Abstract
Metals and metalloids are toxic, persistent, and non-biodegradable and can be biomagnified (e.g., Hg), and therefore pose a serious threat to the algal flora of aquatic ecosystems. This laboratory study tested the effects of metals (Zn, Fe, and Hg) and a metalloid (As) on the cell wall morphology and protoplasmic content of living cells of six widespread diatom genera over 28 days. Diatoms exposed to Zn and Fe had a higher frequency of deformed diatom frustules (> 1%) compared to the As, Hg, and control treatments (< 1%). Deformities in the valve outline and striae were found in all treatments, including the control, whereas deformed raphes and more than one type of deformity were more prevalent under Zn and Hg stress. The order of toxicity is as follows: Zn > Fe > Hg≈As. Deformities were more frequent in Achnanthes and Diploneis (adnate forms) than in the motile genera of Nitzschia and Navicula. The correlation between the % healthy diatoms and % deformities in all six genera showed a negative relationship with the integrity of protoplasmic content (i.e., greater alteration in protoplasmic content was associated with greater frustule deformation). We conclude that diatom deformities can be a good indicator of metal and metalloid stress in waterbodies and are very useful in the rapid biomonitoring of aquatic ecosystems.
Graphical Abstract
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Barral-Fraga L, Morin S, Rovira MD, Urrea G, Magellan K, Guasch H (2016) Short-term arsenic exposure reduces diatom cell size in biofilm communities. Environ Sci Pollut Res 23(5):4257–4270. https://doi.org/10.1007/s11356-015-4894-8
Barral-Fraga L, Martina-Prieto D, Barral MT, Morin S, Guasch H (2018) Mutual interaction between arsenic and biofilm in a mining impacted river. Sci Total Environ 636:985–998. https://doi.org/10.1016/j.scitotenv.2018.04.287
Biggs BJF, Kilroy C (2000) Stream periphyton monitoring manual. NIWA, Christchurch, NZ, pp 1–246
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6(9):e04691. https://doi.org/10.1016/j.heliyon.2020.e04691
Cantonati M, Angeli N, Virtanen L, Wojtal AZ, Gabriell J, Falasco E, Lavoie I, Morin S, Marchetoo A, Fortin C, Smirnova S (2014) Achnanthidium minutissimum (Bacillariophyta) valve deformities as indicators of metal enrichment in diverse widely-distributed freshwater habitats. Sci Total Environ 75:201–215. https://doi.org/10.1016/j.scitotenv.2013.10.018
Cantonati M, Scola S, Angeli N, Guella G, Frassanito R (2009) Environmental controls of epilithic diatom depth-distribution in an oligotrophic lake characterized by marked water-level fluctuations. Eur J Phycol 44(1):15–29. https://doi.org/10.1080/09670260802079335
Cattaneo A, Asioli A, Comoli P, Manca M (1998) Organisms’ response in a chronically polluted lake supports hypothesized link between stress and size. Limnol Oceanogr 43(8):1938–1943. https://doi.org/10.4319/lo.1998.43.8.1938
Cattaneo A, Couillard Y, Wunsam S, Courcelles M (2004) Diatom taxonomic and morphological changes as indicators of metal pollution and recovery in Lac Dufault (Quebec, Canada). J Paleolimnol 32:163–175. https://doi.org/10.1023/B:JOPL.0000029430.78278.a5
Chen B, Stein AF, Castell N, Gonzalez-Castanedo Y, De La Campa AS, De La Rosa JD (2016) Modelling and evaluation of urban pollution events of atmospheric heavy metals from a large Cu-smelter. Sci Total Environ 539:17–25. https://doi.org/10.1016/j.scitotenv.2015.08.117
Cohn SA, Pickett-Heaps JD (1988) The effects of colchicine and dinitrophenol on the in vivo rates of anaphase A and B in the diatom Surirella. Eur J Cell Biol 46:523–530
Cohn SA, Farrell JF, Munro JD, Ragland RL, Weitzell RE Jr, Wibisono BL (2003) The effect of temperature and mixed species composition on diatom motility and adhesion. Diatom Res 18:225–243. https://doi.org/10.1080/0269249X.2003.9705589
Corcoll N, Ricart M, Franz S, Sans-Piché F, Schmitt-Jansen M, Guasch H (2012) The use of photosynthetic fluorescence parameters from autotrophic biofilms for monitoring the effect of chemicals in river ecosystems. Emerging and Priority Pollutants in Rivers 19:85–115. https://doi.org/10.1007/978-3-642-25722-3_4
Cox EJ (1996) Identification of freshwater diatoms from live material. Chapman and Hall, London 32(2):203–205
Debenest T, Silvestre J, Coste M, Delmas F, Pinelli E (2008) Herbicide effects on freshwater benthic diatoms: induction of nucleus alterations and silica cell wall abnormalities. Aquat Toxicol 88(1):88–94. https://doi.org/10.1016/j.aquatox.2008.03.011
Dickman MD (1998) Benthic marine diatom deformities associated with contaminated sediments in Hong Kong. Environ Int 24(7):749–759. https://doi.org/10.1016/S0160-4120(98)00060-9
Falasco E, Bona F, Badino G, Hoffmann L, Ector L (2009) Diatom teratological forms and environmental alterations: a review. Hydrobiologia 623(1):1–35. https://doi.org/10.1007/s10750-008-9687-3
Falasco E, Ector L, Wetzel CE, Badino G, Bona F (2021) Looking back, looking forward: a review of the new literature on diatom teratological forms (2010–2020). Hydrobiologia 848(8):1675–1753. https://doi.org/10.1007/s10750-021-04540-x
Farahat E, Linderholm HW (2015) The effect of long-term wastewater irrigation on accumulation and transfer of heavy metals in Cupressus sempervirens leaves and adjacent soils. Sci Total Environ 512:1–7. https://doi.org/10.1016/j.scitotenv.2015.01.032
Gelis MN, Mujica MA, Pecile A, Donadelli J, Simonetti M, Gómez N, Cochero J (2020) Diatom motility and nuclear alterations are affected by sediment elutriates of agricultural streams. Ecotoxicol Environ Saf 205:111322. https://doi.org/10.1016/j.ecoenv.2020.111322
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60. https://doi.org/10.2478/intox-2014-0009
Jumbe AS, Nandini N (2009) Heavy metals analysis and sediment quality values in urban lakes. Am J Environ Sci 5(6):678. https://doi.org/10.3844/ajessp.2009.678.687
Liang Y, Osada K, Sunaga Y, Yoshino T, Bowler C, Tanaka T (2015) Dynamic oil body generation in the marine oleaginous diatom Fistulifera solaris in response to nutrient limitation as revealed by morphological and lipidomic analysis. Algal Res 12:359–367. https://doi.org/10.1016/j.algal.2015.09.017
Licursi M, Gómez N (2013) Short-term toxicity of hexavalent-chromium to epipsammic diatoms of a microtidal estuary (Río de la Plata): Responses from the individual cell to the community structure. Aquat Toxicol 134:82–91. https://doi.org/10.1016/j.aquatox.2013.03.007
Loska K, Wiechula D (2003) Application of principal component analysis for the estimation of source of heavy metal contamination in surface sediments from Rybnik Reservoir. Chemosphere 51:723–733
Magnusson M, Heimann K, Negri AP (2008) Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar Pollut Bull 56(9):1545–1552
Martin JH (1990) Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5(1):1–13
McCormick PV, Cairns J Jr (1994) Algae as indicators of environmental change. J Appl Phycol 6:509–526
Moir KE, Ridal JJ, Cumming BF (2022) Spatiotemporal and teratological analyses of diatom assemblages from sediments contaminated with industrial effluents in the St. Lawrence River near Cornwall (Ontario, Canada). Hydrobiologia 849:1417–1436
Morin S, Cordonier A, Lavoie I, Arini A, Blanco S, Duong TT, Tornés E, Bonet B, Corcoll N, Faggiano L, Laviale M, Pérès F, Becares E, Coste M, Feurtet-Mazel A, Fortin C, Guasch H, Sabater S (2012) Consistency in diatom response to metal-contaminated environments. In: Guasch H, Ginebreda A, Geiszinger A (eds) Emerging and Priority Pollutants in Rivers. Springer-Verlag, Berlin, pp 117–146
Morin S, Gómez N, Tornés E, Licursi M, Rosebery J (2016) Benthic diatom monitoring and assessment of freshwater environments: standard methods and future challenges. In: Romaní AM, Guasch H, Balaguer MD (eds) Aquatic biofilms: ecology, water quality and water treatment. Caister Academic Press, UK, pp 111–124. https://doi.org/10.21775/9781910190173.06
Mu W, Jia K, Liu Y, Pan X, Fan Y (2017) Response of the freshwater diatom Halamphora veneta (Kützing) Levkov to copper and mercury and its potential for bioassessment of heavy metal toxicity in aquatic habitats. Environ Sci Pollut Res 24(34):26375–26386
Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZ, Zia-Ul-Haq M (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48(1):1–7
Pandey LK, Kumar D, Yadav A, Rai J, Gaur JP (2014) Morphological abnormalities in periphytic diatoms as a tool for biomonitoring of heavy metal pollution in a river. Ecol Indic 36:272–279
Pandey LK, Han T, Gaur JP (2015) Response of a phytoplanktonic assemblage to copper and zinc enrichment in microcosm. Ecotoxicology 24:573–582
Pandey LK, Bergey EA (2016) Exploring the status of motility, lipid bodies, deformities and size reduction in periphytic diatom community from chronically metal (Cu, Zn) polluted waterbodies as a biomonitoring tool. Sci Total Environ 550:372–381
Pandey LK, Bergey EA, Lyu J, Park J, Choi S, Lee H, Depuydt S, Oh Y-T, Lee S-M, Han T (2017) The use of diatoms in ecotoxicology and bioassessment: insights, advances and challenges. Water Res 118:39–58
Pandey LK, Lavoie I, Morin S, Park J, Lyu J, Choi S, Lee H, Han T (2018a) River water quality assessment based on a multi-descriptor approach including chemistry, diatom assemblage structure, and non-taxonomical diatom metrics. Ecol Indic 84:140–151
Pandey LK, Sharma YC, Park J, Choi S, Lee H, Jie L, Han H (2018b) Evaluating features of periphytic diatom communities as biomonitoring tools in fresh, brackish and marine waters. Aquat Toxicol 194:67–77
Park J, Lee H, Depuydt S, Han T, Pandey LK (2020) Assessment of five live-cell characteristics in periphytic diatoms as a measure of copper stress. J Hazard Mater 400:123113
Pinto E, Sigaud-kutner TC, Leitao MA, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal–induced oxidative stress in algae 1. J Phycol 39(6):1008–1018
Price NM, Morel FMM (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344(6267):658–660
Rai LC, Mallick N (1993) Heavy metal toxicity to algae under synthetic microcosm. Ecotoxicology 2:231–242
Renzi M, Roselli L, Giovani A, Focardi SE, Basset A (2014) Early warning tools for ecotoxicity assessment based on Phaeodactylum tricornutum. Ecotoxicology 23(6):1055–1072
Smith MA (1983) The effect of heavy metals on the cytoplasmic fine structure of Skeletonema costatum (Bacillariophyta). Protoplasma 116(1):14–23
Smith T, Manoylov K (2007) Diatom deformities from an acid mine drainage site at Friendship Hills National Historical Site. Pennsylvania J Freshw Ecol 22(3):521–527
Stevenson RJ, Pan Y, Vandam H (2010) Assessing environmental conditions in rivers and streams with diatoms. In: Smol JP, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences, second eds. Cambridge University Press, London, pp 57–85. https://doi.org/10.1017/CBO9780511763175.005
Taylor JC, Harding WR, Archibald CGM (2007) A methods manual for the collection, preparation and analysis of diatom samples. Version 1:60
Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544
Ullrich-Eberius CI, Sanz A, Novacky AJ (1989) Evaluation of arsenate-and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba G1. J Exp Bot 40:119–128
Wood RJ, Mitrovic SM, Kefford BJ (2014) Determining the relative sensitivity of benthic diatoms to atrazine using rapid toxicity testing: a novel method. Sci Total Environ 485:421–427. https://doi.org/10.1016/j.scitotenv.2014.03.115
Wood RJ, Mitrovic SM, Lim RP, Kefford BJ (2016) How benthic diatoms within natural communities respond to eight common herbicides with different modes of action. Sci Total Environ 557:636–643
Wu Y, Wang WX (2011) Accumulation, subcellular distribution and toxicity of inorganic mercury and methylmercury in marine phytoplankton. Environ Pollut 159(10):3097–3105
Acknowledgements
Sangeeta thanks SERB, New Delhi, for the financial assistance in the form of JRF. SN, MG, DG, SS, and AK thanks SERB, New Delhi, for helping to carry out their dissertation work through SSR (Scientific Social Responsibility) policy. We are thankful to Dr. Kalyan Mitra and Mr. J.P. Pandey of the Electron microscopy unit, Sophisticated Analytical Instrumentation Facility (SAIF), CSIR-CDRI, for the assistance with electron imaging of diatom samples. We are also grateful to Dr. J.C. Taylor (North-West University, South Africa) for the generous gift of Pleurax.
Funding
This work was supported by SERB, New Delhi in the form of a SERB-SRG (File No. SRG/2020/000432) project.
Author information
Authors and Affiliations
Contributions
Sudeeksha Negi: formal analysis; investigation; data curation; writing—original draft; writing—review and editing visualization.
Taejun Han: writing—review and editing.
Jihae Park: writing—review and editing.
Elizabeth A. Bergey: formal analysis; investigation; data curation; writing—original draft; writing—review and editing; visualization.
Jyoti Chaubey: investigation; data curation; writing—original draft; visualization.
Sangeeta: investigation, data curation, visualization.
Mahima Gupta: investigation, data curation, visualization.
Abhishek Kumar: investigation, data curation, visualization.
Divyanshi Gupta: investigation, data curation, visualization.
Shivangi Singh: investigation, data curation, visualization.
Lalit Kumar Pandey: conceptualization; methodology; validation; formal analysis; investigation; data curation; writing—original draft; writing—review and editing; visualization.
Corresponding author
Ethics declarations
Animal research (ethics)
No animal used in this research work.
Consent to participate (ethics)
Ready to participate.
Consent to publish (ethics)
Ready to publish in subscription.
Plant reproducibility
No plant used. We do research on algae.
Clinical trial registration
No clinical registration requires as work is on algae.
Conflict of interest
The authors declare no competing interests.
Additional information
Handling Editor: Andreas Holzinger
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Negi, S., Han, T., Park, J. et al. Qualitative and quantitative assessment of diatom deformities and protoplasmic condition under metal and metalloid stress. Protoplasma 260, 1501–1513 (2023). https://doi.org/10.1007/s00709-023-01864-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-023-01864-4