Putting the N in dinoflagellates
Steve Dagenais-Bellefeuille and David Morse
Front Microbiol. 2013; 4: 369.
Published online 2013 Dec 4.
Creative Commons license.
There are so many “Wow”‘s in this review that I’m just going to quote like a demon and be thankful that the article is under a Creative Commons license from the cited authors.
Their story begins when dino’s radiate about 400 million years ago after the late Devonian extinction.
Some choice quote and a little commentary..
In conditions of N-stress dinoflagellate cells either die or modify their metabolism and trophic behavior to ensure their survival.
The original motive for the bloom.
The marine N cycle is probably the most complex of the biogeochemical cycles, as it involves various chemical forms and multiple transformations that connect all marine organisms.
About 94% of the oceanic N inventory exists as biologically unavailable dissolved nitrogen gas (N2; Gruber, 2008). This gas can be made bioavailable through N2-fixation, a process carried out by photoautotrophic prokaryotes, mainly cyanobacteria, using iron-dependent nitrogenases to catalyze reduction of N2 to NH+4.
Didn’t know that much N was dissolved gas.
Didn’t know nitrogen fixation was iron-dependent.
Generally, when growing in presence of various different N compounds, dinoflagellates (as well as plants and algae) prefer to take up NH+4. However, there is a concentration threshold above which NH+4 becomes toxic to the cells[…]
Another tendency in dinoflagellates is inhibition of NO−3 uptake when in the presence of NH+4.
Curiously, different blooming populations of dinoflagellates were found to have high uptake rates for urea and/or amino acids, and these rates were always higher than the rates for NO−3 uptake (Kudela and Cochlan, 2000; Fan et al., 2003; Collos et al., 2007).
So there is some basis for the theory that amino acids “cause” or are related to HAB’s
Dinoflagellates often display a diurnal vertical migration (DVM) in the water column and, because NO−3 concentrations increase with depth, dark NO−3 uptake was first described as a means to sustain uninterrupted growth by meeting their N requirements under conditions where the cells cannot photosynthesize (Harrison, 1976). It was further suggested that the DVM of dinoflagellates gave them a competitive advantage for N uptake over the non-motile diatoms (Harrison, 1976; Smayda, 1997).
We will finish with a model proposed by Jeong et al. (2010) where mixotrophy explains the outbreak and persistence of HABs in aquatic ecosystems limited in inorganic nutrients.
Spectacularly, some pallium and peduncle feeders are able to ingest prey up to 10 times their size (Jacobson, 1987). As for prey types, MTDs and HTDs feed on a wide array of taxa. They were shown to ingest cryptophytes, haptophytes, chlorophytes, prasiophytes, raphidophytes, diatoms, heterotrophic nanoflagellates, ciliates, and other dinoflagellates (Jacobson and Anderson, 1986; Hansen, 1991; Bockstahler and Coats, 1993b; Strom and Buskey, 1993; Nakamura et al., 1995; Tillmann, 2004; Jeong et al., 2005a, 2008; Menden-Deuer et al., 2005; Adolf et al., 2007; Berge et al., 2008). However, while some HTDs can feed on blood, flesh, eggs and early naupliar stages and adults forms of metazoans, no MTDs have been shown to do so (Miller and Belas, 2003; Parrow and Burkholder, 2004; Jeong et al., 2007).
It was long believed that bacteria were too small to be ingested by dinoflagellates. In the last few years, however, fluorescence and transmission electron microscopy observations revealed that multiple HTDs and MTDs were able to feed on heterotrophic bacteria and cyanobacteria (Jeong et al., 2005a, 2008; Seong et al., 2006; Glibert et al., 2009). In particular, feeding on the N2-fixing Synechococcus spp. was seen in 18 species reported to form HABs (Jeong et al., 2005a; Seong et al., 2006; Glibert et al., 2009). Generally, when prey concentration was high (106 cells/ml), the ingestion rates increased with increasing size of the dinoflagellate predators (Jeong et al., 2005a). Moreover, ingestion rates of Synechococcus were comparable to those observed in heterotrophic nanoflagellates (Seong et al., 2006). A mixture of P. mininum and P. donghaiense was able to remove up to 98% of the Synechococcus population within 1 h, showing that grazing by these species on bacteria could be very substantial (Jeong et al., 2005a). Thus, bacterivory in dinoflagellates was suggested to be a cause of HABs outbreaks and persistence in nutrient-limited waters (Glibert et al., 2009; Jeong et al., 2010). A model was further proposed where MTDs would supply their N requirement by ingesting cyanobacteria, while meeting their P requirement by ingesting heterotrophic bacteria, which are reported to generally have a high P:N ratio (Jeong et al., 2010). This model as yet to be tested in the environment.
Symbiosis with diazotrophs is an example of a strategy that is shared by some diatom and dinoflagellate species. The diatom genera Hemiaulus and Rhizosolenia both form endosymbiotic associations with the cyanobacteria Richelia intracellularis (Venrick, 1974; Carpenter et al., 1999). Both the hosts and the symbionts were observed to bloom together in the oligotrophic waters of the North Pacific Central Gyre and South West Atlantic Ocean. N2-fixation by Richelia introduced an amount of “new N” to the ecosystems that could even exceed the N2 fixed by non-blooming Trichodesmium. Carpenter et al. (1999) suggested that the silicate- and iron-enriched water of the Amazon River could have been factors in initiating and sustaining the blooms in the SW Atlantic Ocean. Silicate is required for the formation of the diatom frustule, while iron is necessary for the action of the diazotroph nitrogenases.
While it was not directly shown that Symbiodinium formed symbiotic association with cyanobacteria, the coral host was found to do so. In fact, whole communities of beneficial bacteria including N2-fixers and chitin decomposers were identified in all coral structures, including the surface mucous layer, tissue layers and the skeleton (Lesser et al., 2004; Rosenberg et al., 2007). Interestingly, amplification of the nitrogenase gene nifH in tissues of 3 different coral species revealed that 71% of the sequences came from a bacterial group closely related to rhizobia, the N2-fixers symbiotic with legumes (Lema et al., 2012). The products of N2-fixation were initially assimilated by the zooxanthellae, then translocated to the animal host, as determined by δ15N analysis (Lesser et al., 2007). Moreover, Symbiodinium population density was positively correlated with nifH sequence copy number, suggesting that growth and division of the zooxanthellae might be dependent upon the product of N2-fixation (Olson et al., 2009). Taken together, these examples suggest that the cyanobacteria barter their N2-fixing ability for protection and nutrients from their hosts, thus providing a selective advantage to the hosts in N-limited environments.