Synchronized Regulation of Different Zwitterionic Metabolites in the Osmoadaption of Phytoplankton

Abstract

The ability to adapt to different seawater salinities is essential for cosmopolitan marine phytoplankton living in very diverse habitats. In this study, we examined the role of small zwitterionic metabolites in the osmoadaption of two common microalgae species Emiliania huxleyi and Prorocentrum minimum. By cultivation of the algae under salinities between 16‰ and 38‰ and subsequent analysis of dimethylsulfoniopropionate (DMSP), glycine betaine (GBT), gonyol, homarine, trigonelline, dimethylsulfonioacetate, trimethylammonium propionate, and trimethylammonium butyrate using HPLC-MS, we could reveal two fundamentally different osmoadaption mechanisms. While E. huxleyi responded with cell size reduction and a nearly constant ratio between the major metabolites DMSP, GBT and homarine to increasing salinity, osmolyte composition of P. minimum changed dramatically. In this alga DMSP concentration remained nearly constant at 18.6 mM between 20‰ and 32‰ but the amount of GBT and dimethylsulfonioacetate increased from 4% to 30% of total investigated osmolytes. Direct quantification of zwitterionic metabolites via LC-MS is a powerful tool to unravel the complex osmoadaption and regulation mechanisms of marine phytoplankton.

Phosphorus and nitrogen starvation reveal life‐cycle specific responses in the metabolome of Emiliania huxleyi (Haptophyta)

“…Our data show high variability of DMSP contents in the separate nutrient‐replete setups. Comparison of various studies also reveals general differences in the DMSP concentration, showing that separate cultivations cannot necessarily be directly compared (Gebser and Pohnert ). The more pronounced difference for nutrient‐replete stages of the P‐starvation setup could derive from the difference in harvesting time point, which has been reported before (Keller et al ).…”

“…We also found a significantly higher concentration of DMSP in the diploid stage, as has been shown before for the exact same E. huxleyi life‐cycle stages (2N: 580 fg cell −1 vs. 1N: 380 fg cell −1 ) (Spielmeyer et al ). Osmolyte abundance is influenced by salinity (Gebser and Pohnert ), however we assume that salinity (calculated as 31.27 g kg −1 ) did not change during cultivation. It is more likely that the lower DMSP abundance in the haploid stage is caused by an increased turnover of DMSP to dimethylsulfide (DMS), reported at transcriptomic level for DMSP lyase (Rokitta et al , Alcolombri et al 2015), which catalyzes the reaction.…”

Assessment of DMSP turnover reveals a non-bioavailable pool of dissolved DMSP in coastal waters of the Gulf of Mexico

“…Several intermediates in the phytoplankton DMSP synthesis pathway, such as dimethylsulfonium hydroxybutyrate, [68] could be present in seawater but virtually nothing is known about the lability of these compounds or their concentrations in seawater. The dimethylsulfonium compounds, gonyauline and gonyol are produced by some dinoflagellates such as Lingulodinium polyhedrum and Prorocentrum minimum, [69,70] and dimethylsulfocholine is present in the diatoms Nitzschia alba [71,72] and Phaeodactylum tricornutum, [73] but again nothing is known about the concentrations of these dimethyl sulfur compounds in seawater, or whether they release DMS under the alkaline conditions of our assays. Yet another possibility for the observed refractory 'DMSPd' pool is that it is a DMS complex of some kind that releases the DMS under strong basic conditions.…”

Linking microbial metabolism and organic matter cycling through metabolite distributions in the ocean

“…Studies using untargeted metabolomics with cultures of marine microbes have demonstrated that metabolites vary with growth stage in a marine diatom (Barofsky et al 2009) and that many metabolites produced cannot be predicted based on genomic information in a Synechococcus species . The fluctuation of different osmolytes in phytoplankton species as a function of salinity has also been observed (Gebser and Pohnert 2013). Co-culturing experiments have demonstrated that bacteria can induce changes in the metabolome of phytoplankton and that viral infection can also lead to increased production of certain metabolites Rosenwasser et al 2014).…”

“…Due to the sensitivity of metabolite concentrations to both genetic and environmental factors, the metabolite profile of an organism can be considered an aspect of its phenotype. Intracellular metabolite concentrations respond to physical, chemical, and biological environmental cues including nutrient limitation , salinity (Gebser and Pohnert 2013), temperature (Thompson et al 1992), oxidative stress (Lesser 2006), grazing (Pohnert 2000), viral lysis , and the presence of infochemicals ). For example, in response to infection by a phage, a marine bacterium had elevated intracellular concentrations of some amino acids and sugars .…”