Expression of the nitrogen stress response gene ntcA reveals nitrogen-sufficient Synechococcus populations in the oligotrophic northern Red Sea

Abstract

Determining the nitrogen (N) status of phytoplankton is important for understanding primary production and N cycling in marine ecosystems. We assayed transcript levels of the N regulatory gene ntcA to assess the physiological N status of Synechococcus populations exposed to different N regimes in the meso-to oligotrophic Gulf of Aqaba, Red Sea. Synechococcus populations were N sufficient even in low-N environments when the ratio of dissolved nitrogen to phosphorus indicated that overall phytoplankton biomass was constrained by N. Ammonium supported Synechococcus N requirements under most conditions, but during a massive spring bloom in April 2000 alternative N sources were utilized. Evidence from ntcA clone libraries indicates changes in the genotypic makeup of Synechococcus populations under different N regimes, suggesting that the Synechococcus genotypes present in N-poor waters were those adapted for life in these environments. Thus, the success of Synechococcus in the open oceans is likely to be at least partially due to the selection of genotypes suited to life under prevailing N conditions rather than to prolonged manifestation of the N stress response, mediated by ntcA, in less well-adapted genotypes.Low photosynthetic biomass, prevalent in vast oligotrophic expanses of the world's oceans, is often attributed to 1 Corresponding authors (anton.post@huji.ac.il, dlindell@mit.edu).

Decoupling of ammonium regulation and ntcA transcription in the diazotrophic marine cyanobacterium Trichodesmium sp. IMS101

“…The use of the glutamine synthetase inhibitor MSX indicated that metabolized (as opposed to ambient) ammonium suppressed the transcription of N genes in the Trichodesmium filaments, similar to our findings in marine Synechococcus (Lindell and Post, 2001;Lindell et al, 2005). This is consistent with the concept that a-oxoglutarate accumulates and acts as the NtcA activator molecule when ammonium supplies are limiting Tanigawa et al, 2002).…”

“…Uptake rates of ammonium often exceed rates of N 2 fixation (Mulholland et al, 2001). Although both organisms thrive in N-depleted environments, N assimilation is thus not as stringently controlled in Trichodesmium as was found in marine Synechococcus (Lindell and Post 2001;Lindell et al, 1998Lindell et al, , 2005. This led us to hypothesize that NtcA control over N assimilation may be principally different in the non-heterocystous filaments of Trichodesmium spp.…”

“…Surprisingly, ammonium did not repress the transcription of the N-regulatory gene ntcA, and its mRNA accumulated to high levels, even in the presence of 2-2000 mM ammonium. In Synechococcus WH7803, ntcA transcript levels dropped below detection when ammonium concentrations exceed 1 mM (Lindell and Post, 2001;Lindell et al, 2005).…”

“…Ammonium addition immediately downregulated nitrate assimilation and N 2 fixation. In the non-N 2 -fixing Synechococcus WH7803, ntcA transcription is below detection when ammonium concentrations exceed 1 mM, and transcript levels are upregulated in nitrate-grown cells and become maximal under N-deplete conditions (Lindell and Post 2001;Lindell et al, 1998Lindell et al, , 2005. It has been reported that ambient ammonium accumulates to B2 mM in N 2 -fixing ( ¼ N-deplete) cultures of Trichodesmium IMS101 (Mulholland et al, 2001), thus raising questions about the mechanisms of ammonium control over N assimilation and N 2 fixation in this organism.…”

“…Its gene product, NtcA, is a 24 kD DNA-binding protein that belongs to the cAMP receptor protein (CRP) family of transcriptional activators (VegaPalas et al, 1992;Flores and Herrero, 1994). Freshwater and marine unicellular, non-N 2 -fixing cyanobacteria show a clear, direct relationship between ntcA expression and low ammonium levels (Frias et al, 1994;Lee et al, 1999;Sauer et al, 1999;Lindell and Post, 2001;Lindell et al, 2005) Marine Synechococcus WH7803 expresses ntcA at basic levels when grown on ammonium. These levels increase to intermediate when exposed to alternative N sources and maximum transcript levels are attained under N starvation (Lindell and Post, 2001;Lindell et al, 2005).…”