The effect of field-collected biofilms on the toxicity of copper to a marine microalga (Tetraselmis sp.) in laboratory bioassays
Jacqueline L. Levy A B E , Jenny L. Stauber B , Steven A. Wakelin C D and Dianne F. Jolley A
+ Author Affiliations
- Author Affiliations
A School of Chemistry, University of Wollongong, Wollongong, NSW 2522, Australia.
B Centre for Environmental Contaminants Research, CSIRO Land and Water, Locked Bag 2007, Kirrawee, NSW 2232, Australia.
C Centre for Environmental Contaminants Research, CSIRO Land and Water, Waite Campus, Private Mail Bag 2, Glen Osmond, SA 5064, Australia.
D AgResearch Ltd, Lincoln Science Centre, Private Bag 4749, Christchurch 8140, New Zealand.
E Corresponding author. Email: jacqui.levy@gmail.com
Marine and Freshwater Research 62(12) 1362-1372 https://doi.org/10.1071/MF10313
Submitted: 10 December 2010 Accepted: 16 August 2011 Published: 27 October 2011
Abstract
Standard algal growth rate inhibition bioassays can lack environmental realism and may over- or underestimate metal bioavailability in natural systems. In aquatic environments, algal species interact with other biota, including other algae, bacteria and biofilms. In this work, the feasibility of incorporating marine biofilms into 72 h algal growth inhibition toxicity tests was explored. The effects of copper on Tetraselmis sp. were tested in the absence and presence of characterised field-collected biofilms. We hypothesised that the addition of biofilm would prevent copper toxicity to the alga primarily through interactions of the metal with other cells and biofilm exudates. The sensitivity of Tetraselmis sp. to copper (based on 72 h IC50 values; the copper concentration to inhibit population growth by 50%) in the presence of a blended biofilm inoculum varied 2-fold and was independent of the amount of biofilm added. However, increases in IC10 and IC20 values indicated some amelioration of copper toxicity. When intact biofilms were added to the bioassays, amelioration of toxicity was more consistent, probably due to increased binding of copper to cell surfaces or exudates. Difficulties in characterising biofilms and distinguishing that material from the test alga need to be overcome before biofilms can be routinely incorporated into laboratory bioassays.
Additional keywords: bacteria, Cu, marine, PCR-DGGE, phytoplankton.
References
Adams, M. S., and Stauber, J. L. (2004). Development of a whole-sediment toxicity test using a benthic marine microalga. Environmental Toxicology and Chemistry 23, 1957–1968.| Development of a whole-sediment toxicity test using a benthic marine microalga.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFOisLo%3D&md5=a993cb2a80aaf01481570a9f3f15ecdfCAS |
Adler, N. E., Schmitt-Jansen, M., and Altenburger, R. (2007). Flow cytometry as a tool to study phytotoxic modes of action. Environmental Toxicology and Chemistry 26, 297–306.
| Flow cytometry as a tool to study phytotoxic modes of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWmsrY%3D&md5=35db21e181e3219ecfe6c1bc177a0b91CAS |
Admiraal, W., Blanck, H., Buckert-De Jong, M., Guasch, H., Ivorra, N., et al. (1999). Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream. Water Research 33, 1989–1996.
| Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjslGjsr0%3D&md5=f4d6939484b42412192a7642859105f0CAS |
APHA/AWWA/WEF (2006). ‘Standard Methods for the Examination of Water and Wastewater.’ (American Public Health Association, American Water Works Association, Water Environment Federation: Washington, DC.)
Barranguet, C., Charantoni, E., Plans, M., and Admiraal, W. (2000). Short-term response of monospecific and natural algal biofilms to copper exposure. European Journal of Phycology 35, 397–406.
| Short-term response of monospecific and natural algal biofilms to copper exposure.Crossref | GoogleScholarGoogle Scholar |
Barranguet, C., Plans, M., van der Grinten, E., Sinke, J. J., and Admiraal, W. (2002). Development of photosynthetic biofilms affected by dissolved and sorbed copper in a eutrophic river. Environmental Toxicology and Chemistry 21, 1955–1965.
| Development of photosynthetic biofilms affected by dissolved and sorbed copper in a eutrophic river.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt12jt7c%3D&md5=fb9f1b329afdb71f253d2e7106b50273CAS |
Barranguet, C., van den Ende, F. P., Rutgers, M., Breure, A. M., Greijdanus, M., et al. (2003). Copper-induced modifications of the trophic relations in riverine algal-bacterial biofilms. Environmental Toxicology and Chemistry 22, 1340–1349.
| 1:CAS:528:DC%2BD3sXnsVGgsrc%3D&md5=fa7c406ce258a31b50e44c76a8f7814cCAS |
Barranguet, C., Veuger, B., Van Beusekom, S. A. M., Marvan, P., Sinke, J. J., et al. (2005). Divergent composition of algal-bacterial biofilms developing under various external factors. European Journal of Phycology 40, 1–8.
| Divergent composition of algal-bacterial biofilms developing under various external factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivF2iu7g%3D&md5=4b67f26aef6146c2d45171f6bf679180CAS |
Biggs, B. J. F., and Kilroy, C. (2000). ‘Stream Periphyton Monitoring Manual.’ (National Institute of Water and Atmospheric Research: Christchurch, NZ.)
Boivin, M.-E. Y., Massieux, B., Breure, A. M., van den Ende, F. P., Greve, G. D., et al. (2005). Effects of copper and temperature on aquatic bacterial communities. Aquatic Toxicology 71, 345–356.
| Effects of copper and temperature on aquatic bacterial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCkt78%3D&md5=74f09a9b151e76f6af751f9d27b7acbcCAS |
Bradac, P., Wagner, B., Kistler, D., Traber, J., Behra, R., et al. (2010). Cadmium speciation and accumulation in periphyton in a small stream with dynamic concentration variations. Environmental Pollution 158, 641–648.
| Cadmium speciation and accumulation in periphyton in a small stream with dynamic concentration variations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1Onsg%3D%3D&md5=6bb4a48c60b448cd44bac67e4111f84bCAS |
Burmølle, M., Webb, J. S., Rao, D., Hansen, L. H., Sørensen, S. J., et al. (2006). Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Applied and Environmental Microbiology 72, 3916–3923.
| Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms.Crossref | GoogleScholarGoogle Scholar |
Burns, A., and Ryder, D. S. (2001). Potential for biofilms as biological indicators in Australian riverine systems. Ecological Management & Restoration 2, 53–64.
| Potential for biofilms as biological indicators in Australian riverine systems.Crossref | GoogleScholarGoogle Scholar |
Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
| Non-parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappinscott, H. M. (1995). Microbial biofilms. Annual Review of Microbiology 49, 711–745.
| Microbial biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovVWjtbg%3D&md5=ef2a5d489ca6c98a7b65adae2049564dCAS |
Dillon, J. G., McMath, L. M., and Trout, A. L. (2009). Seasonal changes in bacterial diversity in the Salton Sea. Hydrobiologia 632, 49–64.
| Seasonal changes in bacterial diversity in the Salton Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVSgtbw%3D&md5=e9fe0f8838ad11b9546ef835d51ab406CAS |
Franklin, N. M., Adams, M. S., Stauber, J. L., and Lim, R. P. (2001). Development of an improved rapid enzyme inhibition bioassay with marine and freshwater microalgae using flow cytometry. Archives of Environmental Contamination and Toxicology 40, 469–480.
| Development of an improved rapid enzyme inhibition bioassay with marine and freshwater microalgae using flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivVGht7g%3D&md5=64590453d912260ba81d9d0be0a024aeCAS |
Franklin, N. M., Stauber, J. L., Apte, S. C., and Lim, R. P. (2002). Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environmental Toxicology and Chemistry 21, 742–751.
| Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlCqt7Y%3D&md5=b8f354eec32b7d836288f8d8577c7954CAS |
Franklin, N. M., Stauber, J. L., and Lim, R. P. (2004). Development of multispecies algal bioassays using flow cytometry. Environmental Toxicology and Chemistry 23, 1452–1462.
| Development of multispecies algal bioassays using flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1ylsb0%3D&md5=7000c9dfa1b83fa85d259ab548a52344CAS |
Fuchs, S., Haritopoulou, T., Schafer, M., and Wilhelmi, M. (1997). Heavy metals in freshwater ecosystems introduced by urban rainwater runoff – monitoring of suspended solids, river sediments and biofilms. Water Science and Technology 36, 277–282.
| Heavy metals in freshwater ecosystems introduced by urban rainwater runoff – monitoring of suspended solids, river sediments and biofilms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFKjsA%3D%3D&md5=65d6c96a8746710b2ba84655d8a83085CAS |
García-Meza, J. V., Barranguet, C., and Admiraal, W. (2005). Biofilm formation by algae as a mechanism for surviving on mine tailings. Environmental Toxicology and Chemistry 24, 573–581.
| Biofilm formation by algae as a mechanism for surviving on mine tailings.Crossref | GoogleScholarGoogle Scholar |
Gold, C., Feurtet-Mazel, A., Coste, M., and Boudou, A. (2003). Impacts of Cd and Zn on the development of periphytic diatom communities in artificial streams located along a river pollution gradient. Archives of Environmental Contamination and Toxicology 44, 189–197.
| Impacts of Cd and Zn on the development of periphytic diatom communities in artificial streams located along a river pollution gradient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsF2ntw%3D%3D&md5=b01aa25f155ec7584ff4445a94de52edCAS |
Grossart, H. P. (1999). Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis and Thalassiosira weissflogii) incubated under various conditions in the lab. Aquatic Microbial Ecology 19, 1–11.
| Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis and Thalassiosira weissflogii) incubated under various conditions in the lab.Crossref | GoogleScholarGoogle Scholar |
Harris, E., and Angal, S. (Eds) (1989) ‘Protein Purification Methods – A Practical Approach.’ (Oxford University Press: Oxford.)
Holding, K. L., Gill, R. A., and Carter, J. (2003). The relationship between epilithic periphyton (biofilm) bound metals and metals bound to sediments in freshwater systems. Environmental Geochemistry and Health 25, 87–93.
| The relationship between epilithic periphyton (biofilm) bound metals and metals bound to sediments in freshwater systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFyqu7w%3D&md5=f92a988800e0284dbe1d27687601adffCAS |
Hu, Z. Q., Jin, J., Abruna, H. D., Houston, P. L., Hay, A. G., et al. (2007). Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy. Environmental Science & Technology 41, 936–941.
| Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlaksrfP&md5=1b70b18639cd74b5bdf74ff0e608adcdCAS |
Ivorra, N., Barranguet, C., Jonker, M., Kraak, M. H. S., and Admiraal, W. (2002). Metal-induced tolerance in the freshwater microbenthic diatom Gomphonema parvulum. Environmental Pollution 116, 147–157.
| Metal-induced tolerance in the freshwater microbenthic diatom Gomphonema parvulum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXot1Oisrk%3D&md5=a9fc19ba95e4176a443cee8c3fad3421CAS |
Koukal, B., Rosse, P., Reinhardt, A., Ferrari, B., Wilkinson, K. J., et al. (2007). Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation. Water Research 41, 63–70.
| Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1KitbbJ&md5=0c6a545561716aa0fe4cb4c33b5ac319CAS |
Levy, J. L., Stauber, J. L., and Jolley, D. F. (2007). Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Science of the Total Environment 387, 141–154.
| Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVyrsLfI&md5=0588d36c76081c46640ef88b3daf21a6CAS |
Levy, J. L., Angel, B. M., Stauber, J. L., Poon, W. L., Simpson, S. L., et al. (2008). Uptake and internalisation of copper by three marine microalgae: comparison of copper sensitive and copper tolerant species. Aquatic Toxicology 89, 82–93.
| Uptake and internalisation of copper by three marine microalgae: comparison of copper sensitive and copper tolerant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Gntrk%3D&md5=f584d621d544b4e7c10180f89a90ab52CAS |
Levy, J. L., Stauber, J. L., Wakelin, S. A., and Jolley, D. F. (2009). The effect of bacteria on the sensitivity of microalgae to copper in laboratory bioassays. Chemosphere 74, 1266–1274.
| The effect of bacteria on the sensitivity of microalgae to copper in laboratory bioassays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVygtr8%3D&md5=51258e8c48d6fdf7f663af00f893d340CAS |
Mages, M., Ovari, M., von Tumpling, W., and Kropfl, K. (2004). Biofilms as bio-indicator for polluted waters? Total reflection x-ray fluorescence analysis of biofilms of the Tisza river (Hungary). Analytical and Bioanalytical Chemistry 378, 1095–1101.
| 1:CAS:528:DC%2BD2cXhsVOqurk%3D&md5=e7acae0e1f532001b2c2fcf4ee18fde8CAS |
Massieux, B., Boivin, M. E. Y., van den Ende, F. P., Langenskiold, J., Marvan, P., et al. (2004). Analysis of structural and physiological profiles to assess the effects of Cu on biofilm microbial communities. Applied and Environmental Microbiology 70, 4512–4521.
| Analysis of structural and physiological profiles to assess the effects of Cu on biofilm microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1elt7c%3D&md5=51e2955c4b98e85d178381dc32f8d032CAS |
Meylan, S., Behra, R., and Sigg, L. (2003). Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater. Environmental Science & Technology 37, 5204–5212.
| Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Oisbk%3D&md5=db803cbd175a868d9f041ea2730ac092CAS |
Morel, F. M. M., and Palenik, B. (1989). The aquatic chemistry of trace metals in biofilms. In ‘Structure and Function of Biofilms’. (Eds W. G. Characklis and P. A. Wilderer.) pp. 289–300. (John Wiley & Sons: Chichester, UK.)
Muyzer, G., Dewaal, E. C., and Uitterlinden, A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59, 695–700.
| 1:CAS:528:DyaK3sXit1Kktrk%3D&md5=9772f43d30f6f8699da688f15cd17886CAS |
Palmer, R. J., and White, D. C. (1997). Developmental biology of biofilms: implications for treatment and control. Trends in Microbiology 5, 435–440.
| Developmental biology of biofilms: implications for treatment and control.Crossref | GoogleScholarGoogle Scholar |
Rodgers, J. H., Dickson, K. L., and Cairns, J. (1979). A review and analysis of some methods used to measure functional aspects of periphyton. In ‘Methods and Measurements of Periphyton Communities: a Review, ASTM STP 690’. (Ed. R. L. Weitzel.) pp. 142–167. (American Society for Testing and Materials: Philadelphia, PA, USA.)
Serra, A., Guasch, H., Admiraal, W., Van der Geest, H. G., and Van Beusekom, S. A. M. (2010). Influence of phosphorus on copper sensitivity of fluvial periphyton: the role of chemical, physiological and community-related factors. Ecotoxicology 19, 770–780.
| Influence of phosphorus on copper sensitivity of fluvial periphyton: the role of chemical, physiological and community-related factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvVeisrc%3D&md5=993d716a4da7b77cab8d346426689ffbCAS |
Soldo, D., and Behra, R. (2000). Long-term effects of copper on the structure of freshwater periphyton communities and their tolerance to copper, zinc, nickel and silver. Aquatic Toxicology 47, 181–189.
| Long-term effects of copper on the structure of freshwater periphyton communities and their tolerance to copper, zinc, nickel and silver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1Sms78%3D&md5=9c095e55629529e3972fbe055fbde603CAS |
Sprague, J. B., and Fogels, A. (1976). Watch the Y in bioassay. In ‘Proceedings of the 3rd Aquatic Toxicity Workshop’. (Eds W. R. Parker, E. Pessah, P. G. Wells and G. F. Westlake.) pp. 107–118. (Environmental Protection Service, Environment Canada: Ottawa, ON, Canada.)
Stal, L. J., and Défarge, C. (2005). Structure and dynamics of exopolymers in an intertidal diatom biofilm. Geomicrobiology Journal 22, 341–352.
| Structure and dynamics of exopolymers in an intertidal diatom biofilm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVajsLvL&md5=d8b2603880c9a6f77c221f4e5cc95ff8CAS |
Stauber, J. L., and Davies, C. M. (2000). Use and limitations of microbial bioassays for assessing copper bioavailability in the aquatic environment. Environmental Reviews 8, 255–301.
| Use and limitations of microbial bioassays for assessing copper bioavailability in the aquatic environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlagtLs%3D&md5=75b6976bd63bbffcd3491af4dd285c57CAS |
Sutherland, I. W. (2001). The biofilm matrix – an immobilised but dynamic microbial environment. Trends in Microbiology 9, 222–227.
| The biofilm matrix – an immobilised but dynamic microbial environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFSiu7o%3D&md5=fca79b3f80bc600d67a8875f03ff013cCAS |
Wakelin, S. A., Macdonald, L. M., Rogers, S. L., Gregg, A. L., Bolger, T. P., et al. (2008). Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biology & Biochemistry 40, 803–813.
| Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFKrtw%3D%3D&md5=98cb6bcc3a10d3913caffd8602f95205CAS |
Wilkinson, K., and Buffle, J. (2004). Critical evaluation of physicochemical parameters and processes for modelling the biological uptake of trace metals in environmental (aquatic) systems. In ‘Physicochemical Kinetics and Transport at Biointerfaces’. (Eds H. P. van Leeuwen and W. Köster.) pp. 445–533. (John Wiley & Sons: Chichester, UK.)
Yu, Y., Kong, F. X., Wang, M. L., Qian, L. L., and Shi, X. L. (2007). Determination of short-term copper toxicity in a multispecies microalgal population using flow cytometry. Ecotoxicology and Environmental Safety 66, 49–56.
| Determination of short-term copper toxicity in a multispecies microalgal population using flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Sjsr3M&md5=3785e5739613d5dd8c886fe2fe59f719CAS |
Zippel, B., and Neu, T. R. (2005). Growth and structure of phototrophic biofilms under controlled light conditions. Water Science and Technology 52, 203–209.
| 1:CAS:528:DC%2BD2MXhtlWntrnI&md5=f121a43a9ad7ca9d6cf232ce93e134d9CAS |
