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

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. Dissolved organic matter (DOM) from laboratory cultures of Trichodesmium sp. was isolated, concentrated 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, terminal restriction fragment length polymorphism (TRFLP) was used to assess the bacterial community 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 cyclotron 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 reduced 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. KEY WORDS: Red tide · Trichodesmium · Karenia brevis · DON · FT-ICR MS · ESI-MSResale or republication not permitted without written consent of the publisher

Five decades of N2 fixation research in the North Atlantic Ocean

“…Recent advances in DOM characterization are currently starting to answer some of these questions. For example, Sipler et al (2013) have shown that Trichodesmium produces labile dissolved organic nitrogen compounds capable of triggering toxic microalgae blooms. Integrative approaches including stable isotope tracing experiments in combination with state-of-theart DOM characterization techniques hold great promise for new discoveries.…”

“…In principle, the transfer of fixed N 2 should be highly efficient because the product of this reaction is ammonium, which is readily available to photoautotrophic microbes. Trichodesmium also releases large amounts of fixed N 2 as labile dissolved organic nitrogen (Capone et al, 1994;Sipler et al, 2013), and the role of UCYN in providing these organic compounds could also be important (Benavides et al, 2013d). Modern high-resolution mass spectrometry techniques such as nano-scale secondary ion mass spectrometry (nanoSIMS) have recently been used to yield new insights into the efficiency of this transfer and the partitioning of fixed N 2 between planktonic groups in different trophic levels.…”

Biogeochemical and biological impacts of diazotroph blooms in a low-nutrient, low-chlorophyll ecosystem: synthesis from the VAHINE mesocosm experiment (New Caledonia)

“…These studies suggest a potential transfer of DDN from diazotrophic to non-diazotrophic phytoplankton. Ac-tual calculations of DDN transfer were first performed by Bronk et al (2004), Lenes and Heil (2010) and Sipler et al (2013), who demonstrated how the DDN released by Trichodesmium spp. affected the bloom dynamics of the toxic dinoflagellate Karenia brevis in the Gulf of Mexico.…”

Positive feedbacks between bottom-up and top-down controls promote the formation and toxicity of ecosystem disruptive algal blooms: A modeling study

“…Osmotrophic utilization of DON as an N source is widespread in marine algae and is particularly prevalent in many low-nutrient, Kadapted species, including Karenia brevis (Sipler et al, 2013) and many other HAB/EDAB species (Bronk et al, 2007;Glibert and Legrand, 2006;Burkholder et al, 2008). Biologically labile DON molecules, such as urea and amino acids, are often an important component of grazer-mediated regenerated N so biological utilization of DON can be important source of recycled N to phytoplankton.…”

“…Biologically labile DON molecules, such as urea and amino acids, are often an important component of grazer-mediated regenerated N so biological utilization of DON can be important source of recycled N to phytoplankton. Furthermore, there is evidence that the release of DON by Trichodesmium or other diazotrophic cyanobacteria can promote the growth of K. brevis blooms (Sipler et al, 2013). However, such increase in fixed-N supply from N 2 -fixation can drive these systems into P-limitation of algal growth rate, which also increases cellular brevetoxin:C ratios (Hardison et al, 2013).…”