Trichodesmium-derived dissolved organic matter is a source of nitrogen capable of supporting the growth of toxic red tide Karenia brevis

Re Sipler,Om Schofield,Da Bronk,Lr Mcguinness,Ca Heil,Rj Lauck,Lj Kerkhof,Gj Kirkpatrick,Sp Seitzinger

doi:10.3354/meps10258

Abstract

Dissolved organic nitrogen (DON) produced by the nitrogen-fixer Trichodesmium sp. has the potential to serve as a nitrogen source for the red tide dinoflagellate Karenia brevis. Dis- solved organic matter (DOM) from laboratory cultures of Trichodesmium sp. was isolated, concen- trated and then supplied as a nutrient source to K. brevis cells collected from the Gulf of Mexico. K. brevis abundance increased immediately after Trichodesmium sp. cellular exudate (TCE) addition, allowing the population to double within the first 24 h. There was rapid and complete utilization of the TCE DON as well as ~89% of the TCE dissolved organic phosphorus (DOP). Additionally, ter- minal restriction fragment length polymorphism (TRFLP) was used to assess the bacterial commu- nity response to the addition of TCE . The number of bacterial operational taxonomic units (OTUs) initially increased after the TCE DOM addition, but decreased as K. brevis reached its maximum abundance. Electrospray ionization mass spectrometry (ESI-MS) and Fourier transform ion cy- clotron resonance mass spectrometry (FT-ICR MS) were used to chemically characterize the DOM. Approximately 25% of compounds disappeared within the first 24 h, corresponding to the greatest increase in K. brevis abundance. Using FT-ICR MS, 391 DON and 219 DOP potentially bioavailable compounds were characterized. The bioavailable DON compounds were highly re- duced and 44% had molar ratios indicative of lipid or protein-like compounds. The changes in DON concentration and compound composition show that Tricho desmium sp. provides a sufficient source of nitrogen to directly or indirectly support K. brevis blooms.

Highlights

Blooms of the toxic red-tide dinoflagellate, Karenia brevis (Davis) Hansen and Moestrup (previously known as Gymnodinium breve (Davis) and Ptychodiscus brevis (Davis) Steidinger), occur frequently on the West Florida Shelf in the subtropical waters of the Gulf of Mexico (GOM)
The objectives of this study were 4-fold: (1) to investigate how Dissolved organic nitrogen (DON) produced by Trichodesmium affected the growth of Karenia brevis; (2) to determine what proportion of DON produced by Trichodesmium was bioavailable; (3) to chemically characterize the Dissolved organic matter (DOM) produced by Trichodesmium and consumed by the K. brevis-dominated microbial community; and (4) to determine whether bacterial community composition changes with K. brevis growth
Karenia brevis abundance doubled in the presence of Trichodesmium-derived DOM, confirming that K. brevis is able to directly or indirectly use Trichodesmium sp. cellular exudate (TCE) DON as a nutrient source but that it can grow rapidly on DON substrates

Summary

Introduction

Blooms of the toxic red-tide dinoflagellate, Karenia brevis (Davis) Hansen and Moestrup (previously known as Gymnodinium breve (Davis) and Ptychodiscus brevis (Davis) Steidinger), occur frequently on the West Florida Shelf in the subtropical waters of the Gulf of Mexico (GOM). K. brevis blooms occur annually and account for a significant proportion of the annual carbon fixation within the GOM (Vargo et al 1987). Non-bloom concentrations of K. brevis are ubiquitous throughout the eastern. Blooms of K. brevis (>1000 cells l−1) have been observed in 28 of the 42 years between 1957 and 1998 (Walsh & Steidinger 2001). The frequency and cause of K. brevis blooms is important because this species produces a potent neurotoxin, brevetoxin. Economic losses associated with K. brevis blooms can reach $6.5 million per month to the tourism industry alone (2007 US dollars; Larkin & Adams 2007)

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