Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica

Abstract

Summary Dimethylsulfoniopropionate (DMSP) is a globally abundant marine metabolite and a significant source of organic carbon and sulfur for marine microbial ecosystems with the potential to influence climate regulation. However, the physiological function of DMSP has remained enigmatic for >30 yr. Recent insight suggests that there are different physiological roles for DMSP based on the cellular DMSP concentrations in producers. Differential production of DMSP was tested with multiple physiological experiments that altered nitrate availability, salinity and temperature to create stressed growth and target different metabolic conditions in Emiliania huxleyi, a high DMSP producer and Thalassiosira oceanica, a low DMSP producer. Emiliania huxleyi intracellular DMSP did not respond to metabolically imbalanced conditions, while Thalassiosira oceanica intracellular DMSP was significantly correlated to stressed growth rate across all conditions tested and exhibited a plastic response on a timescale of hours in nonsteady‐state. The previous assumption that proposed DMSP mechanism(s) can be universally applied to all producers is shown to be unlikely. Rather, two distinct ecological roles for DMSP likely exist that differ by producer type, where: (1) the primary role of DMSP in high producers is a constitutive compatible solute; and (2) DMSP production in low producers is a finely tuned stress response.

DMSP synthesis genes distinguish two types of DMSP producer phenotypes

“…Prediction of in situ DMSP production is challenging, and the cellular roles of DMSP in producers remain unknown. However, recent work suggests that the two groups of DMSP producers, HiDPs and LoDPs, regulate DMSP synthesis for different cellular roles (McParland et al ., 2020). Accurate quantification of these two groups, particularly the HiDPs which appear to produce DMSP constitutively, could result in more accurate predictions of in situ DMSP production (Lyon et al ., 2011; McParland and Levine, 2019).…”

“…Recent work based on measurements of DMSP in many different isolates demonstrated that DMSP producers can be divided into two groups: high DMSP producers (HiDPs) and low DMSP producers (LoDPs). The two groups are defined by both the intracellular DMSP concentrations of producers, and changes in DMSP concentrations in response to different environmental conditions (McParland and Levine, 2019;McParland et al, 2020) (Fig. 1).…”

“…However, it is now known that LoDPs are phylogenetically widespread, and include many diatoms, as well as some Cyanobacteria, and heterotrophic Alphaproteobacteria (Bucciarelli et al ., 2013; Curson et al ., 2017; McParland and Levine, 2019). In contrast to HiDPs, LoDPs modify intracellular DMSP concentrations as a predictable function of stressed growth across many different environmental conditions (McParland et al ., 2020). The significant phenotypic differences between HiDPs and LoDPs are predicted to result in a general dominance of HiDP contribution to in situ DMSP production throughout the global open ocean, and a limited contribution by LoDPs (McParland and Levine, 2019).…”

Enhancing Salt Tolerance of Plants: From Metabolic Reprogramming to Exogenous Chemical Treatments and Molecular Approaches

“…In another study conducted in N. tabacum plants, short-term and low-dose SS induced metabolic shifts toward gluconeogenesis, which involved accumulation of mainly glucose, sucrose and fructose with depletion of pyrimidine and purine metabolites, while a high-dose of salt increased the accumulation of the osmolytes proline, myo-inositol and GABA [ 61 ]. Dimethylsulfoniopropionate (DMSP) is produced by a large diversity of macroalgae [ 110 ] and has a significant impact on SS and temperature shifts [ 111 , 112 ]. Intracellular functions of DMSP are not well understood but this molecule has been proposed to act as an osmoregulator [ 113 ] and antioxidant [ 114 ].…”

Dual thermal ecotypes co-exist within a nearly genetically-identical population of the unicellular marine cyanobacteriumSynechococcus

“…In addition, we measured the photosynthetic efficiency of photosystem II (Fv/Fm) 410 for these two strains when acclimated to 28° C using a PHYTO-PAM with an excitation 411 wavelength set to 645 nm for C-phycocyanin and allophycocyanin (Heinz Walz, Effeltrich, 412 Germany). Fv/Fm measurements were made using triplicate cultures and three technical 413 replicates each that were dark acclimated for 20 minutes, as in McParland et al (2019).…”