Impact of erythromycin on a non-target organism: Cellular effects on the freshwater microalga Pseudokirchneriella subcapitata
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The increasing and indiscriminate use of antibiotics is the origin of their introduction in aquatic systems through domestic and livestock effluents. The occurrence of erythromycin (ERY), a macrolide antibiotic, in water bodies raises serious concerns about its potential toxic effect in aquatic biota (non-target organisms), particularly in microalgae, the first organisms in contact with aquatic contaminants. This study aimed to evaluate the possible toxic effects of ERY on relevant cell targets of the freshwater microalga Pseudokirchneriella subcapitata. Algal cells incubated with significant environmental ERY concentrations presented disturbance of the photosynthetic apparatus (increased algal autofluorescence and reduction of chlorophyll a content) and mitochondrial function (hyperpolarization of mitochondrial membrane). These perturbations can apparently be attributed to the similarity of the translational machinery of these organelles (chloroplasts and mitochondria) with the prokaryotic cells. P. subcapitata cells treated with ERY showed a modification of metabolic activity (increased esterase activity) and redox state (alteration of intracellular levels of reactive oxygen species and reduced glutathione content) and an increased biovolume. ERY induced an algistatic effect: reduction of growth rate without loss of cell viability (plasma membrane integrity). The present study shows that chronic exposure (72 h), at low (μg L-1) ERY concentrations (within the range of concentrations detected in surface and ground waters), induce disturbances in the physiological state of the alga P. subcapitata. Additionally, this work alerts to the possible negative impact of the uncontrolled use of ERY on the aquatic systems.
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ERY has adverse effects on freshwater microalgae.
“One group of organisms that has come under scrutiny is freshwater microalgae, where studies have illuminated the adverse effects of ERY (Machado and Soares 2019).”
From Integrated morpho-physiological and biochemical description of the mechanisms leading stress responses in cyanobacteria (Arthrospira platensis) upon exposure to Erythromycin (2025) · cites this paper as Machado and Soares 2019
Low concentrations of antibiotics can have ecological hazards and impact non-targeted organisms.
“The ostensibly low concentrations of antibiotics belie their potential ecological hazards and impact on non-targeted organisms (Machado and Soares 2019).”
From Integrated morpho-physiological and biochemical description of the mechanisms leading stress responses in cyanobacteria (Arthrospira platensis) upon exposure to Erythromycin (2025) · cites this paper as Machado and Soares 2019
ERY enhanced accumulation of ROS in non-target aquatic biota such as P. subcapitata.
“Machado and Soares (2019) reported that ERY enhanced the accumulation of ROS in non-target aquatic biota such as the freshwater microalga P. subcapitata .”
From Integrated morpho-physiological and biochemical description of the mechanisms leading stress responses in cyanobacteria (Arthrospira platensis) upon exposure to Erythromycin (2025) · cites this paper as Machado and Soares (2019)
Cites
Reactive oxygen species: Metabolism, oxidative stress, and signal transduction
Apel, K., & Hirt, H. (2004) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.55.031903.141701 · Cited by 11,723 · see citing works
Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., & Buxton, H. T. (2002) · Environmental Science & Technology · doi:10.1021/es011055j · Cited by 7,953 · see citing works
Origins and evolution of antibiotic resistance
Davies, J., & Davies, D. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00016-10 · Cited by 5,784 · see citing works
Lodish, H. F. (1986) · Cited by 5,640 · see citing works
Occurrence, fate and effects of pharmaceutical substances in the environment- A review
Halling-Sørensen, B., Nors Nielsen, S., Lanzky, P. F., Ingerslev, F., Holten Lützhøft, H. C., & Jørgensen, S. E. (1998) · Chemosphere · doi:10.1016/s0045-6535(97)00354-8 · Cited by 3,285 · see citing works
Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions
Asada, K. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.082040 · Cited by 2,758 · see citing works
Occurrence of Antibiotics in the Aquatic Environment
Hirsch, R., Ternes, T., Haberer, K., & Kratz, K.-L. (1999) · Science of The Total Environment · doi:10.1016/s0048-9697(98)00337-4 · Cited by 2,140 · see citing works
Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2005.03.013 · Cited by 1,795 · see citing works
Katzung, B. G. (2018) · Cited by 1,383 · see citing works
Geometric models for calculating cell biovolume and surface area for phytoplankton
Sun, J. (2003) · Journal of Plankton Research · doi:10.1093/plankt/fbg096 · Cited by 1,154 · see citing works
Essential versus accessory aspects of cell death: recommendations of the NCCD 2015
Galluzzi, L., Bravo-San Pedro, J. M., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Alnemri, E. S., Altucci, L., Andrews, D., Annicchiarico-Petruzzelli, M., et al. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.137 · Cited by 1,002 · see citing works
González-Pleiter, M., Gonzalo, S., Rodea‐Palomares, I., Leganés, F., Rosal, R., Boltes, K., Marco, E., & Fernández‐Piñas, F. (2013) · Water Research · doi:10.1016/j.watres.2013.01.020 · Cited by 786 · see citing works
Ritchie, R. J. (2008) · Photosynthetica · doi:10.1007/s11099-008-0019-7 · Cited by 684 · see citing works
Toxic and genotoxic evaluation of six antibiotics on non-target organisms
Isidori, M., Lavorgna, M., Nardelli, A., Pascarella, L., & Parrella, A. (2005) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2004.11.017 · Cited by 680 · see citing works
Tarpey, M. M., Wink, D. A., & Grisham, M. B. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00361.2003 · Cited by 673 · see citing works
(1987) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(87)90055-3 · Cited by 640 · see citing works
Antibiotics in agriculture and the risk to human health: how worried should we be?
Chang, Q., Wang, W., Regev‐Yochay, G., Lipsitch, M., & Hanage, W. P. (2014) · Evolutionary Applications · doi:10.1111/eva.12185 · Cited by 574 · see citing works
Determination of Antibiotic Residues in Manure, Soil, and Surface Waters
Christian, T., Schneider, R. J., Färber, H. A., Skutlarek, D., Meyer, M. T., & Goldbach, H. E. (2003) · Acta hydrochimica et hydrobiologica · doi:10.1002/aheh.200390014 · Cited by 538 · see citing works
Kerksick, C. M., & Willoughby, D. S. (2005) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-2-2-38 · Cited by 503 · see citing works
McArdell, C. S., Molnár, É., Suter, M. J. ‐., & Giger, W. (2003) · Environmental Science & Technology · doi:10.1021/es034368i · Cited by 485 · see citing works
Effect of antibiotics in the environment on microbial populations
Ding, C., & He, J. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2649-5 · Cited by 467 · see citing works
Protein import into chloroplasts
Soll, J., & Schleiff, E. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1333 · Cited by 462 · see citing works
The Origin and Establishment of the Plastid in Algae and Plants
Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130134 · Cited by 453 · see citing works
Identification of the pharmaceuticals for human use contaminating the Italian aquatic environment
Zuccato, E., Castiglioni, S., & Fanelli, R. (2005) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2005.03.001 · Cited by 406 · see citing works
Pharmacological approaches to restore mitochondrial function
Andreux, P. A., Houtkooper, R. H., & Auwerx, J. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4023 · Cited by 383 · see citing works
Evaluation of antimicrobial agents for veterinary use in the ecotoxicity test using microalgae
Eguchi, K., Nagase, H., Ozawa, M., ENDOH, Y. S., 後藤, 起., Hirata, K., Miyamoto, K., & Yoshimura, H. (2004) · Chemosphere · doi:10.1016/j.chemosphere.2004.07.017 · Cited by 330 · see citing works
Beale, S. I. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2005.05.005 · Cited by 289 · see citing works
The Chlamydomonas reinhardtii Plastid Chromosome
Maul, J., Lilly, J. W., Cui, L.-Y., dePamphilis, C., Miller, W., Harris, E. H., & Stern, D. (2002) · The Plant Cell Online · doi:10.1105/tpc.006155 · Cited by 280 · see citing works
Toxicological impacts of antibiotics on aquatic micro-organisms: A mini-review
Välitalo, P., Kruglova, A., Mikola, A., & Vahala, R. (2017) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2017.02.003 · Cited by 274 · see citing works
Jiang, Y., Li, M., Guo, C., An, D., Xu, J. F., Zhang, Y., & Xi, B. (2014) · Chemosphere · doi:10.1016/j.chemosphere.2014.04.075 · Cited by 266 · see citing works
Toxicity of 12 metal-based nanoparticles to algae, bacteria and protozoa
Aruoja, V., Pokhrel, S., Sihtmäe, M., et al. (2015) · Environmental Science Nano · doi:10.1039/c5en00057b · Cited by 213 · see citing works
Wan, J., Guo, P., Peng, X., & Wen, K. (2014) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2014.10.026 · Cited by 213 · see citing works
Nie, X., Liu, B.-Y., Yu, H., Liu, W., & Yang, Y.-F. (2012) · Environmental Pollution · doi:10.1016/j.envpol.2012.08.013 · Cited by 202 · see citing works
Franklin, N. M., Stauber, J. L., & Lim, R. P. (2001) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620200118 · Cited by 193 · see citing works
The chloroplast protein import system: From algae to trees
Shi, L.-X., & Theg, S. M. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.10.002 · Cited by 191 · see citing works
Occurrence of antibiotics as emerging contaminant substances in aquatic environment
Milić, N., Milanović, M., Grujić-Letić, N. N., Sekulić, M. T., Radonić, J. R., Mihajlović, I. J., & Miloradov, M. V. (2012) · International Journal of Environmental Health Research · doi:10.1080/09603123.2012.733934 · Cited by 188 · see citing works
Liu, Y., Nie, X., Liu, W., et al. (2011) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2011.01.022 · Cited by 188 · see citing works
Schafhauser, B. H., Kristofco, L. A., de Oliveira, C. M. R., & Brooks, B. W. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.03.052 · Cited by 187 · see citing works
Chloroplast ribosomes and protein synthesis
Harris, E. H., Boynton, J. E., & Gillham, N. W. (1994) · Microbiological Reviews · doi:10.1128/mr.58.4.700-754.1994 · Cited by 182 · see citing works
Zhang, R., Tang, J., Li, J., Cheng, Z., Chaemfa, C., Liu, D., Zheng, Q., Song, M., Luo, C., & Zhang, G. (2013) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2013.02.024 · Cited by 180 · see citing works
PAN, X., DENG, C., ZHANG, D., WANG, J., Guang‐Li, M. U., & CHEN, Y. (2008) · Aquatic Toxicology · doi:10.1016/j.aquatox.2008.06.018 · Cited by 155 · see citing works
Ji, K., Kim, S., Han, S. B., Seo, J., Lee, S., Park, Y., Choi, K., Kho, Y., Kim, P.-G., Park, J., et al. (2012) · Ecotoxicology · doi:10.1007/s10646-012-0956-6 · Cited by 143 · see citing works
Gallaher, S. D., Fitz‐Gibbon, S. T., Strenkert, D., Purvine, S. O., Pellegrini, M. A., & Merchant, S. (2017) · The Plant Journal · doi:10.1111/tpj.13788 · Cited by 125 · see citing works
Chlorophyll a fluorescence as a biomarker for rapid toxicity assessment
Fai, P. B. A., Grant, A., & Reid, B. J. (2007) · Environmental Toxicology and Chemistry · doi:10.1897/06-394r1.1 · Cited by 115 · see citing works
A novel method using cyanobacteria for ecotoxicity test of veterinary antimicrobial agents
Ando, T., Nagase, H., Eguchi, K., Hirooka, T., Nakamura, T., Miyamoto, K., & Hirata, K. (2007) · Environmental Toxicology and Chemistry · doi:10.1897/06-195r.1 · Cited by 112 · see citing works
Xue, B., Zhang, R., Wang, Y., et al. (2013) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2013.02.009 · Cited by 109 · see citing works
Forkink, M., Manjeri, G. R., Liemburg-Apers, D. C., Nibbeling, E. A. R., Blanchard, M. G., Wojtala, A., Smeitink, J. A. M., Wieckowski, M. R., Willems, P. H. G. M., & Koopman, W. J. H. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2014.04.008 · Cited by 106 · see citing works
Selection and sensitivity comparisons of algal species for toxicity testing
Rojíčková, R., & Maršálek, B. (1999) · Chemosphere · doi:10.1016/s0045-6535(98)00566-9 · Cited by 103 · see citing works
Samson, G., Morisette, J. C., & Popovic, R. B. (1988) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1988.tb02829.x · Cited by 92 · see citing works
Oxford Dictionary of Biochemistry and Molecular Biology
(2006) · Oxford University Press eBooks · doi:10.1093/acref/9780198529170.001.0001 · Cited by 91 · see citing works
Liu, B., Liu, W., Nie, X., et al. (2011) · Journal of Environmental Sciences · doi:10.1016/s1001-0742(10)60608-0 · Cited by 81 · see citing works
Effect of antibiotics on bacterial populations: a multi-hierarchical selection process
Martínez, J. L. (2017) · F1000Research · doi:10.12688/f1000research.9685.1 · Cited by 78 · see citing works
Soto, P., Gaete, H., & Hidalgo, M. E. (2011) · Latin American Journal of Aquatic Research · doi:10.3856/vol39-issue2-fulltext-9 · Cited by 76 · see citing works
Machado, M. D., & Soares, E. V. (2013) · Aquatic Toxicology · doi:10.1016/j.aquatox.2013.11.017 · Cited by 68 · see citing works
Self-citationSendra, M., Moreno‐Garrido, I., Blasco, J., & Araújo, C. V. M. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.07.009 · Cited by 66 · see citing works
González-Pleiter, M., Rioboo, C., Reguera, M., Abreu, I., Leganés, F., Cid, Á., & Fernández‐Piñas, F. (2017) · Aquatic Toxicology · doi:10.1016/j.aquatox.2017.02.021 · Cited by 63 · see citing works
Soto, P., Gaete, H., & Hidalgo, M. E. (2011) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · doi:10.4067/s0718-560x2011000200009 · Cited by 58 · see citing works
Chloramphenicol is an inhibitor of photosynthesis
Okada, K., Satoh, K., & Katoh, S. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)81407-y · Cited by 57 · see citing works
Sousa, C. A., Soares, H. M. V. M., & Soares, E. V. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2018.08.022 · Cited by 57 · see citing works
Self-citationYruela, I., Alfonso, M., de Zarate, I. O., et al. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53906-5 · Cited by 56 · see citing works
Pérez, R. A., Albero, B., Férriz, M., & Tadeo, J. L. (2017) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2017.08.013 · Cited by 48 · see citing works
Bacterial responses to antibiotics and their combinations
Mitosch, K., & Bollenbach, T. (2014) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12190 · Cited by 43 · see citing works
Machado, M. D., & Soares, E. V. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4185-y · Cited by 42 · see citing works
Self-citationThe interference of the macrolide antibiotics with mitochondrial protein synthesis
Vries, H. D., Arendzen, A. J., & Kroon, A. (1973) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(73)90439-5 · Cited by 42 · see citing works
Sensitivity of freshwater and marine green algae to three compounds of emerging concern
Machado, M. D., & Soares, E. V. (2019) · Journal of Applied Phycology · doi:10.1007/s10811-018-1511-5 · Cited by 36 · see citing works
Self-citationMachado, M. D., & Soares, E. V. (2016) · CLEAN - Soil Air Water · doi:10.1002/clen.201600020 · Cited by 33 · see citing works
Self-citationToxic effects of erythromycin on photosystem I and II in Microcystis aeruginosa
Deng, C. N., Zhang, D. Y., & Pan, X. (2014) · Photosynthetica · doi:10.1007/s11099-014-0063-4 · Cited by 27 · see citing works
Waiser, M. J., Swerhone, G. D. W., Roy, J. W., et al. (2016) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2016.05.026 · Cited by 24 · see citing works
Machado, M. D., & Soares, E. V. (2012) · Journal of Applied Phycology · doi:10.1007/s10811-012-9811-7 · Cited by 23 · see citing works
Self-citationMachado, M. D., & Soares, E. V. (2012) · Water Air & Soil Pollution · doi:10.1007/s11270-012-1358-3 · Cited by 22 · see citing works
Self-citationIntracellular free Ca 2+ signals antibiotic exposure in cyanobacteria
González-Pleiter, M., Leganés, F., & Fernández‐Piñas, F. (2017) · RSC Advances · doi:10.1039/c7ra03001k · Cited by 12 · see citing works
Optimization of analytical methods to improve detection of erythromycin from water and sediment.
Jessick, A. M., Moorman, T. B., & Coats, J. R. (2011) · PubMed · doi:10.1080/03601234.2011.603974 · Cited by 6 · see citing works
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Ainas, M., Touzout, N., Tahraoui, H., Mokeddem, H. E., Moussa, H., Kherbouche, S., Mebrouk, S., Zhang, J., & Amrane, A. (2025) · Ecotoxicology · doi:10.1007/s10646-025-02888-7 · Cited by 8 · see citing works
“…interaction between antibiotics and algae unfolds further in earlier studies that observed harmful effects of ERY, even at concentrations as low as 0.2 mg/L, on species like Pseu-dokirchneriella subcapitata , with an EC50 (50% inhibition concentration) of 0.2 mg/L (Machado and Soares 2019).”
Influential
- Authors
- Machado, M. D., & Soares, E. V.
- Affiliations
- Centro de Inovação em Engenharia e Tecnologia Industrial (PT)
- Corresponding author
- Machado, Manuela D.
- Soares, Eduardo V.
- Venue
- Aquatic Toxicology
- Publisher
- Elsevier BV
- Published
- 2019-03
- Volume
- 208
- Pages
- 179-186
- ISSN
- 0166-445X (ISSN-L)
- OpenAlex
- W2909818607
- Cited by
- 68
- References
- 72
- Citations by year
- 2026: 6 · 2025: 12 · 2024: 9 · 2023: 12 · 2022: 10 · 2021: 11 · 2020: 7 · 2019: 1
- FWCI
- 2.17
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Aquatic Toxicology (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, other-oa)
- Funders
- Portuguese Foundation for Science and Technology (FCT) (UID/BIO/04469/2013)
- COMPETE 2020 (POCI-01-0145-FEDER-006684)
- BioTecNorte operation (NORTE-01-0145-FEDER-000004)
- European Regional Development Fund
- FCT (SFRH/BPD/72816/2010)
- Topics
- Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Keywords
- erythromycin, macrolide antibiotics, Pseudokirchneriella subcapitata, freshwater microalgae, antibiotic toxicity, photosynthetic apparatus, chlorophyll a, mitochondrial membrane hyperpolarization, esterase activity, reactive oxygen species, glutathione, non-target organisms
- MeSH terms
- Chlorophyll A, Anti-Bacterial Agents, Cell Survival, Erythromycin, Fluorescence, Fresh Water, Glutathione, Water Pollutants, Chemical, Reactive Oxygen Species, Intracellular Space, Membrane Potential, Mitochondrial, Microalgae
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