Influence of calcium on cadmium uptake and toxicity to the cyanobacterium Nostoc muscorum Meg 1
Rabbul Ibne A. Ahad, Mayashree B. Syiem
Abstract
It is well known that Ca2+ interferes with uptake and expression of toxicity of Cd2+ in numerous organisms. This study demonstrated that the morphological alterations expressed in the cyanobacterium Nostoc muscorum Meg 1 cells exposed to 0.5 mg L−1 Cd2+ for 7 days were prevented when 10 mg L−1 Ca2+ was included in the experimental set-up. The spectroscopic analysis confirmed a severe reduction in contents of chlorophyll a, phycocyanin, allophycocyanin, phycoerythrin, carotenoids and total protein at the end of 168 h (7 days) in presence of Cd2+; inclusion of Ca2+ significantly lessened these effects. Heterocyst frequency, nitrogenase and, glutamine synthetase activities were similarly improved in the presence of Ca2+. Uptake studies showed a reduction in 94% biosorption of supplied Cd2+ to 50% in the presence of Ca2+ indicating its competition with Cd2+ binding onto the cyanobacterial cell surfaces.
Keywords
References
Abed et al., 2009
R.M.M. Abed, S. Dobretsov, K. Sudesh
Applications of Cyanobacteria in biotechnology
Journal of Applied Microbiology, 106 (1) (2009), pp. 1-12, 10.1111/j.1365-2672.2008.03918.x
Ahad et al., 2018
R.I.A. Ahad, B.L. Kynshi, M.B. Syiem
Protective role of Ca2+ towards Cu2+ induced toxicity on photosynthetic pigments, morphology and ultra-structures of the cyanobacterium Nostoc muscorum Meg 1
Biosciences Biotechnology Research Asia, 15 (3) (2018), pp. 591-601, 10.13005/bbra/2665
Ahad et al., 2017
R.I.A. Ahad, S. Goswami, M.B. Syiem
Biosorption and equilibrium isotherms study of cadmium removal by Nostoc muscorum Meg 1: Morphological, physiological and biochemical alterations
3 Biotech, 7 (2) (2017), p. 104, 10.1007/s13205-017-0730-9
Antosiewicz and Hennig, 2004
D.M. Antosiewicz, J. Hennig
Overexpression of LCT1 in tobacco enhances the protective action of calcium against cadmium toxicity
Environmental Pollution, 129 (2) (2004), pp. 237-245, 10.1016/j.envpol.2003.10.025
Awofolu et al., 2005
O.R. Awofolu, Z. Mbolekwa, V. Mtshemla, O.S. Fatoki
Levels of trace metals in water and sediment from Tyume river and its effects on an irrigated farmland
Water SA, 31 (1) (2005), pp. 87-94, 10.4314/wsa.v31i1.5124
Bennett and Bogorad, 1973
A. Bennett, L. Bogorad
Complementary chromatic adaption in a filamentous blue-green alga
The Journal of Cell Biology, 58 (1973), pp. 419-435, 10.1083/jcb.58.2.419
Cassier-Chauvat, 2015
C. Cassier-Chauvat, F. Chauvat
Responses to oxidative and heavy metal stresses in cyanobacteria: Recent advances
International Journal of Molecular Sciences, 16 (1) (2015), pp. 871-886, 10.3390/ijms16010871
Chandrangsu et al., 2017
P. Chandrangsu, C. Rensing, J.D. Helmann
Metal homeostasis and resistance in bacteria
Nature Reviews Microbiology, 15 (2017), pp. 338-350, 10.1038/nrmicro.2017.15
Checchetto et al., 2013
V. Checchetto, E. Formentin, L. Carraretto, A. Segalla, G.M. Giacometti, I. Szabo, E. Bergantino
Functional characterization and determination of the physiological role of a calcium-dependent potassium channel from cyanobacteria
Plant Physiology, 162 (2013), pp. 953-964, 10.1104/pp.113.215129
Chen et al., 2012
Q.L. Chen, Z. Luo, J.L. Zheng, X.D. Li, C.X. Liu, Y.H. Zhao, et al.
Protective effects of calcium on copper toxicity in Pelteobagrus fulvidraco: Copper accumulation, enzymatic activities, histology
Ecotoxicology and Environmental Safety, 7 (2012), pp. 126-134
Choong et al., 2014
G. Choong, Y. Liu, D.M. Templeton
Interplay of calcium and cadmium in mediating cadmium toxicity
Chemico-Biological Interactions, 211 (2014), pp. 54-65, 10.1016/j.cbi.2014.01.007
Clemens et al., 1998
S. Clemens, D.M. Antosiewicz, J.M. Ward, D.P. Schachtman, J.I. Schroeder
The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast
Proceedings of the National Academy of Sciences, 95 (20) (1998), pp. 12043-12048, 10.1073/pnas.95.20.12043
Clemens, 2006
S. Clemens
Toxic metal accumulation responses to exposure and mechanisms of tolerance in plants
Biochemie, 88 (11) (2006), pp. 1707-1719, 10.1016/j.biochi.2006.07.003
Dubey et al., 2011
S.K. Dubey, J. Dubey, S. Mehra, P. Tiwari, A.J. Bishwas
Potential use of cyanobacterial species in bioremediation of industrial effluents
African Journal of Biotechnology, 10 (7) (2011), pp. 1125-1132, 10.5897/AJB10.908
Fernandez-Piñas et al., 1995
F. Fernandez-Piñas, P. Mateo, I. Bonilla
Cadmium toxicity in NostocUAM208: Protection by calcium
New Phytologist, 131 (3) (1995), pp. 403-407, 10.1111/j.1469-8137.1995.tb03077.x
Gaballa and Helmann, 2003
A. Gaballa, J.D. Helmann
Bacillus subtilis CPx-Type ATPases: Characterization of Cd, Zn, Co and Cu efflux systems
BioMetals, 16 (4) (2003), pp. 497-505, 10.1023/A:1023425321617
Gibbons et al., 2011
S.M. Gibbons, K. Feris, M.A. McGuirl, S.E. Morales, A. Hynninen, P.W. Ramsey, et al.
Use of microcalorimetry to determine the costs and benefits to Pseudomonas putida strain KT2440 of harboring cadmium efflux genes
Applied and Environmental Microbiology, 77 (1) (2011), pp. 108-113, 10.1128/AEM.01187-10
Gipps and Coller, 1982
J.F. Gipps, B.A.W. Coller
Effect of some nutrient cations on uptake of cadmium by Chlorella pyrenoidosa
Marine and Freshwater Research, 33 (6) (1982), pp. 979-987, 10.1071/MF9820979
Goswami et al., 2015a
S. Goswami, M.B. Syiem, K. Pakshirajan
Cadmium removal by Anabaena doliolum Ind1 isolated from a coal mining area in Meghalaya India: Associated structural and physiological alterations
Environmental Engineering Research, 20 (1) (2015), pp. 41-50, 10.4491/eer.2014.059
Goswami et al., 2015b
S. Goswami, O.L. Diengdoh, M.B. Syiem, K. Pakshirajan, M.G. Kiran
Zn(II) and Cu(II) removal by Nostoc muscorum: A cyanobacterium isolated from a coal mining pit in Chiehruphi, Meghalaya, India
Canadian Journal of Microbiology, 61 (3) (2015), pp. 209-215, 10.1139/cjm-2014-0599
Gupta and Rastogi, 2008
V.K. Gupta, A. Rastogi
Biosorption of lead(II) from aqueous solutions by non-living algal biomass Oedogonium sp. and Nostocsp. – A comparative study
Colloids and Surfaces B: Biointerfaces, 64 (2) (2008), pp. 170-178, 10.1016/j.colsurfb.2008.01.019
Hayakaway et al., 2011
N. Hayakaway, R. Tomiokay, C. Takenaka
Effects of calcium on cadmium uptake and transport in the tree species Gamblea innovans
Soil Science and Plant Nutrition, 57 (5) (2011), pp. 691-695, 10.1080/00380768.2011.608196
Hudek and Ackland, 2017
L. Hudek, M.L. Ackland
Selective metal ion homeostasis in cyanobacteria
Prospects and Challenges in Algal Biotechnology (2017), pp. 219-232
Huertas et al., 2014
M.J. Huertas, L. López-Maury, J. Giner-Lamia, A.M. Sánchez-Riego, F.J. Florencio
Metals in cyanobacteria: Analysis of the copper, nickel, cobalt and arsenic homeostasis mechanisms
Life (Basel), 4 (2014), pp. 865-886, 10.3390/life4040865
Inouye et al., 1983
S. Inouye, T. Franceschini, M. Inouye
Structural similarities between the development-specific protein S from a gram-negative bacterium Myxococcus xanthus, and Calmodulin
Proceedings of the National Academy of Sciences of the United States of America, 80 (22) (1983), pp. 6829-6833
Jacobson and Turner, 1980
K.B. Jacobson, J.E. Turner
The interaction of cadmium and certain other metal ions with proteins and nucleic acids
Toxicology, 16 (1) (1980), pp. 1-37, 10.1016/0300-483X(80)90107-9
Kanamura et al., 1993
K. Kanamura, S. Kashiwagi, T. Mizuno
The cyanobacterium Synechococcus sp. PCC7942, possess two distinct genes encoding cation transporting P-type ATPases
FEBS Letter, 330 (1993), pp. 99-104
Kaneko et al., 1996
T. Kaneko, S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, et al.
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions
DNA Research, 3 (1996), pp. 109-136
Kim et al., 2002
Y. Kim, Y. Yang, Y. Lee
Pb and Cd uptake in rice roots
Physiologia Plantarum, 116 (3) (2002), pp. 368-372, 10.1034/j.1399-3054.2002.1160312.x
Lavoie et al., 2014
M. Lavoie, P.G.C. Campbell, C. Fortin
Predicting cadmium accumulation and toxicity in a green alga in the presence of varying essential element concentrations using a biotic ligand model
Environmental Science and Technology, 48 (2) (2014), pp. 1222-1229, 10.1021/es402630z
Liorti et al., 2017
A. Liorti, T. Crease, A. Heyland
Interactive effects of copper and calcium in Daphnia pulex
Journal of Limnology, 76 (2017), pp. 281-291, 10.4081/jlimnol.2016.1498
Lowry et al., 1951
O.H. Lowry, N.J. Roserbough, A.L. Farr, R.J. Randall
The Folin by Oliver
Journal of Biological Chemistry, 193 (1951), pp. 265-275, 10.1016/0304-3894(92)87011-4
Lu et al., 2010
L. Lu, S. Tian, M. Zhang, J. Zhang, X. Yang, H. Jiang
The role of Ca pathway in Cd uptake and translocation by the hyperaccumulator Sedum alfredii
Journal of Hazardous Materials, 183 (1–3) (2010), pp. 22-28, 10.1016/j.jhazmat.2010.06.036
Mackinney, 1941
G. Mackinney
Absorption of light by chlorophyll solutions
Journal of Biological Chemistry, 140 (1941), pp. 315-322
Marchetti, 2012
C. Marchetti
Role of calcium channels in heavy metal toxicity
ISRN Toxicology (2012), 10.1155/2013/184360
Mateo et al., 1994
P. Mateo, F. Fernandez-Pinas, I. Bonilla
O2-induced inactivation of nitrogenase as a mechanism for the toxic action of Cd2+ on NostocUAM208
New Phytologist, 126 (2) (1994), pp. 267-272, 10.1111/j.1469-8137.1994.tb03945.x
Meeks, 2007
J.C. Meeks
Physiological adaptations in nitrogen-fixing Nostoc–plant symbiotic associations
K. Pawlowski (Ed.), Prokaryotic symbionts in plants. Microbiology monographs, Vol. 8, Springer, Berlin, Heidelberg (2007)
Mishra et al., 2012
S.K. Mishra, A. Shrivastav, R.R. Maurya, S.K. Patidar, S. Haldar, S. Mishra
Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp. isolated from Gujarat coast India
Protein Expression Purification, 81 (1) (2012), pp. 5-10
Morgan, 1967
R.C. Morgan
The carotenoids of Queensland fruits – Carotenes of the watermelon (Citrullus vulqaris)
Journal of Food Science, 32 (3) (1967), pp. 275-278, 10.1111/j.1365-2621.1967.tb01311.x
Nies, 1999
D.H. Nies
Microbial heavy-metal resistance
Applied Microbiology and Biotechnology, 51 (6) (1999), pp. 730-750
http://www.ncbi.nlm.nih.gov/pubmed/10422221
Nongbri and Syiem, 2012
B.B. Nongbri, M.B. Syiem
Diversity analysis and molecular typing of cyanobacteria isolated from various ecological niches in the state of Meghalaya North-East India
Environmental Engineering Research, 17 (S1) (2012), pp. 21-26, 10.4491/eer.2012.17.S1.S21
Nongrum and Syiem, 2012
N.A. Nongrum, M.B. Syiem
Effects of copper ion (Cu2+) on the physiological and biochemical activities of the cyanobacterium NostocANTH
Environmental Engineering Research, 17 (S1) (2012), pp. S63-S67
Outten and O’Halloran, 2001
C.E. Outten, T.V. O’Halloran
Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis
Science, 292 (5526) (2001), pp. 2488-2492, 10.1126/science.1060331
Pandey et al., 1996
P.K. Pandey, B.B. Singh, R. Mishra, P.S. Bisen
Ca2+ uptake and its regulation in the cyanobacterium NostocMAC
Current Microbiology, 32 (1996), pp. 332-335, 10.1007/s002849900059
Pitta et al., 1997
T.P. Pitta, E.E. Sherwood, A.M. Kobel, H.C. Berg
Calcium is required for swimming by the non-flagellated cyanobacterium Synechococcus strain WH8113
Journal of Bacteriology, 179 (8) (1997), pp. 2524-2528
Rippka et al., 1979
R. Rippka, J. Dereulles, J.B. Waterbury, M. Herdman, R.Y. Stanier
Generic assignments, strain histories and properties of pure cultures of cyanobacteria
Journal of General Microbiology, 111 (1979), pp. 1-61, 10.1099/00221287-111-1-1
Robinson et al., 1982
S.J. Robinson, C.S. Deroo, C.F. Yocum
Photosynthetic electron transfer in preparations of the cyanobacterium Spirulina platensis
Plant Physiology, 70 (1) (1982), pp. 154-161, 10.1104/pp.70.1.154
Sampaio et al., 1979
M.J.A.M. Sampaio, P. Rowell, W.D.P. Stewart
Purification and some properties of glutamine synthetase from the nitrogen-fixing cyanobacteria Anabaena cylindrica and a Nostoc sp.
Journal of General Microbiology, 111 (1) (1979), pp. 181-191, 10.1099/00221287-111-1-181
Shcolnick and Keren, 2006
S. Shcolnick, N. Keren
Metal homeostasis in cyanobacteria and chloroplasts balancing benefits and risks to the photosynthetic apparatus
Plant Physiology, 141 (2006), pp. 805-810, 10.1104/pp.106.079251
Singh et al., 2016
J.S. Singh, A. Kumar, A.N. Rai, D.P. Singh
Cyanobacteria: A precious bio-resource in agriculture
Ecosystem and Environmental Sustainability, 7 (2016), p. 529, 10.3389/fmicb.2016.00529
Stewart et al., 1967
W.D. Stewart, G.P. Fitzgerald, R.H. Burris
In situ studies on N2 fixation using the acetylene reduction technique
Proceedings of the National Academy of Sciences, 58 (5) (1967), pp. 2071-2078, 10.1073/pnas.58.5.2071
Sulaymon et al., 2013
A.H. Sulaymon, A.A. Mohammed, T.J. Al-musawi
Competitive biosorption of lead, cadmium, copper and arsenic ions using algae
Environment Science and Pollution Research, 20 (5) (2013), pp. 3011-3023, 10.1007/s11356-012-1208-2
Torrecilla et al., 2004
I. Torrecilla, F. Leganés, I. Bonilla, F. Fernández-Piñas
A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120
Microbiology, 150 (11) (2004), pp. 3731-3739, 10.1099/mic.0.27403-0
Warjri and Syiem, 2018
S.M. Warjri, M.B. Syiem
Analysis of biosorption parameters, equilibrium isotherms and thermodynamic studies of chromium (VI) uptake by a Nostocsp. isolated from a coal mining site in Meghalaya, India
Mine, Water and the Environment, 37 (2018), p. 713, 10.1007/s10230-018-0523-3
Watkins et al., 1995
N.J. Watkins, M.R. Knight, A.J. Trewavas, A.K. Campbell
Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin
The Biochemical Journal, 306 (3) (1995), pp. 865-869
Werthén and Lundgren, 2001
M. Werthén, T. Lundgren
Intracellular Ca2+ mobilization and kinase activity during acylated homoserine lactone-dependent quorum sensing in Serratia liquefaciens
Journal of Biological Chemistry, 276 (9) (2001), pp. 6468-6472, 10.1074/jbc.M009223200
Wolk, 1965
C.P. Wolk
Control of sporulation in a blue-green alga
Developmental Biology, 12 (1) (1965), pp. 15-35
http://www.ncbi.nlm.nih.gov/pubmed/5833109
Zeng et al., 2012
X. Zeng, J. Tang, X. Liu, P. Jiang
Response of P. aeruginosa E1 gene expression to cadmium stress
Current Microbiology, 65 (6) (2012), pp. 799-804, 10.1007/s00284-012-0224-2
Zorrig et al., 2012
W. Zorrig, Z. Shahzad, C. Abdelly, P. Berthomieu
Calcium enhances cadmium tolerance and decreases cadmium accumulation in lettuce (Lactuca sativa)
African Journal of Biotechnology, 11 (34) (2012), pp. 8441-8448, 10.4314/ajb.v11i34