SpringerLink
Log in

Synergistic effects of temperature and nutrients on growth and saxitoxin content of the cyanobacterium Raphidiopsis raciborskii

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

Abstract

The eutrophication of aquatic ecosystems combined with the rise in global temperature has favored the frequency and intensity of harmful cyanobacterial blooms. Although the importance of temperature and nutrients on biomass, biovolume, and toxin production by the cyanobacterium Raphidiopsis raciborskii (Woloszynska) Aguliera et al. has been studied, the synergistic effects of these factors have not received due attention. We investigated the individual and combined effects of high nitrogen, phosphorus, and temperature on the biomass, cell volume, and saxitoxin (STXs) content of R. raciborskii. The cyanobacterium was exposed to high nitrogen (N +) and phosphorus (P +) concentrations at two temperatures, 24 and 30 °C, for 8 days. Raphidiopsis raciborskii biomass was highest under conditions P + and N + at 30 °C. The highest growth rates were observed at 24 °C in cultures exposed to the N + conditions. The changes in cell volume induced by nutrients, temperatures, and incubation time were interactively significant. Cultures incubated at 30 °C had significantly reduced cell volume regardless of the nitrogen condition. Condition P + stimulated higher STXs production by the cyanobacterium at 24 °C compared to the other experimental conditions tested. Linear regression models indicated that P + had a strong relationship with biomass and saxitoxins production at the investigated temperatures—24 and 30 °C. Our results suggest a synergy of nutrient and temperature variation promotes the proliferation of R. raciborskii, supporting the existing hypothesis on the geographic expansion of this species. However, it is not yet clear whether elevated temperatures could reduce the toxicity of STX-producing strains.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

  • Aguilera A, Aubriot L, Echenique RO, Donadelli JL, Salerno GL (2019) Raphidiopsis mediterranea (Nostocales) exhibits a flexible growth strategy under light and nutrient fluctuations in contrast to Planktothrix agardhii (Oscillatoriales). Hydrobiologia 839:145–215

    Article  CAS  Google Scholar 

  • Antunes JT, Leão PN, Vasconcelos VM (2012) Influence of biotic and abiotic factors on the allelopathic activity of the cyanobacterium Cylindrospermopsis raciborskii strain LEGE 99043. Microb Ecol 64:584–592

    Article  CAS  PubMed  Google Scholar 

  • Antunes JT, Leão PN, Vasconcelos VM (2015) Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front Microbiol 6:473

    Article  PubMed  PubMed Central  Google Scholar 

  • Babica P, Kohoutek J, Bláha L, Adamovský O, Maršálek B (2006) Evaluation of extraction approaches linked to ELISA and HPLC for analyses of microcystin-LR, -RR and-YR in freshwater sediments with different organic material contents. Anal Bioanal Chem 385:1545–1551

    Article  CAS  PubMed  Google Scholar 

  • Bittencourt-Oliveira MC, Chia MA, Camargo-Santos D, Dias CTS (2016) The effect of saxitoxin and non-saxitoxin extracts of Cylindrospermopsis raciborskii (cyanobacteria) on cyanobacteria and green microalgae. J Appl Phycol 28:241–250

    Article  CAS  Google Scholar 

  • Bláhová L, Oravec M, Maršálek B, Šejnohová L, Šimek Z, Bláha L (2009) The first occurrence of the cyanobacterial alkaloid toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC/MS methods. Toxicon 53:519–524

    Article  PubMed  Google Scholar 

  • Bonilla S, González-Piana M, Soares MCS, Huszar VLM, Becker V, Somma A, Aubriot L (2016) The success of the cyanobacterium Cylindrospermopsis raciborskii in freshwaters is enhanced by the combined effects of light intensity and temperature. J Limnol 75:606–617

    Google Scholar 

  • Brandenburg K, Siebers L, Keuskamp J, Jephcott TG, Van de Waal DB (2020) Effects of nutrient limitation on the synthesis of N-rich phytoplankton toxins: a meta-analysis. Toxins 12:221

    Article  CAS  PubMed Central  Google Scholar 

  • Briand E, Bormans M, Quiblier CMJ, Salençon MJ, Humbert JF (2013) Evidence of the cost of the production of microcystins by Microcystis aeruginosa under differing light and nitrate environmental conditions. PLoS ONE 7:e29981

    Article  Google Scholar 

  • Buratti FM, Manganelli M, Vichi S, Stefanelli M, Scardala S, Testai E, Funari E (2017) Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch Toxicol 91:1049–1130

    Article  CAS  PubMed  Google Scholar 

  • Burford MA, Davis TW, Orr PT, Sinha R, Willis A, Neilan BA (2014) Nutrient-related changes in the toxicity of field blooms of the cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microb Ecol 89:135–148

    Article  CAS  Google Scholar 

  • Burford MA, Beardall J, Willis A, Oorr PT, Magalhães VF, Rangel LM, Neilan BA (2016) Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 54:44–53

    Article  PubMed  Google Scholar 

  • Burford MA, Willis A, Chuang A, Man X, Orr PT (2018) Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii. J Oceanol Limnol 36:1032–1039

    Article  CAS  Google Scholar 

  • Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407

    Article  CAS  PubMed  Google Scholar 

  • Castro D, Vera D, Lagos N, Garcıa C, Vásquez M (2004) The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon 44:483–489

    Article  CAS  PubMed  Google Scholar 

  • Casero MC, Ballot A, Agha R, Quesada A, Cirés S (2014) Characterization of saxitoxin production and release and phylogeny of sxt genes in paralytic shellfish poisoning toxin-producing Aphanizomenon gracile. Harmful Algae 37:28–37

    Article  CAS  Google Scholar 

  • Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Webster NS (2019) Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17:569–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chislock MF, Sharp KL, Wilson AE (2014) Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res 49:207–214

    Article  CAS  PubMed  Google Scholar 

  • Chiu YHM, Henn BC, Hsu H-HL, Pendo MP, Coull BA, Austin C, Cagna G, Fedrighi C, Placidi D, Robert DRS, Wright RO, Lucchini RG, Arora M (2017) Sex differences in sensitivity to prenatal and early childhood manganese exposure on neuromotor function in adolescents. Environ Res 159:458–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cirés S, Delgado A, González-Pleiter M, Quesada A (2017) Temperature influences the production and transport of saxitoxin and the expression of sxt genes in the cyanobacterium Aphanizomenon gracile. Toxins 9:322

    Article  PubMed Central  Google Scholar 

  • De la Cruz AA, Chernoff N, Sinclair JL, Hill D, Diggs DL, Lynch AT (2020) Introduction to cyanobacteria and cyanotoxins. In: Hiskia AE, Trinatis TM, Antoniou MG, Kaloudis T, Dioysiou DD (eds) Water treatment for purification from cyanobacteria and cyanotoxins. Wiley, NY, pp 1–35

    Google Scholar 

  • Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci 106:12788–12793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Descy JP, Darchambeau F, Lambert T, Stoyneva-Gaertner MP, Bouillon S, Borges AV (2017) Phytoplankton dynamics in the Congo River. Freshw Biol 62:87–101

    Article  CAS  Google Scholar 

  • Dias E, Pereira P, Franca S (2002) Production of paralytic shellfish toxins by Aphanizomenon sp. LMECYA 31 (cyanobacteria). J Phycol 38:705–712

  • Edwards KF, Thomas MK, Klausmeier CA, Litchman E (2012) Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol Oceanogr 57:554–566

    Article  Google Scholar 

  • Galvanese FE, Padial AA, Aubriot L (2019) Acclimation at high temperatures increases the ability of Raphidiopsis raciborskii (cyanobacteria) to withstand phosphate deficiency and reveals distinct strain responses. Eur J Phycol 54:359–368

    Article  CAS  Google Scholar 

  • Gobler CJ, Burkholder JM, Davis TW, Harke MJ, Johengen T, Stow CA, Van de Waal DB (2016) The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97

    Article  CAS  PubMed  Google Scholar 

  • Gorham PR, McLachlan J, Hammer UT, Kim WK (1964) Isolation and culture of toxic strains of Anabaena flos-aquae (Lyngb.) de Bréb. Int Ver Theor Angew Limnol Verh 15:796–804

  • Heffer P, Prud'homme M (2016) Fertilizer outlook 2016–2020. 84th IFA Annual Conference, Russia.

  • Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • IPCC - Climate Change (2012) The physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Agenda 996. Cambridge University Press, Cambridge

  • Irwin N, Clarke GC, Green BD, Greer B, Harriott P, Gault VA, Flatt PR (2006) Evaluation of the antidiabetic activity of DPP IV resistant N-terminally modified versus mid-chain acylated analogues of glucose-dependent insulinotropic polypeptide. Biochem Pharmacol 72:719–728

    Article  CAS  PubMed  Google Scholar 

  • Jiang Z, Du P, Liu J, Chen Y, Zhu Y, Shou L, Chen J (2019) Phytoplankton biomass and size structure in **angshan Bay, China: current state and historical comparison under accelerated eutrophication and warming. Mar Pollut Bull 142:119–128

    Article  CAS  PubMed  Google Scholar 

  • Khan MN, Mohammad F (2014) Eutrophication: challenges and solutions. In: Ansari AA, Gill SS (eds) Eutrophication: causes, consequences and control, vol 2. Springer, Dordrecht, pp 1–15

    Google Scholar 

  • Kovács AW, Présing M, Vörös L (2016) Thermal dependent growth characteristics for Cylindrospermopsis raciborskii (Cyanoprokaryota) at different light availabilities: methodological considerations. Aquat Ecol 50:623–638

    Article  Google Scholar 

  • Lee KH, Jeong HJ, Lee K, Franks PJ, Seong KA, Lee SY, Kim KY (2019) Effects of warming and eutrophication on coastal phytoplankton production. Harmful Algae 81:106–118

    Article  PubMed  Google Scholar 

  • Lürling M, Van Oosterhout F, Faassen E (2017) Eutrophication and warming boost cyanobacterial biomass and microcystins. Toxins 9:64

    Article  PubMed Central  Google Scholar 

  • Lürling M, Van Oosterhout F, de Senerpont DL, Marinho MM (2018) Response of natural cyanobacteria and algae assemblages to a nutrient pulse and elevated temperature. Front Microbiol 9:1851

    Article  PubMed  PubMed Central  Google Scholar 

  • Mesquita MC, Lürling M, Dorr F, Pinto E, Marinho MM (2019) Combined effect of light and temperature on the production of saxitoxins in Cylindrospermopsis raciborskii strains. Toxins 11:38

    Article  CAS  PubMed Central  Google Scholar 

  • Mohamed ZA, Al-Shehri AM (2013) Assessment of cylindrospermopsin toxin in an arid Saudi lake containing dense cyanobacterial bloom. Environ Monit Assess 185:2157–2166

    Article  CAS  PubMed  Google Scholar 

  • Moisander PH, Cheshire LA, Braddy J, Calandrino ES, Hoffman M, Piehler MF, Paerl HW (2012) Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiol Ecol 79:800–811

    Article  CAS  PubMed  Google Scholar 

  • Mowe MAD, Mitrovic SM, Lim RP, Furey A, Yeo DCJ (2014) Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J Limnol 53:89–100

    Google Scholar 

  • Mowe MA, Porojan C, Abbas F, Mitrovic SM, Lim RP, Furey A, Yeo DC (2015) Rising temperatures may increase growth rates and microcystin production in tropical Microcystis species. Harmful Algae 50:88–98

    Article  CAS  Google Scholar 

  • Mullin C, Kirchhoff CJ, Wang G, Vlahos P (2020) Future projections of water temperature and thermal stratification in Connecticut reservoirs and possible implications for cyanobacteria. Water Resour Res 56:1–18

    Article  Google Scholar 

  • O’Neil JM, Davis TW, Burford MA, Glober CJ (2012) The rise of harmul cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334

    Article  Google Scholar 

  • O’Reilly CM, Sharma S, Gray DK, Hampton SE, Read JS, Rowley RJ, Zhang GA (2015) Rapid and highly variable warming of lake surface waters around the globe. Geophys Res Lett 42:773–781

  • Piccini C, Aubriot L, Fabre A, Amaral V, González-Piana M, Giani A, Bonilla S (2011) Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10:644–653

    Article  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed Aug 2021

  • Rangel LM, Ger KA, Silva LH, Soares MCS, Faassen EJ, Lürling M (2016) Toxicity overrides morphology on Cylindrospermopsis raciborskii grazing resistance to the calanoid copepod Eudiaptomus gracilis. Microb Ecol 71:835–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Recknagel F, Orr PT, Bartkow M, Swanepoel A, Cao H (2017) Early warning of limit-exceeding concentrations of cyanobacteria and cyanotoxins in drinking water reservoirs by inferential modelling. Harmful Algae 69:18–27

    Article  CAS  PubMed  Google Scholar 

  • Reynolds CS (2006) The ecology of phytoplankton (ecology, biodiversity and conservation). Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rzymski P, Poniedziałek B, Kokociński M, Jurczak T, Lipski DK, Wiktorowicz K (2014) Interspecific allelopathy in cyanobacteria: cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 35:1–8

    Article  CAS  Google Scholar 

  • Saker ML, Griffiths DJ (2000) The effect of temperature on growth and cylindrospermopsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia 39:349–354

    Article  Google Scholar 

  • Seymour B, Andreosso A, Seymour J (2015) Cardiovascular toxicity from marine envenomation. In: Ramachandra M, Thirumalaikoundusubramanian P (eds) The Heart and Toxins. Elsevier, Amsterdam pp 203–223.

  • Sha J, Li HXC, Lu Z, Zhang J, Zhong H, Zhang W, Yan B (2021) Harmful algal blooms and their eco-environmental indication. Chemosphere 274:129912

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Kate BN, Banerjee UC (2005) Bioactive compounds from cyanobacteria and microalgae: an overview. Crit Rev Biotechnol 25:73–95

    Article  CAS  PubMed  Google Scholar 

  • Soares MC, Lürling M, Huszar VLM (2013) Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycol Res 61:61–67

    Article  Google Scholar 

  • Sukenik A, Quesada A, Salmaso N (2015) Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers Conservat 24:89–908

    Article  Google Scholar 

  • Stucken K, John U, Cembella A, Soto-Liebe K, Vásquez M (2014) Impact of nitrogen sources on gene expression and toxin production in the diazotroph Cylindrospermopsis raciborskii CS-505 and non-diazotroph Raphidiopsis brookii D9. Toxins 6:1896–1915

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas SR, dos Santos PV, Bottino F, Calijuri MC (2020) Effect of nutrient concentration on growth and saxitoxin production of Raphidiopsis raciborskii (Cyanophyta) interacting with Monoraphidium contortum (Chlorophyceae). J Appl Phycol 32:421–430

  • Van de Waal DB, Smith VH, Declerck SAJ, Stam ECM, Elser JJ (2014) Stoichiometric regulation of phytoplankton toxins. Ecol Lett 17:736–742

    Article  PubMed  Google Scholar 

  • Vico P, Aubriot L, Martigani F, Rigamonti N, Bonilla S, Piccini C (2016) Influence of nitrogen availability on the expression of genes involved in the biosynthesis of saxitoxin and analogs in Cylindrospermopsis raciborskii. Harmful Algae 56:7–43

    Article  Google Scholar 

  • Vico P, Bonilla S, Cremella B, Aubriot L, Iriarte A, Piccini C (2020) Biogeography of the cyanobacterium Raphidiopsis (Cylindrospermopsis) raciborskii: integrating genomics, phylogenetic and toxicity data. Mol Phylogenet Evol 148:106824

    Article  PubMed  Google Scholar 

  • Vilar MCP, Molica RJR (2020) Changes in pH and dissolved inorganic carbon in water affect the growth, saxitoxins production and toxicity of the cyanobacterium Raphidiopsis raciborskii ITEP-A1. Harmful Algae 97:101870

    Article  CAS  PubMed  Google Scholar 

  • **ão M, Adams MPA, Willis A, Burford MK, O’Brien KR (2017) Variation within and between cyanobacterial species and strains affects competition: implications for phytoplankton modelling. Harmful Algae 69:38–47

  • Walls JT, Wyatt KH, Doll JC, Rubenstein EM, Rober AR (2018) Hot and toxic: temperature regulates microcystin release from cyanobacteria. Sci Total Environ 610:786–795

    Article  PubMed  Google Scholar 

  • Wetzel RG, Likens GE (2000) Limnological analyses. Springer, New York

    Book  Google Scholar 

  • Winder M, Reuter JE, Schladow G (2009) Lake warming favours small-sized planktonic diatoms. Proc Roy Soc Lond B 276:427–435

    Google Scholar 

  • Wood AM, Everroad RC, Wingard LM (2005) Measuring growth rates in microalgal cultures. In. Andersen RA (ed) Algal culturing techniques. Academic Press, NY pp 269–285.

  • Yang Y, Jiang Y, Li X, Li H, Chen Y, **e J, Li R (2017) Variations of growth and toxin yield in Cylindrospermopsis raciborskii under different phosphorus concentrations. Toxins 9:13

    Article  Google Scholar 

  • Yema L, Litchman E, de Tezanos PP (2016) The role of heterocytes in the physiology and ecology of bloom-forming harmful cyanobacteria. Harmful Algae 60:131–138

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank FINEP (Ministry of Science, Technology, and Innovation/Financier of Studies and Projects) CTHIDRO 01/2013 for funding. This research was financed in part by the FAPESQ (Foundation for Research Support of the State of Paraíba) and CNPq (National Council for Scientific and Technological Development), (process 88887.142333/2017-00) for the financing of this study. We also thank the PPGEC (Ecology and Conservation Pos-Graduation Program) of the State University of Paraíba and the Ecology Aquatic Laboratory team-UEPB for the support during the research time.

Author information

Authors and Affiliations

  1. Departamento de Biologia/Programa de Pós-Graduação em Ecologia e Conservação e Programa de Pós-Graduação em Ciência e Tecnologia Ambiental, Universidade Estadual da Paraíba, Rua Baraúnas nº. 351 - Complexo Três Marias, Prédio de Biologia, Térreo - sala 10, Universitário, Paraíba, CEP 58.429-500, Campina Grande, Brazil

    Ranielle Daiana dos Santos Silva, Vanessa Virginia Barbosa, Juliana dos Santos Severiano & José Etham de Lucena Barbosa

  2. Department of Botany, Ahmabu Bello University, Zaria, Nigeria

    Mathias Ahii Chia

Authors
  1. Ranielle Daiana dos Santos Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mathias Ahii Chia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa Virginia Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juliana dos Santos Severiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Etham de Lucena Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RDSS, MAC, JSS, and JELB helped in conceptualization; RDSS contributed to data curation and methodology; RDSS, MAC, and JSS formally analyzed the study and wrote the original draft; RDSS, MAC, JSS, and VVB investigated; JELB acquired the funding, administrated the project, and contributed to resources; JSS and JELB supervised the project; RDSS, MAC, JSS, and JELB validated the study; RDSS, MAC, JSS, VVB, and JELB helped in visualization and writing—review and editing.

Corresponding author

Correspondence to Ranielle Daiana dos Santos Silva.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

dos Santos Silva, R.D., Chia, M.A., Barbosa, V.V. et al. Synergistic effects of temperature and nutrients on growth and saxitoxin content of the cyanobacterium Raphidiopsis raciborskii. J Appl Phycol 34, 941–952 (2022). https://doi.org/10.1007/s10811-021-02678-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02678-8

Keywords

Search

Navigation