Skip to main content
SpringerLink
Log in

Rapid adaptation of some phytoplankton species to osmium as a result of spontaneous mutations

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

To understand the vulnerability of individual species to anthropogenic contamination, it is important to evaluate the different abilities of phytoplankton to respond to environmental changes induced by pollution. The ability of a species to adapt, rather than its initial tolerance, is the basis for survival under rapidly increasing levels of anthropogenic contamination. High doses of osmium (Os) cause massive destruction of diverse phytoplankton groups. In this study, we found that the coastal chlorophyte Tetraselmis suecica and the continental chlorophyte Dictyosphaerium chlorelloides were able to adapt to a lethal dose of Os. In these species, Os-resistant cells arose as a result of rare spontaneous mutations (at rates of approximately 10−6 mutants per cell division) that occurred before exposure to Os. The mutants remained in the microalgal populations by means of mutation–selection balance. The huge size of phytoplankton populations ensures that there are always enough Os-resistant mutants to guarantee the survival of the population under Os pollution. In contrast, we observed that neither a haptophyte species from open ocean regions nor a cyanobacterium from continental freshwater were able to adapt to the lethal Os dose. Adaptation of phytoplankton to Os contamination is relevant because industrial activities are leading to a rapid increase in Os pollution worldwide.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Bañares-España E, López-Rodas V, Salgado C, Costas E, Flores-Moya A (2006) Interstrain variability in the photosynthetic use of inorganic carbon exemplified by the pH compensation point, in the cyanobacterium Microcystis aeruginosa. Aquac Bot 85(2):159–162

    Article  Google Scholar 

  • Baos R, Garcia-Villada L, Agrelo M, López Rodas V, Hiraldo F, Costas E (2002) Short-Term adaptation of microalgae in highly stressful environments: an experimental model analysing the resistance of Scenedesmus intermedius (Chlorophyceae) to the heavy metals mixture from the Aznalcollar mine spill. Eur J Phycol 37:593–600

    Article  Google Scholar 

  • Barbante C, Veysseyre A, Ferrari C, Velde K, Morel C, Copodaglio G, Cescon P, Scarponi G, Boutron C (2001) Greenland snow evidence of large scale atmospheric contamination for platinum, palladium, and rhodium. Environ Sci Technol 35:835–839

    Article  CAS  Google Scholar 

  • Belfiore NM, Anderson SI (2001) Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat Res 489:97–122

    Article  CAS  Google Scholar 

  • Bhattacharya S (2004) Experts divided over poison bomb claim (Online article), New Scientist, Accessed 7 Apr 2004

  • Bickham J (2011) The four cornerstones of evolutionary toxicology. Ecotoxicology 20(3):497–502

    Article  CAS  Google Scholar 

  • Bradley K, Karl Esser, Turekian K (1993) Anthropogenic osmium in coastal deposits. Environ Sci Technol 27(13):2719–2724

    Article  Google Scholar 

  • Bradshaw AD, Hardwick K (1989) Evolution and stress—genotype and phenotype components. Biol J Linn Soc 37:137–155

    Article  Google Scholar 

  • Cairns J, Overbaugh J, Miller S (1988) The origin of mutants. Nature 335:142–145

    Article  CAS  Google Scholar 

  • Carrera-Martínez D, Mateos-Sanz A, López-Rodas V, Costas E (2010) Microalgae response to petroleum spill: an experimental model analysing physiological and genetic response of Dunaliella tertiolecta (Chlorophyceae) to oil samples from the tanker Prestige. Aquat Toxicol 97:151–159

    Article  Google Scholar 

  • Chen C, Sedwick PN, Sharma M (2009) Anthropogenic osmium in rain. Proc Natl Acad Sci USA 106:7724–7728

    Article  CAS  Google Scholar 

  • Costas E (1990) Genetic variability in growth rates in marine Dinoflagellates. Genetica 83:99–102

    Article  Google Scholar 

  • Costas E, Carrillo E, Ferrero LM, Agrelo M, García-Villada L, Juste J, López-Rodas V (2001) Mutation of algae from sensitivity to resistance against environmental selective agents: the ecological genetics of D. chlorelloides (Chlorophyceae) under lethal doses of 3-(3,4-dichlorophenyl)-1,1-dimethylurea herbicide. Phycologia 40:391–398

    Article  Google Scholar 

  • Costas E, Flores-Moya A, Perdigones N, Maneiro E, Blanco JL, García ME, López-Rodas V (2007) How eukaryotic algae can adapt to the Spain’s Rio Tinto: a neo-Darwinian proposal for rapid adaptation to an extremely hostile ecosystem. New Phytol 175:334–339

    Article  Google Scholar 

  • Costas E, Flores-Moya A, López-Rodas V (2008) Rapid adaptation of algae to extreme environments (geothermal waters) by single mutation allows “Noah’s Arks” for photosynthesizers during the Neoproterozoic “Snowball Earth”. New Phytol 189:922–932

    Article  Google Scholar 

  • Costas E, Gonzalez R, López-Rodas V, Huertas IE (2013) Mutation of microalgae allows phytoplankton dispersion through ships biofouling. Biol Invasions. doi:10.1007/s10530-012-0405-8

    Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York

    Google Scholar 

  • Flores-Moya A, Costas E, Bañares-España E, García-Villada L, Altamirano M, López-Rodas V (2005) Adaptation of Spirogyra insignis (Chlorophyta) to an extreme natural environment (sulphureous waters) through preselective mutations. New Phytol 165:655–661

    Article  Google Scholar 

  • Foster PL (2000) Adaptive mutation: implications for evolution. BioEssays 22(106):7–74

    Google Scholar 

  • Gagnon ZE, Newkirk C, Hicks S (2006) Impact of platinum group metals on the environment: a toxicological, genotoxic and analytical chemistry study. J Environ Sci Health A 41:397–414

    Article  CAS  Google Scholar 

  • Garcia Villada L, Rico M, Altamirano M, Sanchez L, López Rodas V, Costas E (2004) Ocurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterization and future implications in the use of copper sulphate as algaecide. Water Res 38:2207–2213

    Article  CAS  Google Scholar 

  • Gonzalez A, Bell Graham (2011) Adaptation and evolutionary rescue in metapopulations experiencing environmental deterioration. Science 332:1327–1330

    Article  Google Scholar 

  • Gonzalez A, Ronce O, Ferriere R, Hochberg ME (2013) Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos Trans R Soc B 368:20120404

    Article  Google Scholar 

  • González R, García-Balboa C, Rouco M, Lopez-Rodas V, Costas E (2012) Adaptation of microalgae to lindane: a new approach for bioremediation. Aquat Toxicol 109:25–32

    Article  Google Scholar 

  • Heidenreich E (2007) Adaptive mutation in Saccharomyces cerevisiae. Crit Rev Biochem Mol 42:285–311

    Article  CAS  Google Scholar 

  • Huertas IE, Rouco M, López-Rodas V, Costas E (2010) Estimating the capability of different phytoplankton groups to adapt to contamination: herbicides will affect phytoplankton species differently. New Phytol 188:478–487

    Article  CAS  Google Scholar 

  • Huertas IE, Rouco M, López-Rodas V, Costas E (2011) Warming will affect phytoplankton differently: evidence through a mechanistic approach. Proc R Soc B 278:3534–3543

    Article  Google Scholar 

  • Kimura M, Maruyama T (1966) The mutational load with epistatic gene interactions in fitness. Genetics 54:1337–1351

    CAS  Google Scholar 

  • Lopez-Rodas V, Agrelo M, Carrillo E, Ferrero L, Larrauri A, Martín-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

    Article  Google Scholar 

  • Lopez-Rodas V, Marvá F, Costas E, Flores-Moya A (2008a) Microalgal adaptation in the stressful acidic, metal-rich mine waters from Mynydd Parys (N Wales, UK) could be due to selection of pre-selective mutants. Environ Exp Bot 61:43–48

    Article  Google Scholar 

  • Lopez-Rodas V, Marvá F, Rouco M, Costas E, Flores-Moya A (2008b) Adaptation of the chlorophycean Dictyosphaerium chlorelloides to the stressful acidic, mine metal-rich waters from Aguas Agrias Stream (SW Spain) as result of pre-selective mutations. Chemosphere 72:703–707

    Article  CAS  Google Scholar 

  • López-Rodas V, Flores-Moya A, Maneiro E, Perdigones N, Marvá F, García ME, Costas E (2007) Resistance to glyphosate in the cyanobacterium Microcystis aeruginosa as result of pre-selective mutations. Evol Ecol 21:535–547

    Article  Google Scholar 

  • López-Rodas V, Costas E, Maneiro E, Marvá F, Rouco M, Delgado A, Flores-Moya A (2009) Living in vulcan’s forge: algae adaptation to stressful geothermal ponds on Vulcano Island (S Italy) as result of pre-selective mutations. Phycol Res 57:111–117

    Article  Google Scholar 

  • López-Rodas V, Rouco M, Sánchez-Fortún S, Flores-Moya A, Costas E (2011) Genetic adaptation and acclimation of phytoplankton along a stress gradient in the extreme waters of the Agrio river–Caviahue lake (Argentina). J Phycol 47(5):1036–1043

    Article  Google Scholar 

  • Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511

    CAS  Google Scholar 

  • Luttrell WE, Giles CB (2007) Toxic tips: osmium tetroxide. J Chem Health Saf 14(5):40

    Article  Google Scholar 

  • Marvá F, López-Rodas V, Rouco M, Navarro MC, Toro FJ, Costas E, Flores-Moya A (2010) Adaptation of green microalgae to the herbicides simazine and diquat as result of pre-selective mutations. Aquat Toxicol 96(2):130–134

    Article  Google Scholar 

  • Poirier A, Gariepy C (2005) Isotopic signature and impact of car catalysts on the anthropogenic osmium budget. Environ Sci Technol 39:4431–4434

    Article  CAS  Google Scholar 

  • Pomati F, Nizzetto L (2013) Assessing triclosan-induced ecological and trans-generational effects in natural phytoplankton communities: a trait-based field method. Ecotoxicology. doi:10.1007/s10646-013-1068-7

    Google Scholar 

  • Rauch S, Hemond H, Barbante C, Owari M, Morrison GM, Peucker-Ehrenbrink B, Wass U (2005) Importance of automobile exhaust catalyst emissions for the deposition of platinum, palladium, and rhodium in the Northern Hemisphere. Environ Sci Technol 39:8156–8162

    Article  CAS  Google Scholar 

  • Romero J, López-Rodas V, Costas E (2012) Estimating the capability of microalgae to physiological acclimatization and genetic adaptation to petroleum and diesel oil contamination. Aquat Toxicol 124:227–237

    Article  Google Scholar 

  • Sager R (1954) Mendelian and non-Mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 40(5):356–363

    Article  CAS  Google Scholar 

  • Sager R (1962) Streptomycin as a mutagen for nonchromosomal genes. Proc Natl Acad Sci USA 48(12):2018–2026

    Article  CAS  Google Scholar 

  • Sager R, Burton WG, Roberts JR, Myers PA (1977) A site-specific single-strand endonuclease from the eukaryote Chlamydomonas. Proc Natl Acad Sci USA 74(7):2687–2691

    Article  Google Scholar 

  • Sharma M, Wasserburg GJ (1997) Osmium in the rivers. Geochim Cosmochim Acta 61(24):5411–5416

    Article  CAS  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. Routledge, London, pp 41–111

    Google Scholar 

  • Skulberg OM, Carmichael WW, Codd GA, Skulberg R (1993) Taxonomy of toxic cyanophyceae (Cyanobacteria). In: Falconer IR (ed) Algal toxins in seafood and drinking water. Academic Press, London, pp 145–164

    Chapter  Google Scholar 

  • Smith IC, Carson BL, Ferguson TL (1974) Osmium: an appraisal of environmental exposure. Environ Health Perspect 8:201–213

    Article  CAS  Google Scholar 

  • Sniegowski PD (2005) Linking mutation to adaptation: overcoming stress at the spa. New Phytol 166:360–362

    Article  Google Scholar 

  • Sniegowski PD, Lenski RE (1995) Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Annu Rev Ecol Evol Syst 26:553–578

    Article  Google Scholar 

  • Spiess EB (1989) Genes in populations, 2nd edn. Wiley, New York

    Google Scholar 

  • Wedepohl KH (1995) The composition of the continental crust. Geochim Cosmochim Acta 59(7):1217–1232

    Article  CAS  Google Scholar 

  • Westbroek P, van Hinte JE, Brummer GJ, Veldhuis M, Brownlee C, Green J, Harris R, Heimdal BR (1994) Emiliania huxleyi as a key to biosphere–geosphere interactions. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Systematics association special, vol 5. Clarendon Press, Oxford, pp 321–334

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Spanish Secretaría de Estado de Investigación, Desarrollo e Innovación (Grant CTM 2012-34757). We thank Eva Salgado for technical support.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Genetica, Facultad de Veterinaria, Univerdidad Complutense de Madrid, Av. Puerta de Hierro s/n 28040, Madrid, Spain

    Camino García-Balboa, Beatriz Baselga-Cervera & Eduardo Costas

  2. Centro de Investigación Marina de Santa Pola (CIMAR), Universidad de Alicante - Ayuntamiento de Santa Pola, 03130, Santa Pola, Alicante, Spain

    Fernando Marvá

Authors
  1. Fernando Marvá
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camino García-Balboa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beatriz Baselga-Cervera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eduardo Costas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo Costas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marvá, F., García-Balboa, C., Baselga-Cervera, B. et al. Rapid adaptation of some phytoplankton species to osmium as a result of spontaneous mutations. Ecotoxicology 23, 213–220 (2014). https://doi.org/10.1007/s10646-013-1164-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1164-8

Keywords

Search

Navigation