2008). Although the occurrence of ATX has been less frequently surveyed than that of microcystins, based on the available data, it is evident that a wide variability in ATX contents is reported from environmental freshwater samples (Testai et ah, 2016).

In the USA, surveys conducted in Florida in 1999 and 2000 did not detect ATX in most of the samples tested, but the maximum concentration found amounted to 156 pg/L (Fristachi & Sinclair, 2008); in Nebraska, variable ATX concentrations up to 35 pg/L were measured in water samples collected from eight reservoirs between 2009 and 2010 (Al-Sammak et ah, 2014), and the highest ATX levels (1170 pg/L) were found in Washington State, where three waterbodies had long-term recurring blooms (Trainer &c Hardy, 2015).

In Europe, a monitoring programme on 80 German lakes and reservoirs found ATX in 25% of the surveyed waterbodies and in 22% of water samples with a maximum total concentration of 13.1 pg/L (Bumke-Vogt et ah, 1999). In Finland, in a survey of 72 lakes with variable trophic state, nearly half of the blooms dominated by Dolicbospermum did not contain detectable ATX (Rapala &c Sivonen, 1998). Furthermore, in Finland, hepatotoxic blooms have been found to be twice as common as neurotoxic ones (Rapala & Sivonen, 1998). Among 20 Irish lakes investigated, homoanatoxin-a was found in four inland waters dominated by blooms of Dolicbospermum spp. at concentrations of up to 34 pg/L (Furey et ah, 2003).

In Kenya, seven lakes (two freshwater and five alkaline saline waters) and the hot spring mats of Lake Bogoria were investigated for cyanotoxins, and ATX was recorded in almost all of them, at up to 1260 pg/g dw but not as dissolved toxin (Kotut et ah, 2006). ATX concentrations up to 2.0 pg/g dw were detected in two alkaline Kenyan crater lakes, dominated by Artbrospira fusiformis (Ballot et ah, 2005).

A number of publications have addressed the production of ATX by benthic cyanobacteria: the highest toxin concentrations being reported in a river mat sample (8 mg/g dw) in France, formed by benthic Kamptonema (Pbormidium) formosum (Gugger et ah, 2005). Levels ranging from 1.8 to 15.3 pg ATX/g of lyophilised weight were detected in Pbormidium biofilms in the Tarn River (France) with high spatiotemporal variability and the highest concentrations being recorded at the end of the summer period (Echenique-Subiabre et al., 2018). The maximum ATX concentration in surface waters reported to date was found in a lake in Ireland (444 pg/L), where no surface blooms were previously observed, and as in the French case, the causative agent was a benthic cyanobacterium (James et ah, 1997). Benthic, mat-forming cyanobacteria are common also in New Zealand rivers, frequently populated by Phormidium, known to produce ATX and HTX, the latter at contents up to 4400 pg/g dw (Wood et ah, 2007b; Wood et ah, 2012). In a study motivated by dog deaths, Wood et ah (2017) reported moderate concentrations of ATX (25 pg/L) and high levels of dhATX (2,118 pg/L), indicating that the latter may be present in higher concentrations than estimated so far. These concentrations, however, are associated with benthic grab samples and do not represent concentrations in larger water volumes (see also section 12.8 on benthic sampling). For an example of animal poisoning at a recreational lake and possible implications for human health see also Box 5.6.

Benthic cyanobacterial mats dominated by Phormidium terebriformis, Microseira (Lyngbya) wollei, Spirulina subsalsa and Synechococcus big- ranulatus in the hot springs at the shore of Lake Bogoria (Kenya) contained MC and ATX (Krienitz et ah, 2003). Recently, periphytic and tychoplank- tic Tychonema have been identified as a producer of ATX and HTX in Italian alpine lakes (Salmaso et ah, 2016) and in a German lowland lake (Fastner et ah, 2018). However, identification at species level has not always been undertaken for benthic cyanobacteria (Puschner et ah, 2008; Faassen et ah, 2012), and it seems likely that more HTX-producing Oscillatoria or Phormidium/Microcoleus populations - and species - will be identified as research continues.

Anatoxin-a occurrence is not limited to freshwater; indeed, it has been found in brackish waters in samples collected off the coast of Poland in the Baltic Sea at the beginning of September (Mazur & Plinski, 2003) and in Chesapeake Bay (USA) at concentrations ranging from 3 x 10-5 to 3 mg/L (Tango & Butler, 2008). Although different planktonic and benthic genera occur and possibly dominate in brackish water (Nodularia, Aphanizomenon, Microcystis, Dolichospermum, Anabaena and Phormidium/Microcoleus), in these environments ATX seems to be produced exclusively by species formerly assigned to Phormidium (Lopes et ah, 2014). Moreover, ATX production was found in a benthic marine cyanobacterium (Hydrocoleum lyn- gbyaceum) in New Caledonia (Mejean et ah, 2010).

Biocrust-forming cyanobacteria inhabiting the Kaffioyra Plain (in the Arctic region) are able to synthesise ATX from 0.322 to 0.633 mg/g dw (Chrapusta et ah, 2015).

The available data and information have not linked ATX to human poisoning via drinking-water (Humpage, 2008). Surveys of cyanotoxins in drinking-water supplies in 1999/2000 across Florida found ATX only in three finished waters with concentrations up to 8.5 pg/L (Burns, 2008). Nevertheless, ATX should not be excluded as a potential human health hazard because some Oscillatoria sp. potentially producing ATX can proliferate in facilities and tanks for water storage (Osswald et al., 2007).

Bioaccumulation

The issue has been extensively reviewed in Testai et al. (2016). Anatoxin-a has been detected at low concentrations (0.51-43.3 pg/g) in Blue Tilapia fish in Florida (Burns, 2008). However, in Nebraska, this toxin could not be detected in fish from a reservoir although it was present in samples of the water and aquatic plants at the location (Al-Sammak et al., 2014). Concentrations similar to those in Tilapia were found in carp and juvenile trout exposed to high concentrations of ATX in an experimental setting (Osswald et al., 2007; Osswald et al., 2011); when mussels were experimentally exposed to live cells of an Anabaena strain (ANA 37), much lower levels were detected in the tissues (Osswald et al., 2008).

A special case of food items potentially containing ATX are “blue-green algal food supplements” (BGAS) that are usually produced from Spirulina maxima or Artbrospira (Spirulina) platensis and Apb. flosaquae. In Spirulina/ Arthrospira-based BGAS, no direct evidence of the presence of ATX has been reported, but two nontoxic metabolites of this toxin have been found at contents of up to 19 pg/g dw (Draisci et al., 2001). When 39 samples containing the genera Artbrospira, Spirulina and Apbanizomenon were analysed, three (7.7%) contained ATX at concentrations ranging from 2.5 to 33 pg/g dw (Rellan et al., 2009). See also section 5.4.

Environmental Fate

Partitioning Between Cells and Water

Anatoxins can be released from producing cells into the surrounding water, but very different results were reported in the ratio between the intra- and extracellular fractions, likely depending on the species and environmental conditions (Testai et al., 2016) as well as on the sensitivity of the analytical method used especially in earlier studies (Wood et al., 2011; Testai et al., 2016). There is currently no evidence that ATXs are released from viable, intact cells to a substantial degree. It may be hence concluded that ATXs are largely confined to viable cyanobacteria 1 cells in the environment and that extracellular release occurs mainly through cell senescence and lysis.

Once released from cells into the surrounding water, ATX can undergo chemical and biological degradation (Rapala 8c Sivonen, 1998) (see below). This is a challenge for its detection in environmental samples: the presence of ATX degradation products reported in some Finnish lakes at concentrations of 100-710 pg/L for еро-ATX and at 5-150 pg/L for dihydro-ATX (Rapala et al., 2005) indicates that ATX derivatives may serve as indicator of the previous presence of dissolved ATX.

Chemical Breakdown

In laboratory studies, ATX has been reported to undergo a rapid photochemical degradation in sunlight, under conditions of the light intensity and pH ranges expected to be associated with blooms: Stevens and Krieger (1991) observed the reaction rate to be positively related to both pH and light intensity, with half-lives for photochemical breakdown at pH>6 of 1.6-11.5 h, whereas at pH of 2, ATX was very stable. Kaminski et al. (2013) showed that ATX was resistant to photosynthetic active radiation with degradation dependent on pH: at low pH (<3), ATX proved stable when stored at room temperature, with minimal (<3%) losses over a period of 9 weeks, but gradual degradation (>37% losses) occurred at neutral (pH 7) and high pH (9.5). Anatoxin-a is relatively stable in the dark (Matsunaga et al., 1989), with a half-life of 4-10 days (Stevens & Krieger, 1991), at a pH of 9.

The mouse bioassay results show that regardless of process, photolytic or nonphotolytic, the breakdown products are of reduced toxicity and not antagonistic towards the effects of ATX (Stevens 8c Krieger, 1991).

In conclusion, once released from cyanobacterial cells and dissolved in water, ATX may degrade faster in water with high pH and further mitigating factors (e.g., microbial activity, elevated temperature), but may generally be more stable than previously assumed.

Biodegradation

Biodegradation by bacteria also has an important role: under natural conditions, ATX and HTX are partially or totally degraded and converted to dihydro- and epoxy-derivatives (James et al., 2005). Isolated Pseudomonas spp. degraded ATX at a rate of 2-10 pg/mL x day (Kiviranta et al., 1991), organisms in sediments reduced ATX concentrations by 25-48% in 22 days (Rapala et al., 1994), and a laboratory experiment with lake sediments and natural bacteria resulted in a half-life of 5 days (Kormas & Lymperopoulou, 2013).

Dihydroanatoxin-a has been considered the major ATX degradation product, representing from 17% to 90% of the total ATX concentration in the environment (Mann et al., 2011). Its concentrations gradually increased over time, paralleled by a decrease in ATX concentrations (Wood et al., 2011), although the involved enzymatic steps are not fully clarified. However, Heath et al. (2014) found that dhATX can account for 64% of the total intracellular ATX quota, suggesting that it is internally formed and is not only the product of cell lysis and environmental degradation, but is synthesised de novo in the cells.

In conclusion, due to the (photo)chemical and biological degradation of ATX and HTX, environmental samples invariably contain large amounts of these derivatives. Similar reactions can be expected to occur within biota, including mammals, although these have so far not been reported. Therefore, both environmental and forensic (e.g., in case of animal poisoning) analyses should also include an investigation of these degradation products.

 
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