Abstract
Dissolved humic substances (DHSs) are the major components of organic matter in the aquatic environment. DHSs are well known to considerably affect the speciation, solubility, and toxicity of a wide variety of pollutants in the aquatic environment. In this study, the effects of the toxicity of heavy metals and hydrophobic organic pollutants (HOPs) on Chlamydomonas reinhardtii in the presence of humic acid (HA) were examined by a microscale algal growth inhibition (μ-AGI) test based on spectrophotometric detection. To clarify the relationship between the chemical properties of HAs and the toxicity change of pollutants, eight HAs from different sources were prepared and used. HAs were responsible for mitigating the toxicity of Hg, Cu, pesticides (γ-HCH, 2,4-D, and DDT), and polycyclic aromatic hydrocarbons (PAHs) such as naphthalene (Nap), anthracene (Ant), and benzo[a]pyrene (BaP). In particular, an approximately 100-fold decrease in the toxicity of BaP was observed in the presence of 10 ppm HAs extracted from tropical peat. The results indicated that the carboxylic group content and the HA molecular weight are correlated to the changes in the heavy metal toxicity. For HOPs, the aromaticity and polarity of HAs are crucial for mitigating their toxicity. Furthermore, it was clearly shown that the lake water including a high concentration of DHSs collected from Central Kalimantan, Indonesia, reduced the toxicity of Hg and γ-HCH on Chlamydomonas reinhardtii.
Similar content being viewed by others
References
Brown JN, Peake BM (2003) Determination of colloidally-associated polycyclic aromatic hydrocarbons (PAHs) in fresh water using C18 solid phase extraction disks. Anal Chim Acta 486:159–169. https://doi.org/10.1016/S0003-2670(03)00472-0
Chin YP, Aiken GR, Danielsen KM (1997) Binding of pyrene to aquatic and commercial humic substances: the role of molecular weight and aromaticity. Environ Sci Technol 31:1630–1635. https://doi.org/10.1021/es960404k
Chiou CT, Kile DE, Brinton TI, Malcolm RL, Leenheer JA, MacCarthy P (1987) A comparison of water solubility enhancements of organic solutes by aquatic humic materials and commercial humic acids. Environ Sci Technol 21:1231–1234. https://doi.org/10.1021/es00165a012
Danielsen KM, Chin YP, Buterbaugh JS, Gautafson TL, Traina SJ (1995) Solubility enhancement and fluorescence quenching of Pyrene by humic Substances: the effect of dissolved oxygen on quenching processes. Environ Sci Technol 29:2162–2165. https://doi.org/10.1021/es00008a042
Fathi P, Sadegi G, Hosseini MJ, Farahmandkia Z, Mehrasebi MR (2020) Effects of copper oxide nanoparticles on the Chlorella algae in the presence of humic acid. SN Appl Sci 2:140. https://doi.org/10.1007/s42452-019-1812-6
Freidig AP, Garicano EA, Busser FJM, Hermens JLM (1998) Estimating impact of humic acid on bioavailability and bioaccumulation of hydrophobic chemicals in Guppies using kinetic solid-phase extraction. Environ Toxicol Chem 17:998–1004. https://doi.org/10.1002/etc.5620170604
Fu P, Wu F, Liu C, Wang F, Li W, Yue L, Guo Q (2007) Fluorescence characterization of dissolved organic matter in an urban river and its complexation with Hg(II). Appl Geochem 22:1668–1679. https://doi.org/10.1016/j.apgeochem.2007.03.041
Garvey JG, Owen HA, Winner RW (1991) Toxicity of copper to the green alga, Chlamidomonas reinhardtii (Chlorophyceae), as affected by humic substances of terrestrial and fresh water origin. Aquat Toxicol 19:89–96. https://doi.org/10.1016/0166-445X(91)90029-9
Gauthier TD, Shane EC, Guerin WF, Seitz WR, Grant CL (1986) Fluorescence quenching method for determining equilibrium constants for polycyclic aromatic hydrocarbons binding to dissolved humic materials. Environ Sci Technol 20:1162–1166. https://doi.org/10.1021/es00153a012
Geis SW, Fleming KL, Korthals ET, Searle G, Reynolds L, Karner DA (2000) Modifications to the algal growth inhibition test for use as a regulatory assay. Environ Toxicol Chem 19:36–41. https://doi.org/10.1002/etc.5620190105
Ikeya K, Watanabe A (2003) Direct expression of an index for the degree of humification of humic acids using organic carbon concentration. Soil Sci Plant Nutr 49:47–53. https://doi.org/10.1080/00380768.2003.10409978
Jones KD, Huang WH (2003) Evaluation of toxicity of the pesticides, chlorpyrifos and arsenic, in the presence of compost humic substances in aqueous system. J Hazard Mater B103:93–105. https://doi.org/10.1016/s0304-3894(03)00227-9
Kosakowska A, Nedzi M, Pempkowiak J (2007) Responces of the toxic cyanobacterium Microcystis aeruginosa to iron and humic substances. Plant Physiol Biochem 45:365–370. https://doi.org/10.1016/j.plaphy.2007.03.024
Koukal B, Gueguen C, Pardos M, Dominik J (2003) Influence of humic substances on the toxic effects of cadmium and zinc to the green alga Pseudokirchneriella subcapitata. Chemosphere 53:953–961. https://doi.org/10.1016/S0045-6535(03)00720-3
Kováčik J, Bujdoš M, Babula P (2018) Impact of humic acid on the accumulation of metals by microalgae. Environ Sci Pollut Res 25:10792–10798. https://doi.org/10.1007/s11356-018-1362-2
Kumada K, Sato O, Ohsumi Y, Ohta S (1967) Humus composition of mountain soils in Central Japan with special reference to the distribution of P type humic acid. Soil Sci Plant Nutr 13:151–158. https://doi.org/10.1080/00380768.1967.10431990
Kuramitz H, Sazawa K, Nanayama Y, Hata N, Taguchi S, Sugawara K, Fukushima M (2012) Electrochemical genotoxicity assay based on a SOS/umu test using hydrodynamic voltammetry in a droplet. Sensors 12:17414–17432. https://doi.org/10.3390/s121217414
Lamelas C, Wilkinson KJ, Slaveykova VI (2005) Influence of the composition of natural organic matter on Pb bioavailability to microalgae. Environ Sci Technol 39:6109–6116. https://doi.org/10.1021/es050445t
Li N, Lee HK (2000) Tandem-cartridge solid-phase extraction followed by GC/MS analysis for measuring partition coefficients of association of polycyclic aromatic hydrocarbons to humic acid. Anal Chem 72:5272–5279. https://doi.org/10.1021/ac000663z
Liu Y, Zhi L, Zhou S, Xie F (2020) Effects of mercury binding by humic acid and humic acid resistance on mercury stress in rice plants under high Hg/humic acid concentration ratios. Environ Sci Pollut Res: Published online 27:18650–18660. https://doi.org/10.1007/s11356-020-08328-9
Lu X, Jaffe R (2001) Interaction between Hg(II) and natural dissolved organic matter: a fluorescence spectroscopy based study. Water Res 35:1793–1803. https://doi.org/10.1016/S0043-1354(00)00423-1
Ma H, Kim SD, Cha DK, Allen HE (1999) Effect of kinetics of complexation by humic acid on toxicity of copper to Ceriodaphnia dubia. Environ Toxicol Chem 18:828–837. https://doi.org/10.1002/etc.5620180504
McDonald S, Bishop AG, Prenzler PD, Robards K (2004) Analytical chemistry of freshwater humic substances. Anal Chim Acta 527:105–124. https://doi.org/10.1016/j.aca.2004.10.011
McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2002) The role of dissolved organic carbon in moderating the bioavailability and toxicity of Cu to rainbow trout during chronic waterborne exposure. Comp Biochem Physiol C 133:147–160. https://doi.org/10.1016/S1532-0456(02)00084-4
Mezin LC, Hale RC (2004) Effect of humic acids on toxicity of DDT and chlorpyrifos to freshwater and estuarine invertebrates. Environ Toxicol Chem 23:583–590. https://doi.org/10.1897/02-431
Paolis F, Kukkonen J (1997) Binding of organic pollutants to humic and fulvic acids: influence of pH and the structure of humic material. Chemosphere 34:1693–1704. https://doi.org/10.1016/S0045-6535(97)00026-X
Paulauskis JD, Winner RW (1988) Effects of water hardness and humic acid on zinc toxicity to Daphnia magna Straus. Aquat Toxicol 12:273–290. https://doi.org/10.1016/0166-445X(88)90027-6
Perminova IV, Grechishcheva NY, Petrosyan VS (1999) Relationships between structure and binding affinity of humic substances for polycyclic aromatic hydrocarbons: relevance of molecular descriptors. Environ Sci Technol 33:3781–3787. https://doi.org/10.1021/es990056x
Peuravuori J, Pihlaja K (1997) Molecular size distribution and spectroscopic properties of aquatic humic substances. Anal Chim Acta 337:133–149. https://doi.org/10.1016/S0003-2670(96)00412-6
Plaza C, Brunetti G, Senesi N, Polo A (2006) Molecular and quantitative analysis of metal ion binding to humic acids from sewage sludge and sludge-amended soils by fluorescence spectroscopy. Environ Sci Technol 40:917–923. https://doi.org/10.1021/es051687w
R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/
Ravichandran M (2004) Interactions between mercury and dissolved organic matter-a review. Chemosphere 55:319–331. https://doi.org/10.1016/j.chemosphere.2003.11.011
Rutheford DW, Chiou CT, Kile DE (1992) Influence of soil organic matter composition on the partition of organic compounds. Environ Sci Technol 26:336–340. https://doi.org/10.1021/es00026a014
Sager R, Granick S (1953) Nutritional Studies with Chlamydomonas reinhardtii. Ann N Y Acad Sci 56:831–838. https://doi.org/10.1111/j.1749-6632.1953.tb30261.x
Salloum MJ, Chefetz B, Hatcher PG (2002) Phenanthrene sorption by aliphatic-rich natural organic matter. Environ Sci Technol 36(9):1953–1958. https://doi.org/10.1021/es015796w
Sazawa K, Tachi M, Wakimoto T, Kawakami T, Hata N, Taguchi S, Kuramitz H (2011) The evaluation for alterations of DOM components from upstream to downstream flow of rivers in Toyama (Japan) using three-dimensional excitation-emission matrix fluorescence spectroscopy. Int J Environ Res Public Health 8:1655–1670. https://doi.org/10.3390/ijerph8051655
Sazawa K, Furuhashi Y, Hata N, Taguchi S, Fukushima M, Kuramitz H (2013) Evaluation of the toxicity of tetrabromobisphenol A and some of its oxidation products using a micro-scale algal growth inhibition test. Toxicol Environ Chem 95:472–482. https://doi.org/10.1080/02772248.2013.775290
Schnitzer M, Khan SU (1972) Humic substances in the environment. Marcel Dekker. Inc, New York
Slaveykova VI, Wilkinson KJ, Ceresa A, Pretsch E (2003) Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii. Environ Sci Technol 37:1114–1121. https://doi.org/10.1021/es025993a
Swift RS (1996) Organic matter characterization. In: Sparks DL (ed) Methods of Soil Analysis, Part 3. Chemical Methods-SSSA Book Series No. 5. Soil Science Society of America Inc, Madison, pp 1011–1069
Tanaka S, Oba K, Fukushima M, Nakayasu K, Hasebe K (1997) Water solubility enhancement of pyrene in the presence of humic substances. Anal Chim Acta 337:351–357. https://doi.org/10.1016/S0003-2670(96)00422-9
Tanaka F, Fukushima M, Kikuchi A, Yabuta H, Ichikawa H, Tatsumi K (2005) Influence of chemical characteristics of a chlorinated dioxin. Chemosphere 58:1319–1326. https://doi.org/10.1016/j.chemosphere.2004.10.008
Thomas JD (1997) The role of dissolved organic matter, particularly free amino acids and humic substances, in freshwater ecosystems. Freshw Biol 38:1–36. https://doi.org/10.1046/j.1365-2427.1997.00206.x
Tsiridis V, Petala M, Samaras P, Hadjispyrou S, Sakellaropoulos G, Kungolos A (2006) Interactive toxic effects of heavy metals and humic acids on Vibrio fischeri. Ecotoxicol Environ Saf 63:158–167. https://doi.org/10.1016/j.ecoenv.2005.04.005
Walsh GE, Garnas RL (1983) Determination of bioactivity of chemical fractions of liquid wastes using freshwater and saltwater algae and crustaceans. Environ Sci Technol 17:180–182. https://doi.org/10.1021/es00109a012
Walsh GE, Duke KM, Foster RB (1982) Algae and crustaceans as indicators of bioactivity of industrial wastes. Water Res 16:879–883. https://doi.org/10.1016/0043-1354(82)90017-3
Wang Z, Li J, Zhao J, Xing B (2011) Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environ Sci Technol 45:6032–6040. https://doi.org/10.1021/es2010573
Winner RW (1986) Relationship between chronic toxicity and bioaccumulation of copper, cadmium and zinc as affected by water hardness and humic Acid. Aquat Toxicol 8:149–161. https://doi.org/10.1016/0166-445X(86)90061-5
Winner RW (1991) Toxicity of copper to Chlamydomonas reinhardtii (Chlorophyceae) and Ceriodaphnia dubia (Crustacea) in relation to changes in water chemistry of a freshwater pond. Aquat Toxicol 19:157–169. https://doi.org/10.1016/0166-445X(91)90070-P
Yoshioka Y (2001) Ecotox-Statics ver.2.6d. Jpn J Environ Toxicol 4:113. http://www.intio.or.jp/jset/ecotox.htm. Accessed 12 Aug 2020
Funding
This work was supported under the JST/JICA Science and Technology Research Partnership for Sustainable Development (SATREPS) Project entitled “Wild Fire and Carbon Management in Peat-forest in Indonesia” and Heiwa Nakajima Foundation for Research in Asia region.
Author information
Authors and Affiliations
Author notes
Masami Fukushima is deceased. This paper is dedicated to his memory.
- Masami Fukushima
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 512 kb)
Rights and permissions
About this article
Cite this article
Nanayama, Y., Sazawa, K., Yustiawati, Y. et al. Effect of humic acids on the toxicity of pollutants to Chlamydomonas reinhardtii: Investigation by a microscale algal growth inhibition test. Environ Sci Pollut Res 28, 211–219 (2021). https://doi.org/10.1007/s11356-020-10425-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10425-8