Limitation of dimethylsulfoniopropionate synthesis at high irradiance in natural phytoplankton communities of the Tropical Atlantic

Predictions of the ocean-atmosphere flux of dimethyl sulfide will be improved by understanding what controls seasonal and regional variations in dimethylsulfoniopropionate (DMSP) production. To investigate the influence of high levels of irradiance including ultraviolet radiation (UVR), on DMSP synthesis rates (lDMSP) and inorganic carbon fixation (lPOC) by natural phytoplankton communities, nine experiments were carried out at different locations in the low nutrient, high light environment of the northeastern Tropical Atlantic. Rates of lDMSP and lPOC were determined by measuring the incorporation of inorganic C into DMSP and particulate organic carbon. Based on measurements over discrete time intervals during the day, a unique lDMSP vs. irradiance (P vs. E) relationship was established. Comparison is made with the P vs. E relationship for lPOC, indicating that light saturation of lDMSP occurs at similar irradiance to lPOC and is closely coupled to carbon fixation on a diel basis. Photoinhibition during the middle of the day was exacerbated by exposure to UVR, causing an additional 55–60% inhibition of both lDMSP and lPOC at the highest light levels. In addition, decreased production of DMSP in response to UVR-induced photoxidative stress, contrasted with the increased net synthesis of photoprotective xanthophyll pigments. Together these results indicate that DMSP production by phytoplankton in the tropical ocean is not regulated in the short term by the necessity to control increasing photooxidative stress as irradiance increases during the day. The study provides new insight into the regulation of resource allocation into this biogeochemically important, multi-functional compatible solute. The oceans emit approximately 28.1 (17.6–34.4) million tons of sulfur in the form of dimethyl sulfide (DMS) each year (Lana et al. 2011), representing the largest natural flux of sulfur to the atmosphere. DMS is a product of the enzymatic breakdown of b-dimethylsulfoniopropionate (DMSP), an osmolyte synthesized by phytoplankton (Challenger and Simpson 1948). In recent years, the debate has intensified over the original proposal that DMS emission from the oceans contributed to an oceanic biology—climate feedback loop (Charlson et al. 1987; Cainey et al. 2008; Woodhouse et al. 2010; Quinn and Bates 2011). Nonetheless, this considerable source of sulfur has a substantial impact on atmospheric chemistry (Toumi 1994; Johnson and Bell 2008; Chen and Jang 2012). Oxidation of DMS results in the formation of sulfuric acid (H2SO4) and methylsulfonic acid (MSA). Sulfuric acid is the primary vapor responsible for new aerosol particles and cloud condensation nuclei (Sipil€ a et al. 2010; Kirkby et al. 2011), while MSA often makes a major contribution to the growth of existing aerosols (Rinaldi et al. 2010). Incorporation of the global seawater DMS climatology (Lana et al. 2011) into an aerosol-chemistry-climate general circulation model, illustrates large regional and seasonal variations in the cooling effect of DMS of 610 W m and a global mean annual influence of close to 22.0 W m (Mahajan et al. 2015). The magnitude of change in DMS emissions in the future remains an important issue for global atmospheric chemistry and climate. Mechanistic models that relate DMS emissions from the oceans to DMSP production and cycling, have attempted to capture the taxonomic and physiological factors that *Correspondence: [email protected] This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 227 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 63, 2018, 227–242 VC 2017 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10625 influence DMSP production to varying degrees (reviewed in Le Clainche et al. 2010). However, the competitive advantage DMSP production confers and how this contributes to temporal and regional patterns in production of DMS, remains unclear. Phytoplankton have generally been represented by between two and four functional types that differ in their DMSP cell quota (e.g., DMSP : carbon ratio) based largely on information derived from laboratory cultures of different microalgal strains (reviewed in Stefels et al. 2007). Intracellular concentrations vary between species of microalgae from undetectable levels to 100s mmol L (Keller et al. 1989). Modeled DMSP production is then a product of the DMSP cell quota, succession of the phytoplankton functional types, and primary production. In several models, parameterization of DMSP cell quotas has included the influence of light and/or nutrient availability and temperature dependence (e.g., Vallina et al. 2008; Vogt et al. 2010; Polimene et al. 2012), reflecting possible physiological roles of DMSP. DMSP appears to play multiple, potentially simultaneous roles in microalgae (reviewed in Stefels 2000, Stefels et al. 2007). The potential for accumulation of DMSP in the chloroplasts of microalgae (Lyon et al. 2011) and demonstrated chloroplast localization in higher plants (Trossat et al. 1998) supports the theory that DMSP, and possibly its breakdown products, may protect photosynthetic systems from oxidative damage caused by excess irradiance or nutrient limitation (Sunda et al. 2002). In contrast, a metabolic overflow hypothesis proposes that DMSP is synthesized to regulate intracellular methionine concentrations and photosynthetic overcapacity during unbalanced growth resulting from excess irradiance or nutrient limitation (Stefels 2000). DMSP may be employed as a methyl donor in biological transmethylation reactions (Ishida 1996 and references therein) and may be a precursor in the biosynthesis of the membrane phospholipid phosphatidylsulphocholine in marine microalgae (Kates and Volcani 1996). In addition, DMSP has been proposed to have a role as a grazing deterrent when ingestion or digestion of phytoplankton by grazers results in its enzymatic cleavage to DMS and acrylate (Dacey and Wakeham 1986; Wolfe and Steinke 1996), although DMSP has also been shown to be a chemoattractant for a variety of planktonic microbes (Seymour et al. 2010). Successfully modeling DMSP production in the ocean may require understanding how the environment affects which physiological roles drive synthesis and the cost vs. benefits of resource allocation to produce DMSP. There is a growing appreciation of the benefits in understanding photosynthetic resource allocation in phytoplankton in order to explain elemental and energetic stoichiometry and their impacts on community structure and ecosystem productivity (reviewed in Halsey and Jones 2015). This study expands this theme to how resource allocation by phytoplankton has implications for the atmosphere-ocean exchange of trace gases that influence atmospheric chemistry. Understanding how physiology and environmental variables affect the allocation of resources to metabolic pathways that result in the production of these volatile products may improve the capability of mechanistic models aimed at predicting oceanatmosphere exchange rates. One of the hurdles to understanding what drives the allocation of resources to DMSP production, and how rapidly DMSP is transformed, is the lack of direct estimates of DMSP synthesis rates. The introduction of a stable-isotope approach to determine in vivo DMSP production rates enables us to investigate how environmental factors drive DMSP production in natural and culture-based systems (Stefels et al. 2009). Without this key measurement, it has proven challenging to link DMS production to DMSP physiological function. Phytoplankton DMSP content and the rates at which it turns over, meaning synthesis vs. metabolism and release from cells, are key underlying factors that influence the seasonal and regional patterns of DMS in the ocean. This study investigated DMSP synthesis rates by natural phytoplankton communities in the high light, low nutrient environment of the subtropical and Tropical Atlantic Ocean. The resource allocation to DMSP was investigated by comparing directly measured rates of DMSP synthesis to rates of carbon fixation. The study aimed to also understand the physiological role of DMSP production by examining the influence of diel patterns of exposure to photosynthetically active radiation (PAR) and ultraviolet radiation (UVR) and the consequence of high light-induced photooxidative stress on DMSP synthesis compared to carbon fixation. The response of DMSP synthesis to photooxidative stress was also compared to the synthesis of pigments involved in the xanthophyll cycle, an established photoprotective mechanism. The study is an advance on previous assessments of the physiological role of DMSP because it examines specific rates of DMSP synthesis in relation to phytoplankton physiology and environmental factors, as opposed to examining net changes in DMSP concentration. By doing so, the study provides a more direct assessment of DMSP function that is less influenced by the many processes that control concentrations of DMSP in natural planktonic communities.