Algal Toxins MIKE COLLINS Civil Engineering Department, University Ofmissouri, Columbia, Missouri 65211
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MICROBIOLOGICAL REVIEWS, Dec. 1978, p. 726-746 Vol. 42, No.4 0146-0749/78/0042-0725$02.00/0 Copyright i 1978 American Society for Microbiology Printed in U.S.A. Algal Toxins MIKE COLLINS Civil Engineering Department, University ofMissouri, Columbia, Missouri 65211 INTRODUCTION .............................. 725 CHLOROPHYCOPHYTA ............................... 725 Caulerpa spp.725.....................................................725 Cheatomorpha m inm 726 Uwva pp....................... 726 CYANOPHYCOPHYTA ..................... 727 Micrcyatis aen ...................................................... 727 Anabaenafloa-aqa e....................... 728 Aphaniamenonfl-aquae .......................... 729 Toxic manine Cyanophycophyta ...... ........................ 730 CHIRYSOPHYCOPHYTA .............................. 731 Prynesiumnparvum 731 Ochrdnwnas8 pp............................... 734 PYRRHOPHYCOPHYTA .............................. 734 Peridium polonicum .......................... 735 735 AmphidinSumaPP ............................ Noctilucna iluars ........................................................... 735 Gymnodinium app................................ 736 Gonyaulax app ................................... 738 RHODOPHIYCOPHYTA ....................... 739 LITERATURE CITED ....................... 741 INTRODUCTION CHLOROPHYCOPHYTA This is a literature review of the toxins pro- The Chlorophycophyta have been associated duced by algae. For this paper, only toxicity to with toxicity only in rare instances. Aside from multicellular organisms was considered. This the three genera discussed below, Prescott's eliminated a large number of publications deal- book The Algae: a Review (122) lists Chlorella ing with antibacterial and antiviral substances and Scenedesmus as death-inducing algae, but released by algae. Because the paper addresses information on these species is rare. those toxins produced by algae, the phenomenon of bioaccumulation of environmental contami- Caulerpa spp. nants is not discussed. Also not discussed is the one pathogenic algal genus, Prototheca, because The marine benthic green alga Caulerpa is there is no indication of a toxin being released responsible for the production of two toxic sub- (review by Sudman [165]). stances, namely, caulerpicin and caulerpin (4,38, What are discussed are a wide variety oftoxins 39). Both of these compounds have demon- produced by five phyla of algae: Chlorophyco- strated toxicity in mice. They were originally phyta (green algae), Cyanophycophyta (blue- isolated from C. racemosa but were also identi- green algae [cyanobactena]), Chrysophyco- fied in C. sertulariodes, C. lentillifera, and C. phyta (diatoms, yellow-green and golden algae), lamourouxii. It is interesting to note that Cau- Pyrrhophycophyta (dinoflagellates), and Rho- lerpa is probably the most popular edible alga dophycophyta (red algae). The types of mole- in the Philippines but becomes toxic during the cules involved are diverse, going from simple rainy months. The toxicity is believed to derive ammonia to complicated polypeptides and poly- from the agitation of the plant during the rainy saccharides. The physiological effects are also season (37). varied, ranging from the acute toxicity of para- The infrared spectrum ofcaulerpicin indicated lytic shellfish poison of Gonyaulax, leading to that this compound was a long-chain saturated death in a short period of time, to the chronic hydroxy amide. Aguilar-Santos and Doty (4) toxicity of carrageenans from red algae, which hypothesized from the spectral data that the induce carcinogenic and ulcerative tissue structure was as follows: changes over long periods of time. Perhaps the CH20H only link among this wide variety of toxin is I that each is produced by some form of alga. CH3-(CHI2)i3-- CH-NH-CO(CH2) -CH3 725 726 COLLINS MICROBIOL. REV. (n = 23, 24, 25). Mass spectral information led TABLE 1. Ichthyotoxic and hemolytic activities of them to believe that the actual substance was a fatty acids occurring in C. minima (from reference mixture of these homologous molecules. This 45) structure has not received full confirmation Hemo- Avg death timeb (144). The human physiological symptoms as- lytic ac- Fatty acid tivitya sociated with caulerpicin ingestion include (saponin 5 mg/100 ml 1 mg/100 ml numbness and a cold sensation of the extremi- units/mg) ties, rapid and difficult breathing, slight depres- 8:0 1.37 11 min (5) 44.6 min (5) sion, and eventually loss of balance. Depending 9:0 0.73 12 min (5) 34.2 min (5) on the dose, the effects are usually gone within 10:0 0.49 13 min (5) 6.6 h (4) a couple of hours to a day. 12:0 0.52 16 min (5) 20.2 min (5) Caulerpin was found to be a heterocyclic, red 14:0 2.48 9.4 h (2) (0) substance after it was crystallized from ether 16:0 3.01 (0) (0) extracts of the alga. It is a pyrazine derivative. 16:1 7.17 1.2 h (5) 2.4 h (5) Both spectral analysis and degradation reactions 18:0 0.35 15.2 h (3) (0) were used to determine the hypothesized struc- 18:1 4.52 2.5 h (5) 1.9 h (2) ture ofdimethyl 6,13-dihydrodibenzo[ b, i] phen- 18:2 9.49 2.8 h (1) (0) azine-5,12-dicarboxylate (Fig. 1) (144). 20:0 0.26 14.3 h (1) (0) a Estimated by the method of Oshima et al. (104) Cheatomorpha minima with 10% ethanol solution. b Numbers in parentheses indicate number offish in The organic extract from the green alga Chea- tomorpha minima has experimentally shown he- each group of five that died within 24 h. molytic activity and fish toxicity (ichthyotoxic- tion of a 70% ethanolic extract). After chemical ity) (45). The infrared spectrum of the organic separations, a total of three distinct hemolysins extract was typical for fatty acids, and the pre- were isolated from Ulva pertusa (44). Of the dominant species detected by gas-liquid chro- three hemolysins isolated, two were water solu- matography were palmitic (33%); palmitoleic ble and the third was fat soluble. The fat-soluble (12%); oleic, elaidic, and/or vaccenic (14%); and hemolysin was identified as palmitic acid (a C16 linoleic (10%) acids. The active, purified organic saturated fatty acid), with a hemolytic activity extract was obtained as a colorless solid which of 0.24 saponin unit per mg. killed killifish (Oryzias latipes) in 120 min at 5 Both of the water-soluble hemolysins were jig/ml and had a hemolytic activity of 1.99 sa- similar in chemical and physical parameters. ponin units (a quantitative measure ofhemolytic Although the final chemical structure has not activity for solid compounds) per mg (60). been elucidated for either of these substances, Eleven separate fatty acids from C. minima were many of the chemical and biological properties tested for ichthyotoxicity and hemolytic activity have been determined. On the basis of infrared (Table 1). The greater the saturation of the fatty spectra and combustion data, one water-soluble acid, the lower the hemolytic activity; however, substance is believed to be a galactolipid with a the saturation level did not correlate well with formula of C31H58014. This substance had a he- the ichthyotoxicity. molytic activity of 1.44 saponin units per mg, as the of Hashimoto and Osh- UOva spp. measured by method ima (60). The second substance is believed to be Another genus of the green algae which has a sulfolipid with a formula of C25H47011SK and hemolytic activity is the Ulva (activity found in a hemolytic activity of 2.01 saponin units per three separate species in the nondialyzable frac- mg. Both of the water-soluble hemolysins were tested on sea urchin (Hemicentrotus pulcherri- CO2CH mus) eggs according to the procedures of Rug- gieri and Nigrelli (133). This test is valuable for N determining developmental modifications (i.e., H animalization, fragmentation, radialized larvae, and abnormally formed plutei). At a concentra- tion of 0.001 ml of either hemolysin per 10 ml of N test solution (hemolysin plus seawater), both fertilized and unfertilized eggs were lysed. At a H CO2CH3 concentration of 0.0001 ml of hemolysin per 10 ml of test solution, neither fertilized nor unfer- FIG. 1. Caulerpin (from Scheuer [144]). tilized eggs were affected. Thus, the hemolysins VOL. 42, 1978 ALGAL TOXINS 727 did not produce developmental modification, one that causes the most harm (46). The deaths but they did induce toxicity. of many poultry and cattle have occurred as results of blooms of this alga (99); however, a CYANOPHYCOPHYTA toxic culture of this alga was shown by Gorham The Cyanophycophyta are one of the three (52) not to be the source of the poison(s) that phyla responsible for the majority of reported causes waterfowl sickness. The alga is found alga-caused deaths of fish, livestock, waterfowl, most frequently in shallow freshwater lakes and humans ponds. Although an M. aeruginosa toxic com- and (the other two are the Chrysophy- pound was the first algal toxin to be chemically cophyta and the Pyrrhophycophyta). This phy- characterized (in terms of which amino acids lum contains most of the genera of the fresh- were present in the polypeptide and the relative water toxic algae along with some of the toxic proportions of amino acids), the chemical struc- marine species. Of the more than 50 genera of tures of the toxins associated with this alga blue-green algae, at least 8 have exhibited toxic remain an enigma. characteristics; these include Anabaena, The NRC-1 strain of M. aeruginosa, isolated Aphanizomenon, Coelosphaerium, Gloeotri- by Gorham (52) and fellow workers, proved to chia, Lyngbea, Microcystis, Nodularia, and be toxic when administered