Abstract
Microcystins (MCs) are the most studied toxins of cyanobacteria in freshwater bodies worldwide. However, they are poorly documented in coastal waters in several parts of the world. In this study, we investigated the composition of cyanobacteria and the presence of microcystins (MCs) in several coastal aquatic ecosystems of Nigeria. Direct morphological analysis revealed that members of the genus Oscillatoria were dominant with five species, followed by Trichodesmium with two species in Nigerian coastal waters. Oso Ibanilo had the highest cyanobacterial biomass (998 × 103 cells/L), followed by Rivers Ocean (156 × 103 cells/L). Except for the Cross River Ocean, cyanobacteria were present in all the investigated aquatic ecosystems. Ten (10) out of twenty water bodies examined had detectable levels of MCs. Furthermore, genomic DNA analysis for the mcyE gene of microcystin synthetase (mcy) cluster showed identities higher than 86% (query coverage > 96%) with toxic strains of cyanobacteria in all the samples analyzed. Also, the sequences of samples matched those of uncultured cyanobacteria from recreational lakes in Southern Germany. Our findings indicate that the presence of toxic cyanobacteria in coastal waters of Nigeria is of public and environmental health concern.
Similar content being viewed by others
Abbreviations
- MCs:
-
Microcystins
- PCR:
-
Polymerase chain reaction
- NRPSs:
-
Nonribosomal peptide synthetases
- PKSs:
-
Polyketide synthases
References
Aguiar R, Fiore MF, Franco MW, Ventrella MC, Lorenzi AS, Vanetti CA, Alfenas AC (2008) A novel epiphytic cyanobacterial species from the genus Brasilonema causing damage to Eucalyptus leaves. J Phycol 44:1322–1334. https://doi.org/10.1111/j.1529-8817.2008.00584.x
Al-Kandari M, Al-Yamani FY, Al-Rifaie K (2009) Marine phytoplankton atlas of Kuwait’s waters. Kuwait Institute for Scientific Research, Kuwait
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Ayanlade A, Drake N (2016) Forest loss in different ecological zones of the Niger Delta, Nigeria: evidence from remote sensing. GeoJournal 81:717–735. https://doi.org/10.1007/s10708-015-9658-y
Beaver JR, Tausz CE, Scotese KC, Pollard AI, Mitchell RM (2018) Environmental factors influencing the quantitative distribution of microcystin and common potentially toxigenic cyanobacteria in U.S. lakes and reservoirs. Harmful Algae 78:118–128. https://doi.org/10.1016/j.hal.2018.08.004
Bittencourt-Oliveira MC, Piccin-Santos V, Gouvêa-Barros S (2012) Microcystin-producing genotypes from cyanobacteria in Brazilian reservoirs. Environ Toxicol 27:461–471. https://doi.org/10.1002/tox.20659
Bittencourt-Oliveira MC, Cordeiro-Araújo MK, Chia MA, et al (2016) Lettuce irrigated with contaminated water: photosynthetic effects, antioxidative response and bioaccumulation of microcystin congeners. Ecotoxicol Environ Saf 128 https://doi.org/10.1016/j.ecoenv.2016.02.014
Bittencourt-Oliveira MDC (2003) Detection of potential microcystin-producing cyanobacteria in Brazilian reservoirs with a mcyB molecular marker. Harmful Algae. 2:51–60. https://doi.org/10.1016/S1568-9883(03)00004-0
Buratti FM, Manganelli M, Vichi S, Stefanelli M, Scardala S, Testai E, Funari E (2017) Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch Toxicol 91:1049–1130. https://doi.org/10.1007/s00204-016-1913-6
Chia AM, Abolude DS, Ladan Z, Akanbi O, Kalaboms A (2009a) The presence of microcystins in aquatic ecosystems in Northern Nigeria: Zaria as a case study. Res J Environ Toxicol 3:170–178. https://doi.org/10.3923/rjet.2009.170.178
Chia AM, Oniye SJ, Ladan Z et al (2009b) A survey for the presence of microcystins in aquaculture ponds in Zaria, Northern-Nigeria: possible public health implication. African J Biotechnol 8:6282–6289. https://doi.org/10.5897/AJB09.1263
Chia MA, Auta ZZ, Esson AE, Yisa AG, Abolude DS (2019) Assessment of microcystin contamination of Amaranthus hybridus, Brassica oleracea, and Lactuca sativa sold in markets: a case study of Zaria, Nigeria. Environ Monit Assess 191:569. https://doi.org/10.1007/s10661-019-7725-4
Chia MA, Cordeiro-Araújo MK, Lorenzi AS, Bittencourt-Oliveira MDC (2017) Cylindrospermopsin induced changes in growth, toxin production and antioxidant response of Acutodesmus acuminatus and Microcystis aeruginosa under differing light and nitrogen conditions. Ecotoxicol Environ Saf 142 https://doi.org/10.1016/j.ecoenv.2017.04.015
Chia MA, Kwaghe MJ (2015) Microcystins contamination of surface water supply sources in Zaria-Nigeria. Environ Monit Assess 187:606. https://doi.org/10.1007/s10661-015-4829-3
Christiansen G, Molitor C, Philmus B, Kurmayer R (2008) Nontoxic strains of cyanobacteria are the result of major gene deletion events induced by a transposable element. Mol Biol Evol 25:1695–1704. https://doi.org/10.1093/molbev/msn120
Cordeiro-Araújo MK, Chia MA, Arruda-Neto JDDT et al (2016) Microcystin-LR bioaccumulation and depuration kinetics in lettuce and arugula: human health risk assessment. Sci Total Environ 566-567:566–567. https://doi.org/10.1016/j.scitotenv.2016.05.204
Cordeiro-Araújo MK, Chia MA, Bittencourt-Oliveira MDC (2017) Potential human health risk assessment of cylindrospermopsin accumulation and depuration in lettuce and arugula. Harmful Algae 68:217–223. https://doi.org/10.1016/j.hal.2017.08.010
Essien JP, Antai SP, Benson NU (2008) Microalgae biodiversity and biomass status in Qua Iboe Estuary mangrove swamp, Nigeria. Aquat Ecol 42:71–81. https://doi.org/10.1007/s10452-007-9083-5
Estela Silva-Stenico M, Sturion Lorenzi A, Teschke O, Souza Pamplona Silva C, Etchegaray A, Fatima Fiore M (2013) Antimicrobial cyanopeptide action on bacterial cells observed with atomic force microscopy. Curr Nanosci 9:141–148. https://doi.org/10.2174/1573413711309010024
Fiore MF, Sant’Anna CL, Azevedo MTDP et al (2007) The cyanobacterial genus Brasilonema, gen. nov., a molecular and phenotypic evaluation. J Phycol 43:789–798. https://doi.org/10.1111/j.1529-8817.2007.00376.x
Fujiki H, Suganuma M (2012) Tumor promoters - microcystin-LR, nodularin and TNF-α and human cancer development. Anticancer Agents Med Chem 11:4–18. https://doi.org/10.2174/187152011794941163
Cronberg G, Carpenter EJ, WWC (2004) Taxonomy of harmful cyanobacteria. In: Hallegraeff GM, Anderson DM, CEmbella AD (eds) Manual on harmful marine microalgae. Paris, p 793
Głowacka J, Szefel-Markowska M, Waleron M, et al (2011) Detection and identification of potentially toxic cyanobacteria in Polish water bodies. Acta Biochim Pol 58:321–333. doi: 10.18388/abp.2011_2242
Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hoppenrath DM, Elbrächter GM (2009) Marine phytoplankton. Schweizerbart Science Publishers, Stuttgart, Germany
Indabawa I (2010) Detection of variants of microcystin produced by Microcystis aeruginosa in some burrow pits of Kano, Nigeria. Bayero J Pure Appl Sci 2:189–197. https://doi.org/10.4314/bajopas.v2i1.58544
Isibor PO (2017) Oxidative stress biomarkers in Clarias gariepinus (Burchel, 1822) exposed to Microcystin-LR. Beni-Suef Univ J Basic Appl Sci 6:69–75. https://doi.org/10.1016/j.bjbas.2017.01.005
Jähnichen S, Jäschke K, Wieland F, Packroff G, Benndorf J (2011) Spatio-temporal distribution of cell-bound and dissolved geosmin in Wahnbach Reservoir: causes and potential odour nuisances in raw water. Water Res 45:4973–4982. https://doi.org/10.1016/j.watres.2011.06.043
Jochimsen EM, Carmichael WW, An J, Cardo DM, Cookson ST, Holmes CEM, Antunes MB, de Melo Filho DA, Lyra TM, Barreto VST, Azevedo SMFO, Jarvis WR (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–878. https://doi.org/10.1056/NEJM199803263381304
Joh G, Kim HS, Lee JH, et al (2011) Algal flora of Korea. National Institute of Biological Resources
Kim Tiam S, Gugger M, Demay J, le Manach S, Duval C, Bernard C, Marie B (2019) Insights into the diversity of secondary metabolites of Planktothrix using a biphasic approach combining global genomics and metabolomics. Toxins (Basel) 11:498. https://doi.org/10.3390/toxins11090498
Komárek J, Genuário DB, Fiore MF, Elster J (2015) Heterocytous cyanobacteria of the Ulu Peninsula, James Ross Island, Antarctica. Polar Biol 38:475–492. https://doi.org/10.1007/s00300-014-1609-4
Komárek J, Johansen JR (2015a) Chapter 3 - Coccoid cyanobacteria. In: Wehr JD, Sheath RG, Kociolek JPBT-FA of NA (Second E) (eds) Aquatic ecology. Academic Press, Boston, pp 75–133
Komárek J, Johansen JR (2015b) Chapter 4 - Filamentous cyanobacteria. In: Wehr JD, Sheath RG, Kociolek JPBT-FA of NA (Second E) (eds) Aquatic ecology. Academic Press, Boston, pp 135–235
Kraberg A, Baumann M, Dürselen CD (2010) Coastal phytoplankton: photo guide for Northern European Seas. Pfeil
Kurmayer R, Christiansen G (2009) The genetic basis of toxin production in cyanobacteria. Freshw Rev 2:31–50. https://doi.org/10.1608/frj-2.1.2
Lackey JB (1938) The manipulation and counting of river plankton and changes in some organism due to formalin preservation. U. S. Public Health Report 53:2080–2093
Lone Y, Koiri RK, Bhide M (2015) An overview of the toxic effect of potential human carcinogen Microcystin-LR on testis. Toxicol Reports 2:289–296. https://doi.org/10.1016/j.toxrep.2015.01.008
Lorenzi AS, Chia MA, Lopes FAC, Silva GGZ, Edwards RA, Bittencourt-Oliveira MC (2019) Cyanobacterial biodiversity of semiarid public drinking water supply reservoirs assessed via next-generation DNA sequencing technology. J Microbiol 57:450–460. https://doi.org/10.1007/s12275-019-8349-7
Lorenzi AS, Chia MA, Piccin-Santos V, Bittencourt-Oliveira MDC (2015) Microcystins and cylindrospermopsins molecular markers for the detection of toxic cyanobacteria: a case study of northeastern Brazilian reservoirs. Limnetica 34
Lorenzi AS, Cordeiro-Araújo MK, Chia MA, Bittencourt-Oliveira MC (2018) Cyanotoxin contamination of semiarid drinking water supply reservoirs. Environ Earth Sci 77. https://doi.org/10.1007/s12665-018-7774-y
Mankiewicz J, Tarczyńska M, Walter Z, Zalewski M (2003) Natural toxins from cyanobacteria. Acta Biol. Cracoviensia Ser, Bot
Nishizawa T, Ueda A, Asayama M, Fujii K, Harada KI, Ochi K, Shirai M (2000) Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J Biochem 127:779–789. https://doi.org/10.1093/oxfordjournals.jbchem.a022670
Ostermaier V, Kurmayer R (2009) Distribution and abundance of nontoxic mutants of cyanobacteria in lakes of the Alps. Microb Ecol 58:323–333. https://doi.org/10.1007/s00248-009-9484-1
Park JG (2012a) Cyanophyta: Cyanophyceae: Chroococcales, Oscillatoriales Freshwater Cyanoprokaryota I. Algal Flora of Korea Flora and Fauna of Korea 5:82
Park JG (2012b) Cyanophyta: Cyanophyceae: Chroococcales, Oscillatoriales Freshwater Cyanoprokaryota II. Algal Flora of Korea 5:117
Pestana CJ, Reeve PJ, Sawade E, Voldoire CF, Newton K, Praptiwi R, Collingnon L, Dreyfus J, Hobson P, Gaget V, Newcombe G (2016) Fate of cyanobacteria in drinking water treatment plant lagoon supernatant and sludge. Sci Total Environ 565:1192–1200. https://doi.org/10.1016/j.scitotenv.2016.05.173
Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, Borner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci U S A 101:568–573. https://doi.org/10.1073/pnas.0304489101
Ren Y, Yang M, Chen M, Zhu Q, Zhou L, Qin W, Wang T (2017) Microcystin-LR promotes epithelial-mesenchymal transition in colorectal cancer cells through PI3-K/AKT and SMAD2. Toxicol Lett 265:53–60. https://doi.org/10.1016/j.toxlet.2016.11.004
Silva-Stenico ME, Silva CSP, Lorenzi AS, Shishido TK, Etchegaray A, Lira SP, Moraes LAB, Fiore MF (2011) Non-ribosomal peptides produced by Brazilian cyanobacterial isolates with antimicrobial activity. Microbiol Res 166:161–175. https://doi.org/10.1016/j.micres.2010.04.002
Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan BA (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem Biol 7:753–764. https://doi.org/10.1016/S1074-5521(00)00021-1
Tonk L, Visser PM, Christiansen G, Dittmann E, Snelder EOFM, Wiedner C, Mur LR, Huisman J (2005) The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl Environ Microbiol 71:5117–5181. https://doi.org/10.1128/AEM.71.9.5177-5181.2005
Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe MF, Park HD, Chen GC, Chen G, Yu SZ (1996) Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17:1317–1321. https://doi.org/10.1093/carcin/17.6.1317
Vaitomaa J, Rantala A, Halinen K et al (2003) Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Appl Environ Microbiol 69:7289–7297. https://doi.org/10.1128/AEM.69.12.7289-7297.2003
Vergalli J, Fayolle S, Combes A, Franquet E, Comte K (2019) Persistence of microcystin production by Planktothrix agardhii (Cyanobacteria) exposed to different salinities. Phycologia. 59:24–34. https://doi.org/10.1080/00318884.2019.1664875
Zhang XX, Fu Z, Zhang Z, Miao C, Xu P, Wang T, Yang L, Cheng S (2012) Microcystin-LR promotes melanoma cell invasion and enhances matrix metalloproteinase-2/-9 expression mediated by NF-κB activation. Environ Sci Technol 46:11319–11326. https://doi.org/10.1021/es3024989
Zhou L, Yu H, Chen K (2002) Relationship between microcystin in drinking water and colorectal cancer. Biomed Environ Sci 15:166–171
Funding
This study was sponsored by grants from the São Paulo Research Foundation (FAPESP—2013/15296-2), the Brazilian National Research Council (CNPq—442083/2014-9), and Nigerian Tertiary Education Trust Fund National Research grant (TETF/NRF 2009). A.S.L. and M.A.C. were supported by FAPESP post-doctoral fellowships (Grant 2014/01913-2 and Grant 2014/26898-6 and 2013/11306-3).
Author information
Authors and Affiliations
Contributions
MOK, SI, JUO, OAO, TEU, and MAC conceived and designed the experiments. MOK, SI, JUO, OAO, and TEU carried out the experiments. MOK, MAC, and ASL analyzed the data. MOK, MAC, MCBO, and ASL wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Vitor Manuel Oliveira Vasconcelos
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 25 kb)
Rights and permissions
About this article
Cite this article
Kadiri, M.O., Isagba, S., Ogbebor, J.U. et al. The presence of microcystins in the coastal waters of Nigeria, from the Bights of Bonny and Benin, Gulf of Guinea. Environ Sci Pollut Res 27, 35284–35293 (2020). https://doi.org/10.1007/s11356-020-09740-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09740-x