Skip to main content

Advertisement

Log in

A 4700-Year History of Cyanobacteria Toxin Production in a Shallow Subtropical Lake

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Cyanobacterial toxins or cyanotoxins are secondary metabolites produced by cyanobacteria and are found in water bodies around the world causing negative effects on aquatic ecosystems and human health. There are numerous environmental and biological triggers for toxin production, and the ecological role of most toxins is still being determined. Whereas cyanobacterial toxin occurrence appears to be expanding and monitoring efforts have increased in recent years, the history of toxin existence in lakes is poorly understood. Here, I report the history of the cyanotoxin, cylindrospermopsin (CYN), in sediments of hypereutrophic Lake Griffin, Florida, USA, from approximately 4700 years ago to present. The record includes three periods of toxin abundance: one associated with recent, European settlement in the watershed, and the other two during the middle to late Holocene, prior to human impacts on the lake. Each period corresponds to changes in different paleolimnological measurements suggesting drivers of CYN production have varied through time. This CYN record demonstrates the use of sediment toxin concentrations as a tool to reconstruct historic cyanobacterial toxin occurrence and shows that toxin production can occur independent of anthropogenic stressors.

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.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Berry JP, Lind O. 2010. First evidence of “paralytic shellfish toxin” and cylindrospermopsin in a Mexican freshwater system, Lago Catemaco, and apparent bioaccumulation of the toxins in “tegogolo” snales (Pomacea patula catemacensis). Toxicon 55:930–8.

    Article  CAS  PubMed  Google Scholar 

  • Brenner M, Whitmore TJ, Lasi MA, Cable JE, Cable PH, Schelske CL. 1999. A multi-proxy trophic state reconstruction for shallow Orange Lake, Florida, USA: possible influence of aquatic macrophytes on limnetic nutrient concentrations. J Paleolimnol 22:205–21.

    Article  Google Scholar 

  • de la Cruz AA, Hiskia A, Kaloudis T, Chernoff N, Hill D, Antoniou MG, He X, Loftin K, O’shea K, Zhao C, Pelaez M, Han C, Lynch TJ, Dionysiou DD. 2013. A review of cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ Sci Process Impacts 15:1979–2003.

    Article  PubMed  Google Scholar 

  • Dolman AM, Rucker J, Pick FR, Fastner J, Rohrlack T, Mischke U, Wiedner C. 2012. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLOS One . doi:10.1371/journal.pone.0038757.

    PubMed  PubMed Central  Google Scholar 

  • Donar C, Stoermer EF, Brenner M. 2009. The Holocene paleolimnology of Lake Apopka, Florida. Nova Hedwigia Beiheft 135:57–70.

    Google Scholar 

  • Dyble J, Tester PA, Litaker RW. 2006. Effects of light intensity on cylindrospermopsin production and release by the potentially invasive cyanobacterium Aphanizomenon ovalisporum under temperature and light gradients. Afr J Mar Sci 28:209–312.

    Article  Google Scholar 

  • Efting AA, Snow DD, Fritz SC. 2011. Cyanobacteria and microcystin in the Nebraska (USA) Sand Hills Lakes before and after modern agriculture. J Paleolimnol 46:17–27.

    Article  Google Scholar 

  • Environmental Protection Agency. 2014. Method 6010B: inductively coupled plasma-atomic emission spectrometry. http://www2.epa.gov/region8/method-6010b-inductively-coupled-plasma-atomic-emission-spectrometry.

  • Filley TR, Freeman KH, Bianchi TS, Baskaran M, Colarusso LA, Hatcher PG. 2001. An isotopic biogeochemical assessment of shifts in organic matter input to Holocene sediments from Mud Lake, Florida. Org Geochem 32:1153–67.

    Article  CAS  Google Scholar 

  • Fisher MM, Brenner M, Reddy KR. 1992. A simple, inexpensive piston corer for collecting undisturbed sediment/water interface profiles. J Paleolimnol 7:157–61.

    Article  Google Scholar 

  • Frost JR, Philps EJ, Fulton RSIII, Schelske CL, Kenney W, Cichra M. 2008. Temporal trends of trophic state variables in a shallow hypereutrophic subtropical lake, Lake Griffin, Florida, USA. Arch Hydrobiol 172:263–71.

    Article  CAS  Google Scholar 

  • Griffiths DL, Saker ML. 2003. The Palm Island mystery disease 20 years on: a review of research on the cyanotoxin cylindrospermopsin. Environ Toxicol 18:79–83.

    Article  Google Scholar 

  • Grimm EC, Jacobson GL Jr, Watts WA, Hansen BCS, Maasch KA. 1993. A 50,000-year record of climate oscillations from Florida and its temporal correlation with the Heinrich Events. Science 261:198–200.

    Article  CAS  PubMed  Google Scholar 

  • Gugger M, Molica R, Berre BL, Dufour P, Bernard C, Humbert JF. 2005. Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) Isolated from four continents. Appl Environ Microbiol 17:1097–100.

    Article  Google Scholar 

  • Håkanson L, Jansson M. 1983. Principles of lake sedimentology. New York: Springer.

    Book  Google Scholar 

  • Heussner AH, Mazija L, Fastner J, Dietrich DR. 2012. Toxin content and cytotoxicity of algal dietary supplements. Toxicol Appl Pharmacol 265:263–71.

    Article  CAS  PubMed  Google Scholar 

  • Holland A, Kinnear S. 2013. Interpreting the possible ecological role(s) of cyanotoxins: compounds for competitive advantage and/or physiological aide? Mar Drugs 11:2239–58.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaczorowska A, Kornijow R. 2012. Paleoecological evidence for changes over the past 200 years in chironomid communities of a shallow lake exposed to cyanobacterial toxins. Aquat Ecol 46:465–73.

    Article  Google Scholar 

  • Kaplan A, Harel M, Kaplan-Levy RN, Hadas O, Sukenik A, Dittmann E. 2012. The languages spoken in the water body (or biological role of cyanobacterial toxins). Front Microbiol 3:1–11.

    Article  Google Scholar 

  • Kinnear S. 2010. Cylindrospermopsin: a decade of progress on bioaccumulation research. Mar Drugs 8:542–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klitzke S, Apelt S, Weiler C, Fastner J, Chorus I. 2012. Retention and degradation of the cyanobacterial toxin cylindrospermopsin in sediments—the role of sediment preconditioning and DOM composition. Water Res 46:1549–55.

    Article  CAS  PubMed  Google Scholar 

  • Leavitt PR, Hodgson DA. 2001. Tracking environmental change using lake sediments, terrestrial, algal, and siliceous indicators, Vol. 3Dordrecht: Kluwer. pp 295–325.

    Book  Google Scholar 

  • Lindsay J, Metcalf JS, Codd GA. 2006. Protection against the toxicity of microcystin-LR and cylindrospermopsin in Artemia salina and Daphnia spp. By pre-treatment with cyanobacterial lipopolysaccharide (LPS). Toxicon 48:995–1001.

    Article  CAS  PubMed  Google Scholar 

  • McGregor GB, Sendall BC, Hunt LT, Eaglesham GK. 2011. Report of cyanotoxins cylindrospermopsin and deoxy-cylindrospermopsin from Raphidiopsis mediterranea Skuja (Cyanobacteria/Nostocles). Harmful Algae 10:402–10.

    Article  CAS  Google Scholar 

  • Meyers PA, Teranes JL. 2001. Tracking environmental change using lake sediments, terrestrial, algal, and siliceous indicators, Vol. 2Dordrecht: Kluwer. pp 239–69.

    Book  Google Scholar 

  • Norris RL, Eaglesham GK, Pierens G, Shaw GR, Smith MJ, Chiswell RK, Seawright AA, Moore MR. 1999. Deoxycylindrospermopsin, an analog of cylindrospermopsin from Cylindrospermopsis raciborskii. Environ Toxicol 14:163–5.

    Article  CAS  Google Scholar 

  • Orr PT, Rasmussen JP, Burford MA, Eaglesham GK, Lennox SM. 2010. Evaluation of quantitative real-time PCR to characterize spatial and temporal variations in cyanobacteria, Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju and cylindrospermopsin concentrations in three subtropical Australian reserovoirs. Harmful Algae 9:243–54.

    Article  CAS  Google Scholar 

  • Paerl HW, Paul VJ. 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–63.

    Article  CAS  PubMed  Google Scholar 

  • Pawlik-Skowronska B, Kornijow R, Pirszel J. 2010. Sedimentary imprint of cyanobacterial blooms—a new tool for insight into recent history of lakes. Pol J Ecol 58:663–70.

    CAS  Google Scholar 

  • Romero-Oliva CS, Contardo-Jara V, Block T, Phlugmacher S. 2014. Accumulation of microcystin congeners in different aquatic plants and crops—a case study from lake Amatitlan, Guatemala. Ecotoxicol Environ Saf 102:121–8.

    Article  CAS  PubMed  Google Scholar 

  • Rzymski P, Poniedzialek B. 2014. In search of environmental role of cylindrospermopsin: a review of global distribution and ecology of its producers. Water Res 66:320–37.

    Article  CAS  PubMed  Google Scholar 

  • Saint John’s River Water Management District. 2015. http://www.sjrwmd.com/watershedfacts/factPages/20020381.html.

  • Saker ML, Griffiths DJ. 2000. Effects of temperature on growth and cylindrospermopsin content of seven isoletes of Cylindrospermopsis reciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia 39:349–54.

    Article  Google Scholar 

  • Saker ML, Neilan BA. 2001. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from northern Australia. Appl Environ Microbiol 67:1839–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • SAS. 2006. JMP Version 6.0.3. Cary: SAS Institute Inc.

    Google Scholar 

  • Scheffer M. 1998. Ecology of shallow lakes. London: Kluwer Academic Publishers.

    Google Scholar 

  • Schelske CL. 1998. Sediment and nutrient deposition in Lake Griffin, Spec. Pub. SJ98-SP13. St. Johns River Water Management District, Palatka. http://www.sjrwmd.com/technicalreports/pdfs/SP/SJ98-SP-13.

  • Stuiver M, Reimer PJ. 1993. Extended C14 database and revised CALIB radiocarbon calibration program. Radiocarbon 35:215–30.

    Google Scholar 

  • ter Braak CJF, Smilauer P. 2002. Canoco Reference manual and CanoDraw for Windows User’s guide: software for canonical community ordination version 4.5. Microcomputer Power. Ithaca.

  • Utkilen H, Gjolme N. 1995. Iron-stimulated toxin production in Mycrocystis aeruginosa. Appl Eviron Microbiol 61:797–800.

    CAS  Google Scholar 

  • Vasas G, Suranyi G, Bacsi I, M-Hamvas M, Mathe C, Gonda S, Borbely G. 2013. Alteration of cylindrospermopsin content of Aphanizomenon ovalisporum (Cyanobacteria, Nostocales) due to a step-down from combined nitrogen to dinitrogen. Adv Microbiol 3:557–64.

    Article  Google Scholar 

  • Waters MN, Piehler MF, Smoak JM, Bianchi TS. 2012. Algal community responses to shallow lake dystrophication. Can J Fish Aquat Sci 69:1433–43.

    Article  CAS  Google Scholar 

  • Wetzel RG. 2001. Limnology. San Diego: Elsevier.

    Google Scholar 

Download references

Acknowledgements

Funding for this research was provided by Valdosta State University through a Faculty Research Seed Grant to MNW. Chase Patrick, Sean Earley, Josh Boston, James Ragan, and Justin Wynn aided in fieldwork and lab analysis. Curtis Caufield (Abraxis LLC.) aided in toxin interpretation. MNW also thanks Mark Brenner, Claire Schelske, Antonio Rodriguez, Erik Jeppesen, and two anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. N. Waters.

Additional information

Author contributions

MN Waters conceived the study, performed the research, analyzed data, and wrote the paper.

Data: All data for this research will be available at http://www.valdosta.edu/colleges/arts-sciences/biology/faculty-staff/matthew-waters.php.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 69 kb)

Supplementary material 2 (DOCX 193 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Waters, M.N. A 4700-Year History of Cyanobacteria Toxin Production in a Shallow Subtropical Lake. Ecosystems 19, 426–436 (2016). https://doi.org/10.1007/s10021-015-9943-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-015-9943-0

Keywords

Navigation