Immunolocalisation of microcystins in colonies of the cyanobacterium Rivularia in calcareous streams
Sergio Marco A , Marina Aboal A C , Elena Chaves B , Iván Mulero B and Alfonsa García-Ayala BA Laboratorio de Algología, Departamento de Biología Vegetal, Facultad de Biología, Campus de Espinardo, Universidad de Murcia, E-30100 Murcia, Spain.
B Departamento de Biología Celular e Histologia, Facultad de Biología, Campus de Espinardo, Universidad de Murcia, E-30100 Murcia, Spain.
C Corresponding author. Email: maboal@um.es
Marine and Freshwater Research 63(2) 160-165 https://doi.org/10.1071/MF11168
Submitted: 19 July 2011 Accepted: 8 October 2011 Published: 28 November 2011
Abstract
The cyanobacterium Rivularia is often the dominant genus in unpolluted stretches of many calcareous streams. Previous studies have detected microcystins in field-collected colonies from Mediterranean streams in Spain. Because sheaths and mucilage represent a substantial part of the colonies, the localisation of microcystins within Rivularia colonies was tested with immunological methods to elucidate the role of mucilage in toxicity. Microcystins were localised inside the trichomes, in the filament sheaths and in the colonial mucilage. The presence of microcystins was also shown in some heterocysts, but no mircocystins were detected in multicellular hairs. We suggest that microcystins are important for a benthic organism growing slowly for much of the time, that some labour division may exists between the cells in the colony and that these immunological methods may be a useful alternative for microcystin detection.
Additional keywords: cell labour division, grazers.
References
Aboal, M., and Puig, M. A. (2009). Microcystin production in Rivularia colonies of calcareous streams from Mediterranean Spanish basins. Algological Studies 130, 39–52.| Microcystin production in Rivularia colonies of calcareous streams from Mediterranean Spanish basins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVGisA%3D%3D&md5=8188faebbacfe33550ab4d90e72a38d4CAS |
Aboal, M., Puig, M. A., Mateo, P., and Perona, E. (2002). Implications of cyanophyte toxicity on biological monitoring of calcareous streams in north-east Spain. Journal of Applied Phycology 14, 49–56.
| Implications of cyanophyte toxicity on biological monitoring of calcareous streams in north-east Spain.Crossref | GoogleScholarGoogle Scholar |
Aboal, M., Puig, M. A., and Asencio, A. D. (2005). Production of microcystins in calcareous Mediterranean streams: the Alhárabe River, Segura River Basin in south-east Spain. Journal of Applied Phycology 17, 231–243.
| Production of microcystins in calcareous Mediterranean streams: the Alhárabe River, Segura River Basin in south-east Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVSgtrg%3D&md5=e3b441d250486ba0a3d33ac10990ec37CAS |
Bajpai, R., Sharma, N. K., Lawton, L. A., Edwards, C., and Rai, A. K. (2009). Microcystin-producing cyanobacterium Nostoc sp. BHU001 from a pond in India. Toxicon 53, 587–590.
| Microcystin-producing cyanobacterium Nostoc sp. BHU001 from a pond in India.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislKmsrY%3D&md5=e7cbb3d0cddc6fc9ee992bdd5a4535d2CAS |
Barco, M., Lawton, L. A., Rivera, J., and Caixach, J. (2005). Optimization of the intracellular microcystin extraction for their subsequent analysis by high-performance liquid chromatography. Journal of Chromatography. A 1074, 23–30.
| Optimization of the intracellular microcystin extraction for their subsequent analysis by high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1KksL8%3D&md5=ae0e2f27492cf8ab8b4aa2e8ede46c13CAS |
Berrendero, E., Perona, E., and Mateo, P. (2008). Genetic and morphological characterisation of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. International Journal of Systematic and Evolutionary Microbiology 58, 447–460.
| Genetic and morphological characterisation of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlegt7k%3D&md5=8b27cfa46c68ad55282bf639dd7388e8CAS |
Bourrelly, P. (1970). ‘Les Algues d’Eau Douce, 3.’ (N. Boubée and Cie: Paris.).
Brzuzan, P., Wozny, M., Ciesielski, H., Luczynski, M., Gora, M., Kuzminski, H., and Dobosz, S. (2009). Microcystin-LR induced apoptosis and mRNA expression of p53 and cdkn1a in liver of whitefish (Coregonus lavaretus L.). Toxicon 54, 170–183.
| Microcystin-LR induced apoptosis and mRNA expression of p53 and cdkn1a in liver of whitefish (Coregonus lavaretus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsFOisrk%3D&md5=e87cf33efdac27345bda6229887ffb79CAS |
Chorus, I., and Bartram, J. (Eds). (1999). ‘Toxic Cyanobacteria in Water: A Guide to Public Health Significance, Monitoring and Management.’ (E. and F.N. Spon: London.)
Codd, G., Bell, S., Kaya, K., Ward, C., Beattie, K., and Metcalf, J. (1999). Cyanobacterial toxins, exposure routes and human health. European Journal of Phycology 34, 405–415.
| Cyanobacterial toxins, exposure routes and human health.Crossref | GoogleScholarGoogle Scholar |
Codd, G. A., Morrison, L. F., and Metcalf, J. (2005). Cyanobacterial toxins: risk management for health protection. Toxicology and Applied Pharmacology 203, 264–272.
| Cyanobacterial toxins: risk management for health protection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslWrtLs%3D&md5=7e66565c9358ac62f84ae830bdb9ce03CAS |
Dittmann, E., and Borner, T. (2005). Genetic contributions to the risk assessment of microcystin in the environment. Toxicology and Applied Pharmacology 203, 192–200.
| Genetic contributions to the risk assessment of microcystin in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslWrt7c%3D&md5=23c957fe7add10cea08f8dc28f56bfbaCAS |
Genuário, D. B., Silva-Stenico, M. E., Welker, M., Moraes, L. A. B., and Fiore, M. F. (2010). Characterization of a microcystin and detection of microcystin synthetase genes from a Brazilian isolate of Nostoc. Toxicon 55, 846–854.
| Characterization of a microcystin and detection of microcystin synthetase genes from a Brazilian isolate of Nostoc.Crossref | GoogleScholarGoogle Scholar |
Gerbersdorf, S. U. (2006). An advanced technique for immunolabelling of microcystins in cryosectioned cells of Microcystis aeruginosa PCC 7806 (cyanobacteria): implementation of an experiment with varying light scenarios and culture densities. Toxicon 47, 218–228.
| An advanced technique for immunolabelling of microcystins in cryosectioned cells of Microcystis aeruginosa PCC 7806 (cyanobacteria): implementation of an experiment with varying light scenarios and culture densities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnsl2itg%3D%3D&md5=542739f0c349e7b5e4fb990181efbfa0CAS |
Gjølme, N., and Utkilen, H. (1996). The extraction and the stability of microcystin-RR in different solvents. Phycologia 35, 80–82.
| The extraction and the stability of microcystin-RR in different solvents.Crossref | GoogleScholarGoogle Scholar |
Hurtado, I., Aboal, M., Zafra, E., and Campillo, D. (2008). Significance of microcystin production by benthic communities in water treatment systems of arid zones. Water Research 42, 1245–1253.
| Significance of microcystin production by benthic communities in water treatment systems of arid zones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvFyrtL8%3D&md5=3cb1a31a60aa618c022715624aafd061CAS |
Izaguirre, G., Jungblut, A. D., and Neilan, B. A. (2007). Benthic cyanobacteria (Oscillatoriaceae) that produce microcystin-LR, isolated from four reservoirs in southern California. Water Research 41, 492–498.
| Benthic cyanobacteria (Oscillatoriaceae) that produce microcystin-LR, isolated from four reservoirs in southern California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCmt7vN&md5=14bb317a26d542a4216086f98df579c3CAS |
Jang, M.-H., Ha, K., and Takamura, N. (2008). Microcystin production by Microcystis aeruginosa exposed to different stages of herbivorous zooplankton. Toxicon 51, 882–889.
| Microcystin production by Microcystis aeruginosa exposed to different stages of herbivorous zooplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlSisr4%3D&md5=ccb9a17711014dd41d0677ae54965c86CAS |
Kaebernick, M., Neilan, B. A., Borner, T., and Dittmann, E. (2000). Light and the transcriptional response of the microcystin biosynthesis gene cluster. Applied and Environmental Microbiology 66, 3387–3392.
| Light and the transcriptional response of the microcystin biosynthesis gene cluster.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFars74%3D&md5=21cabea89a4eb94c4e594ce1b809dcddCAS |
Krüger, T., Wiegand, C., Kun, L., Luckas, B., and Pflugmacher, S. (2010). More and more toxins around – analysis of cyanobacterial strains isolated from Lake Chao (Anhui Province, China). Toxicon 56, 1520–1524.
| More and more toxins around – analysis of cyanobacterial strains isolated from Lake Chao (Anhui Province, China).Crossref | GoogleScholarGoogle Scholar |
Kurmayer, R. (2011). The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions. Journal of Phycology 47, 200–207.
| The toxic cyanobacterium Nostoc sp. strain 152 produces highest amounts of microcystin and nostophycin under stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktF2lurk%3D&md5=f601669c0f834e1dc9cb00a76d2d77f1CAS |
Kurmayer, R., Christiansen, G., and Chorus, I. (2003). The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Applied and Environmental Microbiology 69, 787–795.
| The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtF2is74%3D&md5=2ebb16d5e62264820f178f8a74925347CAS |
Lawton, L. A., and Edwards, C. (2001). Purification of microcystins. Journal of Chromatography. A 912, 191–209.
| Purification of microcystins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1Wntrw%3D&md5=d0ec54fabfd2549c531c099b9bee6846CAS |
Lawton, L. A., Chambers, H., Edwards, C., Nwaopara, A. A., and Healy, M. (2010). Rapid detection of microcystins in cells and waters. Toxicon 55, 973–978.
| Rapid detection of microcystins in cells and waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFKnt7c%3D&md5=f022d95abb41cb29dafb18cae921218eCAS |
Li, H., Xie, P., Zhang, D., and Chen, J. (2009). The first study on the effects of microcystin-RR on gene expression profiles of antioxidant enzymes and heat shock protein-70 in Synechocystis sp. PCC6803. Toxicon 53, 595–601.
| The first study on the effects of microcystin-RR on gene expression profiles of antioxidant enzymes and heat shock protein-70 in Synechocystis sp. PCC6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslWqu7k%3D&md5=0a477d408dda9828157fe6cc0ffd29f4CAS |
Livingstone, D., and Whitton, B. A. (1984). Water chemistry and phosphatase activity of the blue-green alga Rivularia in upper Teesdale streams. Journal of Ecology 72, 405–421.
| Water chemistry and phosphatase activity of the blue-green alga Rivularia in upper Teesdale streams.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmtVOgt70%3D&md5=ee49d18c65373575628cf352c9152d9cCAS |
Mancini, M., Rodriguez, C., Bagnis, G., Liendo, A., Prosperi, C., Bonansea, M., and Tundisi, J. (2010). Cyanobacterial bloom and animal mass mortality in a reservoir from central Argentina. Brazilian Journal of Biology 70, 841–845.
| Cyanobacterial bloom and animal mass mortality in a reservoir from central Argentina.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FgtlOhtA%3D%3D&md5=18ac56ddd0c984a31a6ff2848bbdbdf5CAS |
Martins, J. C., Leao, P. N., and Vasconcelos, V. (2009). Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain. Toxicon 53, 409–416.
| Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVGit7s%3D&md5=b0bd819b5b11bd1db94403cd179795eeCAS |
Maruyama, T., Kato, K., Yokoyama, A., Tanaka, T., Hiraishi, A., and Park, H. D. (2003). Dynamics of microcystin-degrading bacteria in the mucilage of Microcystis. Microbial Ecology 46, 279–288.
| Dynamics of microcystin-degrading bacteria in the mucilage of Microcystis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FhtFejsw%3D%3D&md5=24d48ab0cd1988f7b363ff7a418a3170CAS |
Meriluoto, J., Ermsson, J. E., Harada, K. L., Dahlrm, A. M., Sivonen, K., and Carmichael, W. W. (1990). Internal surface reverse phase high-performance liquid chromatographic separation of the cyanobacterial peptide toxins microcystin-LR, -YR, -RR and nodularin. Journal of Chromatography. A 509, 390–395.
| Internal surface reverse phase high-performance liquid chromatographic separation of the cyanobacterial peptide toxins microcystin-LR, -YR, -RR and nodularin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltFSmsbc%3D&md5=27a68531ae6bcfdf8b7053ccad93d3c0CAS |
Mohamed, Z. A., El-Sharouny, H. M., and Ali, W. S. M. (2006). Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon 47, 584–590.
| Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsFaqtLs%3D&md5=cb19f91f9aeb7525af05d50164fe9a3dCAS |
Oudra, B., Dadi-El Andaloussi, M., and Vasconcelos, V. (2009). Identification and quantification of microcystins from a Nostoc muscorum bloom occurring in Oukaïmeden River (High-Atlas mountains of Marrakech, Morocco. Environmental Monitoring and Assessment 149, 437–444.
| Identification and quantification of microcystins from a Nostoc muscorum bloom occurring in Oukaïmeden River (High-Atlas mountains of Marrakech, Morocco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFaktw%3D%3D&md5=933cf4fa2f27929aae711b2b6af880b0CAS |
Pearson, L. A., Hisbergues, M., Börner, T., Dittmann, E., and Neilan, B. A. (2004). Inactivation of an ABC transporter gene, mcyH, results in loss of microcystin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Applied and Environmental Microbiology 70, 6370–6378.
| Inactivation of an ABC transporter gene, mcyH, results in loss of microcystin production in the cyanobacterium Microcystis aeruginosa PCC 7806.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSjurbJ&md5=45b6ecd0d8dd297865aaf1dc6f540d73CAS |
Pentecost, A., and Whitton, B. A. (2000). Limestones. In ‘The Ecology of Cyanobacteria’. (Eds B. A. Whitton and M. B. Potts.) pp. 233–255. (Kluwer Academic Publishers: Dordrecht, The Netherlands.)
Rantala, A., Fewer, D. P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Börner, T., and Sivonen, K. (2004). Phylogenetic evidence for the early evolution of microcystins synthesis. Proceedings of the National Academy of Sciences, USA 101, 568–573.
| Phylogenetic evidence for the early evolution of microcystins synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsFGntQ%3D%3D&md5=b3cf8222fbb27ddb35dd01c4284b9a59CAS |
Rohrlack, T., and Hyenstrand, P. (2007). Fate of intracellular microcystins in the cyanobacterium Microcystis aeruginosa (Chroococcales, Cyanophyceae). Phycologia 46, 277–283.
| Fate of intracellular microcystins in the cyanobacterium Microcystis aeruginosa (Chroococcales, Cyanophyceae).Crossref | GoogleScholarGoogle Scholar |
Shi, L., Charmichael, W. W., and Miller, I. (1995). Immuno-gold localization of hepatotoxins in cyanobacterial cells. Archives of Microbiology 163, 7–15.
| Immuno-gold localization of hepatotoxins in cyanobacterial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvVOhs7k%3D&md5=5c69f2d834bb1a8f6dbb287b74a4fb26CAS |
Sivonen, K., and Jones, G. (1999). Cyanobacterial toxins. In ‘Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management’. (Eds I. Chorus and J. Bartran.) pp. 41–111. (E. and F. N. Spon.: London.)
Spoof, L., Vesterkvist, P., Lindholm, T., and Meriluoto, J. (2003). Screening for cyanobacterial hepatotoxins, microcystins and nodularin in environmental water samples by reversed-phase liquid chromatography-electrospray ionisation mass spectrometry. Journal of Chromatography. A 1020, 105–119.
| Screening for cyanobacterial hepatotoxins, microcystins and nodularin in environmental water samples by reversed-phase liquid chromatography-electrospray ionisation mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos12rt7Y%3D&md5=f33fb0506fe5e9357dddafc4e5ed8754CAS |
Sternberger, L. A. (1986). ‘Immunocytochemistry.’ (John Wiley: New York.)
Underwood, G. J. C., Moulcott, M., Raines, C. A., and Waldron, K. (2004). Environmental effects on exopolymer production by marine benthic diatoms-dynamics, changes in composition and pathways of production. Journal of Phycology 40, 293–304.
| 1:CAS:528:DC%2BD2cXjvFeju7o%3D&md5=8eb51b8862fb98e94107301eaf1d2b88CAS |
Via-Ordorika, L., Fastner, J., Kurmayer, R., Hisbergues, M., Dittmann, E., Komárek, J., Erhard, M., and 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, 592–602.
| Distribution of microcystin-producing and non-microcystin-producing Microcystis sp in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVShsbnL&md5=2e6745c6fa463097aef9d2b4ddd77819CAS |
Whitton, B. A. (1987). The biology of Rivulariaceae. In ‘The Cyanobacteria – A Comprehensive Review’. (Eds P. Fay and C. van Baalen.) pp. 513–534. (Elsevier: Amsterdam, The Netherlands.)
Whitton, B. A., Al-Shehri, A. M., Ellwood, N. T. W., and Turner, B. (2005). Ecological aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. In ‘Organic Phosphorus in the Environment’. (Eds B. L. Turner, B. L., E. Frossard and D. S. Baldwin.) pp. 205–241. (CAB International: Oxford, UK.)
Yelloly, J. M., and Whitton, B. A. (1996). Seasonal changes in ambient phosphate and phosphatase activities of the cyanobacterium Rivularia atra in intertidal pools at Tyne Sands, Scotland. Hydrobiologia 325, 201–212.
| Seasonal changes in ambient phosphate and phosphatase activities of the cyanobacterium Rivularia atra in intertidal pools at Tyne Sands, Scotland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xltl2jtLw%3D&md5=0b3337597967e45a08cc7b320f028b37CAS |
Yen, H.-K., Lin, T.-F., and Liao, P.-C. (2011). Simultaneous detection of nine cyanotoxins in drinking water using dual solid-phase extraction and liquid chromatography-mass spectrometry. Toxicon 58, 209–218.
| Simultaneous detection of nine cyanotoxins in drinking water using dual solid-phase extraction and liquid chromatography-mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovFehsL4%3D&md5=4736bf5e736c162946ca798351ee0df3CAS |
Young, F. M., Morrison, L. F., James, J., and Codd, G. A. (2008). Quantification and localization of microcystins in colonies of a laboratory strain of Microcystis (cyanobacteria) using immunological methods. European Journal of Phycology 43, 217–225.
| Quantification and localization of microcystins in colonies of a laboratory strain of Microcystis (cyanobacteria) using immunological methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFahtr0%3D&md5=b7f877555af4033327ac7fa741b8b5f2CAS |