Nitrogenous nutrients promote the growth and toxicity of Dinophysis acuminata during estuarine bloom events

Theresa K Hattenrath-Lehmann; Maria A Marcoval; Heidi Mittlesdorf; Jennifer A Goleski; Zhihong Wang; Bennie Haynes; Steve L Morton; Christopher J Gobler

doi:10.1371/journal.pone.0124148

Nitrogenous nutrients promote the growth and toxicity of Dinophysis acuminata during estuarine bloom events

PLoS One. 2015 Apr 20;10(4):e0124148. doi: 10.1371/journal.pone.0124148. eCollection 2015.

Authors

Theresa K Hattenrath-Lehmann¹, Maria A Marcoval², Heidi Mittlesdorf¹, Jennifer A Goleski¹, Zhihong Wang³, Bennie Haynes³, Steve L Morton³, Christopher J Gobler¹

Affiliations

¹ Stony Brook University, School of Marine and Atmospheric Sciences, Southampton, New York, United States of America.
² Stony Brook University, School of Marine and Atmospheric Sciences, Southampton, New York, United States of America; Estación Costera "J.J. Nágera", Departamento de Ciencias Marinas (FCEyN), Universidad Nacional de Mar del Plata, Mar del Plata; & Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.
³ NOAA-National Ocean Service, Marine Biotoxins Program, Charleston, South Carolina, United States of America.

Abstract

Diarrhetic Shellfish Poisoning (DSP) is a globally significant human health syndrome most commonly caused by dinoflagellates within the genus Dinophysis. While blooms of harmful algae have frequently been linked to excessive nutrient loading, Dinophysis is a mixotrophic alga whose growth is typically associated with prey availability. Consequently, field studies of Dinophysis and nutrients have been rare. Here, the temporal dynamics of Dinophysis acuminata blooms, DSP toxins, and nutrients (nitrate, ammonium, phosphate, silicate, organic compounds) were examined over four years within two New York estuaries (Meetinghouse Creek and Northport Bay). Further, changes in the abundance and toxicity of D. acuminata were assessed during a series of nutrient amendment experiments performed over a three year period. During the study, Dinophysis acuminata blooms exceeding one million cells L-1 were observed in both estuaries. Highly significant (p<0.001) forward stepwise multivariate regression models of ecosystem observations demonstrated that D. acuminata abundances were positively dependent on multiple environmental parameters including ammonium (p = 0.007) while cellular toxin content was positively dependent on ammonium (p = 0.002) but negatively dependent on nitrate (p<0.001). Nitrogen- (N) and phosphorus- (P) containing inorganic and organic nutrients significantly enhanced D. acuminata densities in nearly all (13 of 14) experiments performed. Ammonium significantly increased cell densities in 10 of 11 experiments, while glutamine significantly enhanced cellular DSP content in 4 of 5 experiments examining this compound. Nutrients may have directly or indirectly enhanced D. acuminata abundances as densities of this mixotroph during experiments were significantly correlated with multiple members of the planktonic community (phytoflagellates and Mesodinium). Collectively, this study demonstrates that nutrient loading and more specifically N-loading promotes the growth and toxicity of D. acuminata populations in coastal zones.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Dinoflagellida / growth & development*
Dinoflagellida / metabolism*
Ecosystem*
Estuaries*
Food*
Humans
Marine Toxins / chemistry*
Nitrogen / metabolism*

Substances

Marine Toxins
Nitrogen

Grants and funding

The authors gratefully acknowledge support from the New York State Department of Environmental Conservation, New York Sea Grant (R/CMB-38-NYCT) and NOAA’s Monitoring and Event Response to Harmful Algal Blooms (MERHAB) program (NA11NOS4780027). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.