Current issue
In press
Archives
About the Journal
Focus and Scope
Editorial Team
Contact
Journal Policies
Journal History
Indexing
Sponsorship
Most read articles
Instruction for Authors
Author guidelines
Submission
Authorship
Copyright Notice
Privacy Statement
Author Fees
PB Society
PB Society
Acta Agrobotanica
Acta Mycologica
Wiadomości Botaniczne
Monographiae Botanicae
RESEARCH PAPER
The first report of the production of anatoxin-a by Bolivian terrestrial cyanobacteria
1
W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, 31-512 Kraków, Poland
2
Laboratory of Metabolomics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland
3
Department of Medicinal Chemistry, Faculty of Pharmacy, Jagiellonian University Medical College, Medyczna 9, 30-688 Kraków, Poland
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2023-07-27
Final revision date: 2023-10-31
Acceptance date: 2023-12-29
Online publication date: 2024-03-28
Publication date: 2024-03-28
Corresponding author
Michał Adamski
W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, 31-512 Kraków, Poland
W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, 31-512 Kraków, Poland
Acta Soc Bot Pol 2024;93:
KEYWORDS
TOPICS
ABSTRACT
Cyanobacterial harmful algal blooms (CyanoHABs) are observed in many regions worldwide with increasing frequency. The massive development of cyanobacteria is a severe problem for the water environment due to negative changes in water parameters, the introduction of toxic metabolites (cyanotoxins) into the water, and the resulting disruption of ecological relations in the ecosystem. Knowledge regarding CyanoHABs in aquatic reservoirs is increasing. However, information about cyanobacteria development in other, untypical habitats like deserts, open soils, or polar regions is still insufficient. Similarly, data regarding the distribution of cyanotoxins are extensive for some regions (for example, in Europe or North America), whereas, in other localities, such as those in South America, the data are scarce. In this paper, we investigated if phototrophic microbial communities collected from open soil (La Paz department, Sud Yungas province, Bolivia) contained cyanobacteria described as cyanotoxin producers. We performed qualitative and quantitative analysis of typical cyanotoxins found in aquatic reservoirs – anatoxin-a (ATX-a), cylindrospermopsin (CYN), and microcystin-LR (MC-LR). The obtained results showed a relatively high biodiversity of the studied microbial phototrophic community, which consists of several cyanobacterial and algal genera. Analyses of cyanotoxins showed that CYN and MC-LR were not present in the studied samples. However, despite the lack of cyanobacteria described as ATX-a producers, high-performance liquid chromatography (HPLC) chromatograms were revealed, and mass spectrometry (MS) spectra confirmed the presence of the toxin in the studied material. The results presented in this paper are, to the best of our knowledge, the first confirmation of the presence of ATX-a in open soil habitats, as well as the first record of cyanotoxin occurrence in Bolivia. The identification of anatoxin-producing cyanobacteria in open soil environments presents a novel finding that necessitates further work to elucidate their prevalence, abundance, and associated potential hazards, as well as the taxonomic classification of the specific cyanobacterial species able for anatoxin synthesis within these soil habitats. Future studies should focus on the distribution of cyanotoxins in cyanobacterial communities in untypical habitats and in localities for which, to date, the information on cyanotoxin occurrence is not currently available.
ACKNOWLEDGEMENTS
We are greatly indebted to the staff of the Herbario Nacional de Bolivia, Instituto de Ecología, Universidad Mayor de San Andrés, La Paz, for their generous long-term cooperation. AF thanks also to Silvia C. Gallegos (La Paz) and Pamela Rodriguez de Flakus (Krakow) for their invaluable assistance during the fieldwork. LC/MS analyses were carried out with use of research infrastructure financed by Polish Operating Programme for Intelligent Development POIR 4.2 project no. POIR.04.02.00-00-D023/20-00.
FUNDING
LC/MS analyses were carried out with use of research infrastructure financed by Polish Operating Programme for Intelligent Development POIR 4.2 project no. POIR.04.02.00-00-D023/20-00.
CONFLICT OF INTEREST
No competing interests have been declared.
REFERENCES (65)
1.
Adamski M., Chrapusta E., Bober B., Kamiński A., Białczyk J. (2014). Cylindrospermopsin: Cyanobacterial secondary metabolite. Biological aspects and potential risk for human health and life. Oceanological and Hydrobiological Studies. 43 (4): 442-449.
2.
Adamski M., Wołowski K., Kaminski A., Hindáková A. (2020). Cyanotoxin cylindrospermopsin producers and the catalytic decomposition process: A review. Harmful Algae. 98.
3.
Adamski M., Zimolag E., Kaminski A., Drukała J., Bialczyk J. (2021). Effects of cylindrospermopsin, its decomposition products, and anatoxin-a on human keratinocytes. Science of the Total Environment. 765.
4.
Adamski M., Zmudzki P., Chrapusta E., Bober B., Kaminski A., Zabaglo K., Latkowska E., Bialczyk J. (2016a). Effect of pH and temperature on the stability of cylindrospermopsin. Characterization of decomposition products. Algal Research. 15: 129-134.
5.
Adamski M., Zmudzki P., Chrapusta E., Kaminski A., Bober B., Zabaglo K., Bialczyk J. (2016b). Characterization of cylindrospermopsin decomposition products formed under irradiation conditions. Algal Research. 18: 1-6.
6.
Al-Ghelani H. M., AlKindi A. Y., Amer S., Al-Akhzami Y. (2005). Harmful algal blooms: Physiology, behavior, population dynamics and global impacts - A review. Sultan Qaboos University Journal for Science [SQUJS]. 10: 1-30.
7.
Antoniou M. G., de la Cruz A. A., Dionysiou D. D. (2005). Cyanotoxins: New generation of water contaminants. Journal of Environmental Engineering. 131 (9): 1239-1243.
8.
Barros M. U. G., Wilson A. E., Leitão J. I. R., Pereira S. P., Buley R. P., Fernandez-Figueroa E. G., Capelo-Neto J. (2019). Environmental factors associated with toxic cyanobacterial blooms across 20 drinking water reservoirs in a semi-arid region of Brazil. Harmful Algae. 86: 128-137.
9.
Bartram J., Carmichael W. W., Chorus I., Jones G., Skulberg O. M., Chorus I., Bartman J. (1999). Toxic cyanobacteria in water: A guide to their public health consequences, monitoring and management. 1-12. E & FN Spon.
10.
Botes D. P., Kruger H., Viljoen C. C. (1982). Isolation and characterization of four toxins from the blue-green alga, Microcystis aeruginosa. Toxicon. 20 (6): 945-954.
11.
Campos A., Redouane E. M., Freitas M., Amaral S., Azevedo T., Loss L., Máthé C., Mohamed Z. A., Oudra B., Vasconcelos V. (2021). Impacts of microcystins on morphological and physiological parameters of agricultural plants: A review. Plants. 10 (4).
12.
Chiswell R. K., Shaw G. R., Eaglesham G., Smith M. J., Norris R. L., Seawright A. A., Moore M. R. (1999). Stability of cylindrospermopsin, the toxin from the cyanobacterium, cylindrospermopsis raciborskii: Effect of pH, temperature, and sunlight on decomposition. Environmental Toxicology. 14 (1): 155-161.
13.
Chorus I., Bartram J. (1999). Toxic cyanobacteria in water - A guide to their public health consequences, monitoring and management. World Health Organization, E & FN Spon.
14.
Chrapusta E., Węgrzyn M., Zabaglo K., Kaminski A., Adamski M., Wietrzyk P., Bialczyk J. (2015). Microcystins and anatoxin-a in Arctic biocrust cyanobacterial communities. Toxicon. 101: 35-40.
15.
Christensen V. G., Maki R. P., Stelzer E. A., Norland J. E., Khan E. (2019). Phytoplankton community and algal toxicity at a recurring bloom in Sullivan Bay, Kabetogama Lake, Minnesota, USA. Scientific Reports. 9 (1).
16.
Cirés S., Casero M. C., Quesada A. (2017). Toxicity at the edge of life: A review on cyanobacterial toxins from extreme environments. Marine Drugs. 15 (7).
17.
Codd G. A., Morrison L. F., Metcalf J. S. (2005). Cyanobacterial toxins: Risk management for health protection. Toxicology and Applied Pharmacology. 203: 264-272.
18.
Corbel S., Mougin C., Bouaïcha N. (2014). Cyanobacterial toxins: Modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere. 96: 1-15.
19.
de La Cruz A. A., Hiskia A., Kaloudis T., Chernoff N., Hill D., Antoniou M. G., He X., Loftin K., O’Shea K., Zhao C., Pelaez M., Han C., Lynch T. J., Dionysiou D. D. (2013). A review on cylindrospermopsin: The global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environmental Sciences: Processes and Impacts. 15 (11): 1979-2003.
20.
Dittmann E., Wiegand C. (2006). Cyanobacterial toxins - Occurrence, biosynthesis and impact on human affairs. Molecular Nutrition and Food Research. 50 (1): 7-17.
21.
Eriksson J. E., Toivola D., Meriluoto J. A. O., Karaki H., Han Y. G., Hartshorne D. (1990). Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases. Biochemical and Biophysical Research Communications. 173 (3): 1347-1353.
22.
Ettl H., Gärtner G. (1995). Syllabus der Boden-, Luft- und Flechtenalgen. Gustav Fischer.
23.
Filatova D., Picardo M., Núñez O., Farré M. (2020). Analysis, levels and seasonal variation of cyanotoxins in freshwater ecosystems. Trends in Environmental Analytical Chemistry. 26.
24.
Fiore M. F., Genuário D. B., da Silva C. S. P., Shishido T. K., Moraes L. A. B., Neto R. C., Silva-Stenico M. E. (2009). Microcystin production by a freshwater spring cyanobacterium of the genus Fischerella. Toxicon. 53 (7–8): 754-761.
25.
Harada K. I., Tsuji K., Watanabe M. F., Kondo F. (1996). Stability of microcystins from cyanobacteria - III. Effect of pH and temperature. Phycologia. 35: 83-88.
26.
Hawkins P. R., Runnegar M. T. C., Jackson A. R. B., Falconer I. R. (1985). Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Applied and Environmental Microbiology. 50 (5): 1292-1295.
27.
Hindák F. (2008). Colour atlas of cyanophytes. Veda, Publishing House of the Slovak Academy of Sciences.
28.
Huertas M. J., Mallén-Ponce M. J. (2021). Dark side of cyanobacteria: Searching for strategies to blooms control. Microbial Biotechnology. 15 (5): 1321-1323.
29.
Huisman J., Codd G. A., Paerl H. W., Ibelings B. W., Verspagen J. M. H., Visser P. M. (2018). Cyanobacterial blooms. Nature Reviews Microbiology. 16 (8): 471-483.
30.
Humbert J. F. (2009). Handbook of Toxicology of Chemical Warfare Agents. 371-379. Academic Press. http://www.sciencedirect.com/science/article/pii/B9780123744845000274.
31.
Jaiswal P., Singh P. K., Prasanna R. (2008). Cyanobacterial bioactive molecules - An overview of their toxic properties. Canadian Journal of Microbiology. 54 (9): 701-717.
32.
John N., Baker L., Ansell B. R. E., Newham S., Crosbie N. D., Jex A. R. (2019). First report of anatoxin-a producing cyanobacteria in Australia illustrates need to regularly up-date monitoring strategies in a shifting global distribution. Scientific Reports. 9 (1).
33.
Khomutovska N., Sandzewicz M., Łach Ł., Suska-Malawska M., Chmielewska M., Mazur-Marzec H., Cegłowska M., Niyatbekov T., Wood S. A., Puddick J., Kwiatowski J., Jasser I. (2020). Limited microcystin, anatoxin and cylindrospermopsin production by cyanobacteria from microbial mats in cold deserts. Toxins. 12 (4).
34.
Kleinteich J., Wood S. A., Puddick J., Schleheck D., Küpper F. C., Dietrich D. (2013). Potent toxins in Arctic environments - Presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. Chemico-Biological Interactions. 206 (2): 423-431.
35.
Komárek J. (2013). Cyanoprokaryota. Heterocytous. Süßwasseflora von Mitteleuropa. Spektrum Akademischer Verlag.
36.
Komárek J., Anagnostidis K. (2000). Cyanoprokaryota. Chroococcales. Süßwasseflora von Mitteleuropa. Spektrum Akademischer Verlag.
37.
Komárek J., Anagnostidis K. (2005). Cyanoprokaryota. Oscillatoriales. Süßwasseflora von Mitteleuropa. Spektrum Akademischer Verlag.
38.
Kurmayer R. (2012). The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. Journal of Phycology. 47 (1): 200-207.
39.
Li D., Wu N., Tang S., Su G., Li X., Zhang Y., Wang G., Zhang J., Liu H., Hecker M., Giesy J. P., Yu H. (2018). Factors associated with blooms of cyanobacteria in a large shallow lake, China. Environmental Sciences Europe. 30 (1).
40.
Lone Y., Koiri R. K., Bhide M. (2015). An overview of the toxic effect of potential human carcinogen microcystin-LR on testis. Toxicology Reports. 2: 289-296.
41.
Malta J. F., Nardocci A. C., Razzolini M. T. P., Diniz V., Cunha D. G. F. (2022). Exposure to microcystin-LR in tropical reservoirs for water supply poses high risks for children and adults. Environmental Monitoring and Assessment. 194 (4).
42.
Massey I. Y., Al Osman M., Yang F. (2022). An overview on cyanobacterial blooms and toxins production: Their occurrence and influencing factors. Toxin Reviews. 41 (1): 326-346.
43.
Massey I. Y., Yang F. (2020). A mini review on microcystins and bacterial degradation. Toxins. 12 (4).
44.
Merel S., Walker D., Chicana R., Snyder S., Baurès E., Thomas O. (2013). State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environment International. 59: 303-327.
45.
Meriluoto J., Codd G. A. (2005). Toxic: Cyanobacterial monitoring and cyanotoxin analysis. Åbo Akademi University Press.
46.
Metcalf J. S., Codd G. A., Whitton B. A. (2012). Ecology of cyanobacteria II: Their diversity in space and time. 651-676. Springer Science & Business Media.
47.
Metcalf J. S., Richer R., Cox P. A., Codd G. A. (2012). Cyanotoxins in desert environments may present a risk to human health. Science of the Total Environment. 421: 118-123.
48.
Moore C. E., Puschner B., Peterson M., Talcott P. (2012). Small animal toxicology, 3rd. 533-540. Saunders Elsevier.
49.
Moreira C., Azevedo J., Antunes A., Vasconcelos V. (2013). Cylindrospermopsin: Occurrence, methods of detection and toxicology. Journal of Applied Microbiology. 114 (3): 605-620.
50.
Pouria S., de Andrade A., Barbosa J., Cavalcanti R. L., Barreto V. T. S., Ward C. J., Preiser W., Poon G. K., Neild G. H., Codd G. A. (1998). Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet. 352 (9121): 21-26.
51.
Puddick J., van Ginkel R., Page C. D., Murray J. S., Greenhough H. E., Bowater J., Selwood A. I., Wood S. A., Prinsep M. R., Truman P., Munday R., Finch S. C. (2021). Acute toxicity of dihydroanatoxin-a from Microcoleus autumnalis in comparison to anatoxin-a. Chemosphere. 263.
52.
Shams S., Capelli C., Cerasino L., Ballot A., Dietrich D. R., Sivonen K., Salmaso N. (2015). Anatoxin-a producing Tychonema (cyanobacteria) in European waterbodies. Water Research. 69: 68-79.
53.
Sivonen K. (1996). Cyanobacterial toxins and toxin production. Phycologia. 35: 12-24.
54.
Sivonen K., Schaechter M. (2009). Encyclopedia of microbiology. 290-307. Elsevier.
55.
Stanier R. Y., Kunisawa R., Mandel M., Cohen-Bazire G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews. 35 (2): 171-205.
56.
Sukenik A., Hadas O., Kaplan A., Quesada A. (2012). Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes - Physiological, regional, and global driving forces. Frontiers in Microbiology. 3.
57.
Sukenik A., Kaplan A. (2021). Cyanobacterial harmful algal blooms in aquatic ecosystems: A comprehensive outlook on current and emerging mitigation and control approaches. Microorganisms. 9 (7).
58.
Svirčev Z., Lalić D., Bojadžija Savić G., Tokodi N., Drobac Backović D., Chen L., Meriluoto J., Codd G. A. (2019). Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Archives of Toxicology. 93: 2429-2481.
59.
Teneva I., Stoyanov P., Belkinova D., Dimitrova-Dyulgerova I., Mladenov R., Dzhambazov B. (2012). Production of cyanobacterial toxins from two Nostoc species (Nostocales) and evaluation of their cytotoxicity in vitro. Journal of Bioscience and Biotechnology. 1 (1): 33-43.
60.
Tufariello J. J., Meckler H., Pushpananda K., Senaratne A. (1984). Synthesis of anatoxin-a: Very fast death factor. Journal of the American Chemical Society. 106 (25): 7979-7980.
61.
Via-Ordorika L., Fastner J., Kurmayer R., Hisbergues M., Dittmann E., Komarek J., Erhard M., Chorus I. (2004). Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: Detection of microcystins and microcystin genes in individual colonies. Systematic and Applied Microbiology. 27 (5): 592-602.
62.
Visser P. M., Verspagen J. M. H., Sandrini G., Stal L. J., Matthijs H. C. P., Davis T. W., Paerl H. W., Huisman J. (2016). How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae. 54: 145-159.
63.
Wilk-Woźniak E., Solarz W., Najberek K., Pociecha A. (2016). Alien cyanobacteria: An unsolved part of the “expansion and evolution” jigsaw puzzle?. Hydrobiologia. 764 (1): 65-79.
64.
Wood S. A., Biessy L., Puddick J. (2018). Anatoxins are consistently released into the water of streams with Microcoleus autumnalis-dominated (cyanobacteria) proliferations. Harmful Algae. 80: 88-95.
65.
Wood S. A., Mountfort D., Selwood A. I., Holland P. T., Puddick J., Cary S. C. (2008). Widespread distribution and identification of eight novel microcystins in antarctic cyanobacterial mats. Applied and Environmental Microbiology. 74 (23): 7243-7251.
| eISSN: | 2083-9480 |
| ISSN: | 0001-6977 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
