Skip to main content
Log in

Assessing the effect of high doses of ampicillin on five marine and freshwater phytoplankton species: a biodegradation perspective

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Previous studies have identified several effects of antibiotic exposure at doses typically found in natural water (~μg). However, high doses of antibiotics can be found near wastewater treatment plants, and antibiotic concentrations in natural watercourses are likely to increase due to continuous current inputs. Therefore, the systematic evaluation of the susceptibility of phytoplankton species to antibiotics in water should be conducted for an improved risk assessment and the development of biotechnology for antibiotic residue management. The aim of the present study was, therefore, to investigate the response to high concentrations of ampicillin in several microalgae and cyanobacteria species with consideration of potential biodegradation applications for industrial and sanitary wastewaters. Pure laboratory cultures of freshwater (Dictyosphaerium chlorelloides, Chlamydomonas reinhardtii and Microcystis aeruginosa) and marine (Emiliania huxleyi and Prochloron sp.) species were exposed to several doses of ampicillin (6–14 mg L−1). Cell growth and other functions were followed in each species for up to a month. The results revealed that the species susceptibility to ampicillin varied greatly. No effect was observed in the chlorophytes, M. aeruginosa presented high inhibition and microcystin stimulation, upregulation/enhancement occurred in E. huxleyi, and photochemical stress occurred in the marine cyanobacterium Prochloron sp. Moreover, we observed that the ampicillin effect varied over time in susceptible species. Despite the variability of response, all the species presented high rates of antibiotic degradation. From these bioassays, it can be inferred that the effect of ampicillin cannot be generalized to microalgae groups. Additionally, the potential of microalgae to mitigate antibiotic impacts by degradation is a novel aspect yet to be investigated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acred P, Brown DM, Turner DH, Wilson MJ (1962) Pharmacology and chemotherapy of ampicillin—a new broad-spectrum penicillin. Br J Pharmacol Chemother 18:356–369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ali AM, Rønning HT, Alarif W, Kallenborn R, Al-Lihaibi SS (2017) Occurrence of pharmaceuticals and personal care products in effluent-dominated Saudi Arabian coastal waters of the Red Sea. Chemosphere 175:505–513

    CAS  PubMed  Google Scholar 

  • Ando T, Nagase H, Eguchi K, Hirooka T, Nakamura T, Miyamoto K, Hirata K (2007) A novel method using cyanobacteria for ecotoxicity test of veterinary antimicrobial agents. Environ Toxicol Chem 26:601–606

    CAS  PubMed  Google Scholar 

  • Arribas A, Herrero-Payo J (1979) Geochemical distribution of uranium in soils and vegetation of the “Fe 3” mine, Saelices, Salamanca, Spain. Phys Chem Earth 11:727–738

    Google Scholar 

  • Baquero F, Martínez J-L, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265

    CAS  PubMed  Google Scholar 

  • Behrenfeld MJ, O’Malley RT, Siegel DA, McClain CR, Sarmiento JL, Feldman GC, Milligan AJ, Falkowski PG, Letelier RM, Boss ES (2006) Climate-driven trends in contemporary ocean productivity. Nature 444:752–755

    CAS  Google Scholar 

  • Ben Chekroun K, Sanchez E, Baghour M (2014) The role of algae in bioremediation of organic pollutants. Int Res J Public Environ Health 1:19–32

    Google Scholar 

  • Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596

    CAS  PubMed  Google Scholar 

  • Campa-Córdova AI, Luna-González A, Ascencio F, Cortés-Jacinto E, Cáceres-Martínez CJ (2006) Effects of chloramphenicol, erythromycin, and furazolidone on growth of Isochrysis galbana and Chaetoceros gracilis. Aquaculture 260:145–150

    Google Scholar 

  • Christian T, Schneider RJ, Färber HA, Skutlarek D, Meyer MT, Goldbach HE (2003) Determination of antibiotic residues in manure, soil, and surface waters. Acta Hydrochim Hydrobiol 31:36–44

    CAS  Google Scholar 

  • Costanzo SD, Murby J, Bates J (2005) Ecosystem response to antibiotics entering the aquatic environment. Mar Pollut Bull 51:218–223

    CAS  PubMed  Google Scholar 

  • de Godos I, Muñoz R, Guieysse B (2012) Tetracycline removal during wastewater treatment in high-rate algal ponds. J Hazard Mater 229–230:446–449

    PubMed  Google Scholar 

  • De Magalhaes J, Borschiver S (2012) Amoxicillin and ampicillin-import trends and increasing use in Brazil. Chim Oggi-Chemistry Today 30:91–93

    Google Scholar 

  • Dias E, Oliveira M, Jones-Dias D, Vasconcelos V, Ferreira E, Manageiro V, Caniça M (2015) Assessing the antibiotic susceptibility of freshwater Cyanobacteria spp. Front Microbiol 6:799

    PubMed  PubMed Central  Google Scholar 

  • Dietrich D, Hoeger S (2005) Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? Toxicol Appl Pharmacol 203:273–289

    CAS  PubMed  Google Scholar 

  • Ding C, He J (2010) Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 87:925–941

    CAS  PubMed  Google Scholar 

  • Dolliver H, Gupta S, Noll S (2008) Antibiotic degradation during manure composting. J Environ Qual 37:1245

    CAS  PubMed  Google Scholar 

  • Downing TG, Meyer C, Gehringer MM, van de Venter M (2005) Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ Toxicol 20:257–262

    CAS  PubMed  Google Scholar 

  • Eguchi K, Nagase H, Ozawa M, Endoh YS, Goto K, Hirata K, Miyamoto K, Yoshimura H (2004) Evaluation of antimicrobial agents for veterinary use in the ecotoxicity test using microalgae. Chemosphere 57:1733–1738

    CAS  PubMed  Google Scholar 

  • Falkowski PG, Raven JA (2013) Aquatic photosynthesis: (Second Edition). Princeton University Press, Princeton

    Google Scholar 

  • Fatta-Kassinos D, Meric S, Nikolaou A (2011) Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem 399:251–275

    CAS  PubMed  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    CAS  PubMed  Google Scholar 

  • Forest A, Tremblay J, Gratton Y, Martin J (2011) Biogenic carbon flows through the planktonic food web of the Amundsen Gulf (Arctic Ocean): a synthesis of field measurements and inverse modeling analyses. Prog Oceanogr 91:410–436

    Google Scholar 

  • González-Plaza JJ, Šimatović A, Milaković M, Bielen A, Wichmann F, Udiković-Kolić N (2018) Functional repertoire of antibiotic resistance genes in antibiotic manufacturing effluents and receiving freshwater sediments. Front Microbiol 8:2675

    PubMed  PubMed Central  Google Scholar 

  • González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064

    PubMed  Google Scholar 

  • Graham LE, Graham JM, Wilcox LW (2009) Algae, 2nd edn. Benjamin Cummings, NY

    Google Scholar 

  • Grenni P, Ancona V, Barra Caracciolo A (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39

    CAS  Google Scholar 

  • Halling-Sorensen B (2000) Environmental risk assessment of antibiotics: comparison of mecillinam, trimethoprim and ciprofloxacin. J Antimicrob Chemother 46:53–58

    CAS  PubMed  Google Scholar 

  • Harke MJ, Gobler CJ (2013) Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One 8:e69834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holten Lützhøft HC, Halling-Sørensen B, Jørgensen SE (1999) Algal toxicity of antibacterial agents applied in Danish fish farming. Arch Environ Contam Toxicol 36:1–6

    Google Scholar 

  • Horst GP, Sarnelle O, White JD, Hamilton SK, Kaul RB, Bressie JD (2014) Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Res 54:188–198

    CAS  PubMed  Google Scholar 

  • Injac R, Kočevar N, Štrukelj B (2009) Optimized method for determination of amoxicillin, ampicillin, sulfamethoxazole, and sulfacetamide in animal feed by micellar electrokinetic capillary chromatography and comparison with high-performance liquid chromatography. Croat Chem Acta 82:685–694

    CAS  Google Scholar 

  • Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 346:87–98

    CAS  PubMed  Google Scholar 

  • Itoh S, Sugiura K (2004) Fluorescence of photosystem I. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. Springer Netherlands, Dordrecht, pp 231–250

  • Jun Y, Zhengyu L (1997) Advances in biological treatmemt processes of antibiotic production wastewater. J Environ Sci 18:83–85

    Google Scholar 

  • Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2008) The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface water in South Wales, UK. Water Res 42:3498–3518

    CAS  PubMed  Google Scholar 

  • Kemper N, Färber H, Skutlarek D, Krieter J (2008) Analysis of antibiotic residues in liquid manure and leachate of dairy farms in Northern Germany. Agric Water Manag 95:1288–1292

    Google Scholar 

  • Knapp CW, Dolfing J, Ehlert PAI, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44:580–587

    CAS  PubMed  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    CAS  Google Scholar 

  • Kulkarni P, Olson ND, Raspanti GA, Rosenberg Goldstein RE, Gibbs SG, Sapkota A, Sapkota AR (2017) Antibiotic concentrations decrease during wastewater treatment but persist at low levels in reclaimed water. Int J Environ Res Public Health:14

  • Kümmerer K (2001) Drugs in the environment: emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources - a review. Chemosphere 45:957–969

    PubMed  Google Scholar 

  • Kümmerer K (2009a) Antibiotics in the aquatic environment--a review--part I. Chemosphere 75:417–434

    PubMed  Google Scholar 

  • Kümmerer K (2009b) Antibiotics in the aquatic environment--a review--part II. Chemosphere 75:435–441

    PubMed  Google Scholar 

  • Kushner DJ, Breuil C (1977) Penicillinase (beta-lactamase) formation by blue-green algae. Arch Microbiol 112:219–223

    CAS  PubMed  Google Scholar 

  • Kvíderová J, Henley WJ (2005) The effect of ampicillin plus streptomycin on growth and photosynthesis of two halotolerant chlorophyte algae. J Appl Phycol 17:301–307

    Google Scholar 

  • Lai H-T, Hou J-H, Su C-I, Chen C-L (2009) Effects of chloramphenicol, florfenicol, and thiamphenicol on growth of algae Chlorella pyrenoidosa, Isochrysis galbana, and Tetraselmis chui. Ecotoxicol Environ Saf 72:329–334

    CAS  PubMed  Google Scholar 

  • Larsson DGJ, de Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148:751–755

    CAS  PubMed  Google Scholar 

  • Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473

    CAS  PubMed  Google Scholar 

  • Li D, Yang M, Hu J, Zhang Y, Chang H, Jin F (2008) Determination of penicillin G and its degradation products in a penicillin production wastewater treatment plant and the receiving river. Water Res 42:307–317

    CAS  PubMed  Google Scholar 

  • Liu Y, Gao B, Yue Q, Guan Y, Wang Y, Huang L (2012a) Influences of two antibiotic contaminants on the production, release and toxicity of microcystins. Ecotoxicol Environ Saf 77:79–87

    CAS  PubMed  Google Scholar 

  • Liu Y, Guan Y, Gao B, Yue Q (2012b) Antioxidant responses and degradation of two antibiotic contaminants in Microcystis aeruginosa. Ecotoxicol Environ Saf 86:23–30

    CAS  PubMed  Google Scholar 

  • Liu Y, Zhang J, Gao B, Feng S (2014) Combined effects of two antibiotic contaminants on Microcystis aeruginosa. J Hazard Mater 279:148–155

    CAS  PubMed  Google Scholar 

  • Lopez-Rodas V, Agrelo M, Carrillo E, Ferrero L, Larrauri A, Martin-Otero L, Costas E (2001) Resistance of microalgae to modern water contaminants as the result of rare spontaneous mutations. Eur J Phycol 36:179–190

    Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    CAS  PubMed  Google Scholar 

  • Mitchell SM, Ullman JL, Teel AL, Watts RJ (2014) pH and temperature effects on the hydrolysis of three β-lactam antibiotics: ampicillin, cefalotin and cefoxitin. Sci Total Environ 466–467:547–555

    PubMed  Google Scholar 

  • Nie XP, Liu BY, Yu HJ, Liu WQ, Yang YF (2013) Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole exposure to the antioxidant system in Pseudokirchneriella subcapitata. Environ Pollut 172:23–32

    CAS  PubMed  Google Scholar 

  • OECD (2011) Freshwater alga and cyanobacteria, growth inhibition test. Test guideline 201. OECD Guidel Test Chem 1–26

  • Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A (2010) Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One 5:e11000

    PubMed  PubMed Central  Google Scholar 

  • Orellana G, López-Rodas V, Costas E, Florez DH, Pampin EM (2010) Biosensors based on microalgae for the detection of environmental pollutants. US20100248286A1

  • Peña-Vázquez E, Maneiro E, Pérez-Conde C, Moreno-Bondi MC, Costas E (2009) Microalgae fiber optic biosensors for herbicide monitoring using sol-gel technology. Biosens Bioelectron 24:3538–3543

    PubMed  Google Scholar 

  • Podola B, Nowack ECM, Melkonian M (2004) The use of multiple-strain algal sensor chips for the detection and identification of volatile organic compounds. Biosens Bioelectron 19:1253–1260

    CAS  PubMed  Google Scholar 

  • Prabaharan D, Sumathi M, Subramanian G (1994) Ability to use ampicillin as a nitrogen source by the marine cyanobacterium Phormidium valderianum BDU 30501. Curr Microbiol 28:315–320

    CAS  Google Scholar 

  • Quezada MS, Rodríguez C del C, Cordoba-Diaz D (2012) Pharmacist’s role in the studies of the veterinary-medicines-residues depletion. Pharm Policy Law 14:223–228

    Google Scholar 

  • Ralph PJ, Schreiber U, Gademann R, Kühl M, Larkum AWD (2005) Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer. J Phycol 41:335–342

    Google Scholar 

  • Schiermeier Q (2010) Ocean greenery under warming stress A century of phytoplankton decline suggests that ocean ecosystems are in peril. Nature. https://doi.org/10.1038/news.2010.379

  • Shen L, Liu Y, Lou XH (2010) Treatment of ampicillin-loaded wastewater by combined adsorption and biodegradation. J Chem Technol Biotechnol 85:814–820

    CAS  Google Scholar 

  • Simon N, Cras A-L, Foulon E, Lemée R (2009) Diversity and evolution of marine phytoplankton. C R Biol 332:159–170

    PubMed  Google Scholar 

  • Smienk HGF, Sevilla Mur E, Peleato ML, Razquin P, Mata L (2007) Validación de un kit para la detección de microcistinas en agua. Aliment Rev Tecnol e Hig los Aliment:104–111

  • Snyder S, Lue-Hing C, Cotruvo J, Drewes JE, Eaton A, Pleus RC, Schlenk D (2009) Pharmaceuticals in the water environment. NACWA. https://www.acs.org/content/dam/acsorg/policy/acsonthehill/briefings/pharmaceuticalsinwater/nacwa-paper.pdf

  • Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014) Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14:742–750

    PubMed  Google Scholar 

  • van der Grinten E, Pikkemaat MG, van den Brandhof E-J, Stroomberg GJ, Kraak MH (2010) Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere 80:1–6

    PubMed  Google Scholar 

  • Versporten A (2013) Articles antibiotic use in eastern Europe: a cross-national database study in coordination with the WHO Regional Office for Europe

  • Vezie C, Brient L, Sivonen K, Bertru G, Lefeuvre J, Salkinoja-Salonen M (1998) Variation of microcystin content of cyanobacterial blooms and isolated strains in Lake Grand-Lieu (France). Microb Ecol 35:126–135

    CAS  PubMed  Google Scholar 

  • Wang Z, Chen Q, Hu L, Wang M (2018) Combined effects of binary antibiotic mixture on growth, microcystin production, and extracellular release of Microcystis aeruginosa: application of response surface methodology. Environ Sci Pollut Res 25:736–748

    CAS  Google Scholar 

  • Watanabe K (2001) Microorganisms relevant to bioremediation. Curr Opin Biotechnol 12:237–241

    CAS  PubMed  Google Scholar 

  • Watanabe MM, Zhang X, Kaya K (1996) Fate of toxic cyclic heptapeptides, microcystins, in toxic cyanobacteria upon grazing by the mixotrophic flagellate Poterioochromonas malhamensis (Ochromonadales, Chrysophyceae). Phycologia 35:203–206

    Google Scholar 

  • Watkinson AJ, Murby EJ, Kolpin DW, Costanzo SD (2009) The occurrence of antibiotics in an urban watershed: from wastewater to drinking water. Sci Total Environ 407:2711–2723

    CAS  PubMed  Google Scholar 

  • Wilde EW, Benemann JR (1993) Bioremoval of heavy metals by the use of microalgae. Biotechnol Adv 11:781–812

    CAS  PubMed  Google Scholar 

  • Wu B, Wang G, Wu J, Fu Q, Liu C (2014) Sources of heavy metals in surface sediments and an ecological risk assessment from two adjacent plateau reservoirs. PLoS One 9:e102101

    PubMed  PubMed Central  Google Scholar 

  • Yu Y, Zhou Y, Wang Z, Torres OL, Guo R, Chen J (2017) Investigation of the removal mechanism of antibiotic ceftazidime by green algae and subsequent microbic impact assessment. Sci Rep 7:4168

    PubMed  PubMed Central  Google Scholar 

  • Zhang R, Tang J, Li J, Cheng Z, Chaemfa C, Liu D, Zheng Q, Song M, Luo C, Zhang G (2013) Occurrence and risks of antibiotics in the coastal aquatic environment of the Yellow Sea, North China. Sci Total Environ 450–451:197–204

    PubMed  Google Scholar 

  • Zhou P, Su C, Li B, Qian Y (2006) Treatment of high-strength pharmaceutical wastewater and removal of antibiotics in anaerobic and aerobic biological treatment processes. J Environ Eng 132:129–136

    CAS  Google Scholar 

Download references

Acknowledgments

Thanks are given to Lara de Miguel and Eva Salgado for their excellent technical support. This work was supported by the Dirección General de Salud Pública, Comunidad de Madrid (Art. 83 UCM/2018).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Camino García-Balboa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 32 kb)

ESM 2

(DOCX 1566 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baselga-Cervera, B., Cordoba-Diaz, M., García-Balboa, C. et al. Assessing the effect of high doses of ampicillin on five marine and freshwater phytoplankton species: a biodegradation perspective. J Appl Phycol 31, 2999–3010 (2019). https://doi.org/10.1007/s10811-019-01823-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01823-8

Keywords

Navigation