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Irradiance-mediated dimethylsulphoniopropionate (DMSP) responses of red coralline algae
Estuarine, Coastal and Shelf Science 96 (2012) 268e272
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Irradiance-mediated dimethylsulphoniopropionate (DMSP) responses of red coralline algae L.N. Rix a, H.L. Burdett b, *, N.A. Kamenos a, b a b
School of Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK School of Geographical and Earth Sciences, University of Glasgow, Glasgow G12 8QQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 May 2011 Accepted 11 November 2011 Available online 18 November 2011
Red coralline algae produce significant quantities of dimethylsulphoniopropionate (DMSP), whose breakdown products include the important climate gas dimethylsulphide (DMS) but little is known about how environmental factors influence this DMS(P) production. The effect of photosynthetically active radiation (PAR) on intracellular DMS(P) concentrations in the red coralline algae Lithothamnion glaciale was investigated using short (30 min) and longer-term (up to 507 h) acclimatory responses and control and high-PAR light regimes. Longer-term acclimatory intracellular DMS(P) concentrations were significantly reduced following exposure to high-PAR (220e250 mmol m2 s1). No short-term acclimatory effects were observed. We conclude that while DMS(P) content in L. glaciale does respond to changes in irradiance, the effect takes place over hours e days rather than minutes, suggesting a continued turnover of DMS(P) to combat oxidative stress induced by prolonged high-PAR exposure. Immediate short-term acclimatory responses do not appear to occur. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: algae coralline algae dimethylsulphide light maerl rhodolith sulphur
1. Introduction Free-living, red coralline algae (Rhodophyta: Corallinales), commonly known as maerl or rhodoliths, are long-lived and extremely slow growing (0.1e2 mm yr1) (Blake and Maggs, 2003; Bosence and Wilson, 2003), factors that may improve their resistance to environmental perturbations. Red coralline algae form extensive, globally distributed beds in coastal waters composed of layers of living and dead thalli overlaying carbonate rich sediments (Steller and Foster, 1995; Foster, 2001; BIOMAERL et al., 2003). Red coralline algae are usually found subtidally in the photic zone, due to their intolerance to desiccation (Wilson et al., 2004), and are depth limited by the level of light penetration (Foster, 2001). Dimethylsulphoniopropionate (DMSP) is a methionine-derived sulphonium compound that was first isolated from the red macroalga Polysiphonia fastigiata (Challenger and Simpson, 1948). DMSP may function as a compatible solute in osmotic regulation (Karsten et al., 1992), a cryoprotectant (Karsten et al., 1992), an overflow mechanism for dissipating excess energy and reduced compounds (Stefels, 2000), as an antioxidant (Sunda et al., 2002) and as an activated defence against herbivory (Van Alstyne et al.,
* Corresponding author. E-mail address: [email protected] (H.L. Burdett). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.11.022
2001; Wolfe et al., 2002). Phytoplankton are thought to be the dominant global producers of DMSP due to their large range and extensive blooms, but many species of macroalgae also contain intracellular DMSP þ dimethylsulphide (DMS) (DMS(P)) concentrations in the mM e mM range (e.g. Karsten et al., 1994; Van Alstyne, 2009), including red coralline algae (Kamenos et al., 2008b). Tropical coral reefs (Broadbent et al., 2002), coral mucus and mucus ropes (Broadbent and Jones, 2004) are often considered to be the most important benthic producers of DMS(P). However, DMS(P) concentrations in red coralline algae are reported to be comparable to concentrations observed in Chlorophyta and coral reefs and may make red coralline algae one of the largest macroalgal DMS(P) producers (Kamenos et al., 2008b). The intracellular DMS(P) content of marine algae is affected by a variety of environmental factors including salinity, temperature, nutrient availability, cell age and light intensity (Malin and Kirst, 1997; Stefels, 2000; Stefels et al., 2007; Van Alstyne and Puglisi, 2007). Increased irradiance has been shown to increase intracellular DMSP content in polar and temperate green macroalgae (Karsten et al., 1990, 1992; Lyons et al., 2010) and phytoplankton (e.g. Phaeocyctis and Emiliania huxleyi, Matrai et al., 1995; Slezak and Herndl, 2003). DMSP/DMS research has focussed on their roles in the biogeochemical sulphur cycle and potential impacts on climate. DMS flux from the ocean to the atmosphere accounts for one-quarter of
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global sulphur emissions (Liss et al., 1997). Atmospheric oxidation of DMS to sulphate aerosol particles may promote the formation of cloud condensation nuclei, influencing climate through increased cloud albedo (Andreae, 1990; Liss et al., 1997). An algal-aerosolclimate feedback loop has been proposed (Charlson et al., 1987), although this depends on a direct link between algal DMSP production and the formation between DMS-derived CCN. Oceanic DMS emissions depend on sea surface concentrations and the gas transfer velocity (Archer et al., 2009), while reactions with halogens and the presence of sea-salt particles and other aerosols in the atmosphere will affect the production of DMS-derived CCN (O’Dowd et al., 2002; Von Glasow and Crutzen, 2004; Leck and Bigg, 2005). The aim of this investigation was to determine the effect of irradiance on intracellular DMS(P) content in the red coralline alga Lithothamnion glaciale in the context of short- and longer-term acclimatory responses to environmental variability. This took into account an immediate response to change in irradiance and a longer-term acclimatory response, which may be important given the slow growth rate of L. glaciale (w200 mm yr1, Kamenos et al., 2008a), and slow production of DMSP by algae (e.g. Karsten et al., 1992; Lyons et al., 2010).
2. Materials and methods 2.1. Sample collection and handling Lithothamnion glaciale thalli were collected randomly from Loch Sween (56 020 N 05 360 W), Scotland, UK in November 2010. Thalli were collected at 6 m chart datum using SCUBA. Samples were transported to the University of Glasgow in seawater and held in 112 L recirculating seawater tanks (flow rate of 216 L h1) under ambient field conditions (10 1 C, 7:17 h light:dark regime, 70 mmol m2 s1 PAR, pH 8.1) for 4 weeks until the experiments were conducted. 2.2. Photosynthetically active radiation (PAR) measurements Light intensity in experimental tanks and in the field was measured using an Apogee QSO-E underwater electric calibrated sensor and Gemini voltage data logger. Field PAR data was collected from Loch Sween over four days to determine the ambient range of PAR experienced by Lithothamnion glaciale at that time of year (62 30 mmol m2 s1, mean SD, n ¼ 928, excludes night-time measurements). These data informed the experimental control level. Experimental PAR was regulated using 24 W T5 white fluorescent tubes, high intensity (14 000 K) 24 W T5 white fluorescent tubes and an Aquabeam 1000 HD LED light tile. The light produced by the Aquabeam tile decreased in intensity away from the center of the tank therefore thalli in this treatment were exposed to a light intensity range of 220e250 mmol m2 s1 within the experimental area (225 cm2). 2.3. Short-term acclimatory responses to brief PAR exposure Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was conducted. To determine the DMS(P)-manifested short-term acclimatory responses to PAR intensity, DMS(P) was quantified before and after 30 min exposure to four PAR treatments: 0, 70 (control intensity), 140 and 220e250 mmol m2 s1. Each PAR treatment was replicated in each of the three experimental tanks (thalli n ¼ 10 per tank, n ¼ 30 per treatment).
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2.4. Longer-term acclimatory responses to extended PAR exposure A time-series experiment was conducted to investigate the effect of PAR on DMS(P)-manifested longer-term acclimation responses in Lithothamnion glaciale over 98 h. Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was conducted. Experiments were conducted at 70 mmol m2 s1 (control treatment) and 220e250 mmol m2 s1 (high-PAR treatment) in separate tanks (n ¼ 2) with thalli (n ¼ 10) positioned to ensure an even distribution of PAR (the short-term acclimatory response experiments had shown no tank-effect on DMS(P) concentrations). Thalli were sampled in the dark (0 h) and after 0.5, 1, 1.5, 6, 50 and 98 h of PAR exposure under a 7:17 h light:dark regime. All replicate thalli were sampled at each sampling event, thus time was considered as a repeated measure. To examine the effect of increased PAR on DMS(P) concentration over an even longer period, additional thalli (n ¼ 10) were exposed to PAR treatments of 70 and 220e250 mmol m2 s1 (7:17 h, light:dark regime) and sampled once after 3 weeks (507 h). 2.5. Effect of burial on DMS(P) content To investigate the effect of burial on DMS(P) content, thalli (n ¼ 10) were half buried in carbonate sand sediment and exposed to 70 mmol m2 s1 PAR. Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was run. A control treatment of unburied thalli was run simultaneously in a separate tank and exposed to 70 mmol m2 s1 PAR (the short-term acclimatory response experiments had shown no tank-effect on DMS(P) concentrations). Thalli were sampled for DMS(P) after 3 weeks. 2.6. DMS(P) quantification For DMS(P) determination, w0.5 g of branch tips were sampled from each Lithothamnion glaciale thallus. Thalli tips were patted dry, cleaned to remove any attached sediment or debris and weighed. Thalli tips were quickly transferred to 14 ml vials containing 2000 ml of 10 M NaOH. NaOH hydrolysis results in a 1:1 conversion of algal DMSP to DMS, which diffuses into the vial headspace. Vials were immediately sealed using PharmaFix septa. Samples were incubated at room temperature in the dark for at least 48 h before analysis. This method does not differentiate between intracellular DMSP and DMS thus all measurements refer to intracellular DMS(P) concentration. DMS(P) was quantified using a Shimadzu 2014 gas chromatograph equipped with a flame photometric detector and capillary column (5% diphenyl-95% dimethyl polysiloxane; length 25 m; inner diameter 0.25 mm; film thickness 0.25 mm). The temperature of the injector, oven and detector were 45 C, 45 C, and 200 C, respectively. DMS retention time was w 1.5 min. Samples were analysed using direct injection of 100 ml from the vial headspace. Concentrations were calibrated against a DMSP standard (Research Plus Inc.) and normalised for algal biomass (5% of total mass for L. glaciale, as determined by Kamenos et al. (2008b)). The standard and sample detection limit was 960 ng of sulphur per headspace injection (sample peaks were w5 the magnitude of the detection limit) and precision was within 3%. 2.7. Statistical analysis All statistical analyses were performed using R v.2.12.1. Data in all experiments were log transformed to homogenise variance and meet assumptions of parametric testing. General linear models (GLMs) were used to analyse data from short-term acclimatory and
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burial experiments. Likelihood-ratio tests (LRTs) were used to compare models and determine the most parsimonious model. A repeated measures ANOVA was used to analyse the longer-term acclimatory experiment to account for the repeated sampling of the same thalli. All test assumptions were met without transformation. 3. Results 3.1. Field PAR measurements In Loch Sween, PAR at 6 m depth ranged from mmol m2 s1 in cloudy conditions and w20e80 w100e200 mmol m2 s1 in sunny conditions (Fig. 1). From these data, the experimental PAR treatments of 70 (control) 140, and 220e250 mmol m2 s1 (maximum field PAR) were chosen. 3.2. Short-term acclimatory responses to brief PAR exposure There was no difference in the mean intracellular DMS(P) concentration between PAR treatments after 30 min of PAR exposure (GLM: F3.116 ¼ 1.08, df ¼ 116, p ¼ 0.36) (Fig. 2). The mean (SE) intracellular concentration of DMS(P) in Lithothamnion glaciale ranged from 5.17 0.41 to 8.03 1.55 mg g1 biomass, with high variation in DMS(P) content among thalli (Fig. 2). Neither a tank effect (LRT: chi-sq ¼ 0.07, df ¼ 2, p ¼ 0.970), nor a tank-PAR interaction (LRT chi-sq ¼ 7.06, df ¼ 6, p ¼ 0.310) was observed. 3.3. Longer-term acclimatory responses to extended PAR exposure There was no significant difference in intracellular DMS(P) concentration in Lithothamnion glaciale with time during the longer-term acclimatory experiment under control conditions (70 mmol m2 s1) (F59 ¼ 0.95, p ¼ 0.33, Fig. 3). Under high-PAR conditions (220e250 mmol m2 s1), intracellular DMS(P) content of L. glaciale was significantly lower following exposure to high-PAR compared to the T0 measurement (F59 ¼ 6.89, p ¼ 0.01, Fig. 3). 3.4. Effect of burial on DMS(P) content No difference in intracellular DMS(P) was observed between unburied and partially buried Lithothamnion glaciale thalli (GLM: F1,18 ¼ 0.529, df ¼ 18, p ¼ 0.48) (Fig. 4).
Fig. 1. Photosynthetically active radiation (PAR, mmol m2 s1) recorded in Loch Sween over 4 days at 6 m chart datum in September 2010.
4. Discussion 4.1. Short-term acclimatory responses to brief PAR exposure PAR had no effect on the DMS(P) content of Lithothamnion glaciale in the short-term acclimatory response experiment (Fig. 2). The 30 min experimental interval may have been an insufficient amount of time to cause a response in DMS(P) synthesis in L. glaciale. While Slezak and Herndl (2003) observed an increase in DMS(P) content in Emiliania huxleyi after 6 h PAR exposure, changes in DMS(P) content in response to PAR have only been observed after several weeks in other marine algae (Karsten et al., 1992; Lyons et al., 2010). There is also evidence that changes in DMS(P) content in response to other environmental factors such as temperature (van Rijssel and Gieskes, 2002; Lyons et al., 2010) and salinity (Edwards et al., 1987, 1988) is a relatively slow process occurring over days to weeks rather than hours. These results support the proposal by Stefels (2000) that DMSP-synthesis (a high-energy process) is not actively regulated in response to shortterm acclimatory shock exposure to environmental change, but rather as a change in cell physiology to sustain growth in the longterm. 4.2. Longer-term acclimatory responses to extended PAR exposure Over the course of the longer-term acclimatory experiment, high-PAR exposure led to a significant lowering of intracellular DMS(P) concentration in Lithothamnion glaciale; an effect not observed in the control treatment (Fig. 3). Under a high-PAR regime, the production of reactive oxygen species (ROS) increases in other species (e.g. Ulva) (Barber and Andersson, 1992; Bischof et al., 2003). After T0, the relatively consistent DMS(P) concentrations in the high-PAR treatment may suggest a continued turnover of DMS(P) to combat antioxidant damage, perhaps mediated by the slow growth and low-light adaptation of red coralline algae (Foster, 2001). In the control treatment, lower ROS production may allow DMS(P) levels to sporadically replenish, leading to more variable intracellular DMS(P) concentrations. This study supports evidence that DMSP and DMS have antioxidant roles within algal cells (Sunda et al., 2002), but perhaps as a longer-term acclimatory mechanism for coping with high-PAR and increased ROS production in the longer-term. Other studies have shown a positive
Fig. 2. Intracellular DMS(P) (mg g1 biomass) in Lithothamnion glaciale after 30 min exposure to 0, 70, 140 and 220e250 mmol m2 s1 PAR. Data presented as mean standard error.
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Fig. 3. Normalised intracellular DMS(P) in Lithothamnion glaciale after 0, 0.5, 1, 1.5, 6, 50, 98 and 507 h exposure to 70 (black bars) or 220e250 (grey bars) mmol m2 s1 PAR under a 7:17 h light:dark regime. Data are normalised to T0 of each treatment and presented as mean standard error.
relationship between irradiance and DMSP content (Karsten et al., 1990, 1991, 1992; Matrai et al., 1995; Slezak and Herndl, 2003; Lyons et al., 2010). Time was also found to have a significant effect on mean intracellular DMS(P) content; high-PAR concentrations were more consistent than those under control conditions (Fig. 3). DMS(P) production and accumulation in L. glaciale appears to be highly variable and is likely affected by a complex interaction of biological and environmental factors. The effect of repeated sampling from thalli is believed to be negligible as red coralline algae reproduce through fragmentation (Foster, 2001), a mechanism that has been shown to have no effect on photosynthetic capacity in the red coralline algae species Phymatolithon calcareum (Wilson et al., 2004). The effect of light on DMS(P) production in marine algae may be influenced by factors other than intensity. In Antarctic green macroalgae, Karsten et al. (1990) found that at long day lengths, there was a positive relationship between DMSP content and increased PAR, but at short day lengths this effect was significantly reduced and DMSP content remained low and constant regardless of irradiance. Day length may be particularly important to consider in high latitude species such as L. glaciale, in which there is significant seasonal variation in the light cycle. The short day lengths used in
this experiment correspond to ambient winter conditions and it is possible that increased PAR would have had greater effect at longer day lengths (i.e. under a summer regime). 4.3. Effect of burial on DMS(P) content Red coralline algae typically inhabit disturbed habitats where they may experience partial burial for short periods of time by dead coralline algal fragments (Kamenos, pers. obs.). Partial burial in carbonate sediment had no significant effect on DMS(P) content after 3 weeks (Fig. 4). Previous studies have found burial to have a negative effect on the survival of red coralline algae, and this was been attributed to lack of light (Hall-Spencer and Moore, 2000; Riul et al., 2008). However, since red coralline algae including Lithothamnion glaciale, can survive long periods in the dark when unburied (Freiwald and Henrich, 1994; Wilson et al., 2004), it has been suggested that physical factors such as reduced water flow and gas exchange also impact coralline algal survival during burial (Wilson et al., 2004; Riul et al., 2008). Since L. glaciale was only 50% covered in this study, it is likely that sufficient light and water movement was present to prevent serious stress, at least over the three week experimental period. 5. Conclusions
Fig. 4. Intracellular DMS(P) (mg g1 biomass) in Lithothamnion glaciale after 3 weeks exposure to 70 mmol m2 s1 PAR: unburied (full exposure) and partial burial (50% thalli coverage with carbonate sand). Data presented as mean standard error.
Changes in PAR had an effect on DMS(P) content in Lithothamnion glaciale at time-scales greater than 30 min. This suggests that DMS(P) content in L. glaciale does not respond to short-term changes in irradiance/PAR. Therefore, in the field, DMS(P) content in L. glaciale is only likely to respond to increases in PAR when exposed for periods of hours to days, perhaps in response to an accumulation of ROS within the cells. Additionally, high variability between and within thalli suggests that irradiance alone does not fully explain the variation in DMS(P) content observed in L. glaciale; other biological or environmental factors may also play an important part in the natural variability of DMS(P) in red coralline algae. Lithothamnion glaciale is a dominant red coralline algal species in mid e high latitude shallow coastal waters and, like most coralline algae, is considered to be low-light adapted (Johansen, 1981). The importance of prolonged exposure in affecting DMSP concentrations suggests that a latitudinal gradient of DMSP content may be observed, with higher concentrations in polar samples where day length, irradiance and low water temperature may induce a cumulative, seasonal effect. L. glaciale has also been
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reported in 70 þ m water depth off the coast of Brazil (Foster et al., in press) e such thalli would be exposed to very low, seasonally consistent, irradiance levels and may, therefore exhibit no seasonal regulation of intracellular DMSP concentration. There is limited knowledge on the impact of coralline algal DMS(P) on dissolved DMS. Epithelial sloughing of coralline algae appears to be a primary factor in the intracellular release of DMSP to the water column and may have contributed to the large natural variation of intracellular DMS(P) concentrations found in this study (Kamenos et al., 2008b). Dissolved DMSP acts as a microbial respiratory substrate and promoting the formation of dissolved DMS. Coralline algae may be significant contributors to the dissolved DMSP/DMS load in coastal systems but this is still yet to be determined in the field. At present there is very little knowledge regarding the dynamics of DMS(P) synthesis in red coralline algae. Understanding the response of DMS(P) content in red coralline algae to environmental conditions will provide more insight into the physiological function of DMS(P) in red coralline algae as well as the role these algae play in the global biogeochemical sulphur cycle. Acknowledgements We thank Dan Haydon and Angela Hatton for analytical advice. This research was made partly possible by grants: Royal Society of Edinburgh/Scottish Government RSE 48704/1 to NAK and a Natural Environmental Research Council studentship NE/H525303/1 to HLB. Thanks also go to anonymous reviewers for helpful suggestions that improved the manuscript. References Andreae, M.O., 1990. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Marine Chemistry 30, 1e29. Archer, S., Cummings, D., Llewellyn, C., Fishwick, J., 2009. Phytoplankton taxa, irradiance and nutrient availability determine the seasonal cycle of DMSP in temperate shelf seas. Marine Ecology Progress Series 394, 111e124. Barber, J., Andersson, B., 1992. Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Sciences 17, 61e66. BIOMAERL, Barbera, C., Bordehore, C., Borg, J.A., Glemarec, M., Grall, J., HallSpencer, J.M., De la Huz, C., Lanfranco, E., Lastra, M., Moore, P.G., Mora, J., Pita, M.E., Ramos-Espla, A.A., Rizzo, M., Sanchez-Mata, A., Seva, A., Schembri, P.J., Valle, C., 2003. Conservation and management of northeast Atlantic and Mediterranean maerl beds. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S65eS76. Bischof, K., Janknegt, P.J., Buma, A.G.J., Rijstenbil, J.W., Peralta, G., Breeman, A.M., 2003. Oxidative stress and enzymartic scavenging of superoxide radicals induced by solar UV-B radiation in Ulva canopies from southern Spain. Scientia Marina (Barcelona) 67, 353e359. Blake, C., Maggs, C.A., 2003. Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from northern Europe. Phycologia 42, 606e612. Bosence, D., Wilson, J., 2003. Maerl growth, carbonate production rates and accumulation rates in the northeast Atlantic. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S21eS31. Broadbent, A.D., Jones, G.B., 2004. DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef. Marine & Freshwater Research 55, 849e855. Broadbent, A.D., Jones, G.B., Jones, R.J., 2002. DMSP in corals and benthic algae from the Great Barrier Reef. Estuarine, Coastal and Shelf Science 55, 547e555. Challenger, F., Simpson, I., 1948. Studies on biological methylation. Part XII. A precursor of the dimethyl sulphide evolved by Polysiphonia fastigiata. dimethyl-2-carboxyethylsulphonium hydroxide and its salts. Journal of the Chemical Society 43, 1591e1597. Charlson, R.J., Lovelock, J.E., Andreae, M.O., Warren, S.G., 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655e661. Edwards, D.M., Reed, R.H., Chudek, J.A., Foster, R., Stewart, W.D.P., 1987. Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Marine Biology 95, 583e592. Edwards, D.M., Reed, R.H., Stewart, W.D.P., 1988. Osmoacclimation in Enteromorpha intestinalis long-term effects of osmotic stress on organic solute accumulation. Marine Biology 98, 467e476. Foster, M.S., 2001. Rhodoliths: between rocks and soft places. Journal of Phycology 37, 659e667.
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Irradiance-mediated dimethylsulphoniopropionate (DMSP) responses of red coralline algae L.N. Rix a, H.L. Burdett b, *, N.A. Kamenos a, b a b
School of Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK School of Geographical and Earth Sciences, University of Glasgow, Glasgow G12 8QQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 20 May 2011 Accepted 11 November 2011 Available online 18 November 2011
Red coralline algae produce significant quantities of dimethylsulphoniopropionate (DMSP), whose breakdown products include the important climate gas dimethylsulphide (DMS) but little is known about how environmental factors influence this DMS(P) production. The effect of photosynthetically active radiation (PAR) on intracellular DMS(P) concentrations in the red coralline algae Lithothamnion glaciale was investigated using short (30 min) and longer-term (up to 507 h) acclimatory responses and control and high-PAR light regimes. Longer-term acclimatory intracellular DMS(P) concentrations were significantly reduced following exposure to high-PAR (220e250 mmol m2 s1). No short-term acclimatory effects were observed. We conclude that while DMS(P) content in L. glaciale does respond to changes in irradiance, the effect takes place over hours e days rather than minutes, suggesting a continued turnover of DMS(P) to combat oxidative stress induced by prolonged high-PAR exposure. Immediate short-term acclimatory responses do not appear to occur. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: algae coralline algae dimethylsulphide light maerl rhodolith sulphur
1. Introduction Free-living, red coralline algae (Rhodophyta: Corallinales), commonly known as maerl or rhodoliths, are long-lived and extremely slow growing (0.1e2 mm yr1) (Blake and Maggs, 2003; Bosence and Wilson, 2003), factors that may improve their resistance to environmental perturbations. Red coralline algae form extensive, globally distributed beds in coastal waters composed of layers of living and dead thalli overlaying carbonate rich sediments (Steller and Foster, 1995; Foster, 2001; BIOMAERL et al., 2003). Red coralline algae are usually found subtidally in the photic zone, due to their intolerance to desiccation (Wilson et al., 2004), and are depth limited by the level of light penetration (Foster, 2001). Dimethylsulphoniopropionate (DMSP) is a methionine-derived sulphonium compound that was first isolated from the red macroalga Polysiphonia fastigiata (Challenger and Simpson, 1948). DMSP may function as a compatible solute in osmotic regulation (Karsten et al., 1992), a cryoprotectant (Karsten et al., 1992), an overflow mechanism for dissipating excess energy and reduced compounds (Stefels, 2000), as an antioxidant (Sunda et al., 2002) and as an activated defence against herbivory (Van Alstyne et al.,
* Corresponding author. E-mail address: [email protected] (H.L. Burdett). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.11.022
2001; Wolfe et al., 2002). Phytoplankton are thought to be the dominant global producers of DMSP due to their large range and extensive blooms, but many species of macroalgae also contain intracellular DMSP þ dimethylsulphide (DMS) (DMS(P)) concentrations in the mM e mM range (e.g. Karsten et al., 1994; Van Alstyne, 2009), including red coralline algae (Kamenos et al., 2008b). Tropical coral reefs (Broadbent et al., 2002), coral mucus and mucus ropes (Broadbent and Jones, 2004) are often considered to be the most important benthic producers of DMS(P). However, DMS(P) concentrations in red coralline algae are reported to be comparable to concentrations observed in Chlorophyta and coral reefs and may make red coralline algae one of the largest macroalgal DMS(P) producers (Kamenos et al., 2008b). The intracellular DMS(P) content of marine algae is affected by a variety of environmental factors including salinity, temperature, nutrient availability, cell age and light intensity (Malin and Kirst, 1997; Stefels, 2000; Stefels et al., 2007; Van Alstyne and Puglisi, 2007). Increased irradiance has been shown to increase intracellular DMSP content in polar and temperate green macroalgae (Karsten et al., 1990, 1992; Lyons et al., 2010) and phytoplankton (e.g. Phaeocyctis and Emiliania huxleyi, Matrai et al., 1995; Slezak and Herndl, 2003). DMSP/DMS research has focussed on their roles in the biogeochemical sulphur cycle and potential impacts on climate. DMS flux from the ocean to the atmosphere accounts for one-quarter of
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global sulphur emissions (Liss et al., 1997). Atmospheric oxidation of DMS to sulphate aerosol particles may promote the formation of cloud condensation nuclei, influencing climate through increased cloud albedo (Andreae, 1990; Liss et al., 1997). An algal-aerosolclimate feedback loop has been proposed (Charlson et al., 1987), although this depends on a direct link between algal DMSP production and the formation between DMS-derived CCN. Oceanic DMS emissions depend on sea surface concentrations and the gas transfer velocity (Archer et al., 2009), while reactions with halogens and the presence of sea-salt particles and other aerosols in the atmosphere will affect the production of DMS-derived CCN (O’Dowd et al., 2002; Von Glasow and Crutzen, 2004; Leck and Bigg, 2005). The aim of this investigation was to determine the effect of irradiance on intracellular DMS(P) content in the red coralline alga Lithothamnion glaciale in the context of short- and longer-term acclimatory responses to environmental variability. This took into account an immediate response to change in irradiance and a longer-term acclimatory response, which may be important given the slow growth rate of L. glaciale (w200 mm yr1, Kamenos et al., 2008a), and slow production of DMSP by algae (e.g. Karsten et al., 1992; Lyons et al., 2010).
2. Materials and methods 2.1. Sample collection and handling Lithothamnion glaciale thalli were collected randomly from Loch Sween (56 020 N 05 360 W), Scotland, UK in November 2010. Thalli were collected at 6 m chart datum using SCUBA. Samples were transported to the University of Glasgow in seawater and held in 112 L recirculating seawater tanks (flow rate of 216 L h1) under ambient field conditions (10 1 C, 7:17 h light:dark regime, 70 mmol m2 s1 PAR, pH 8.1) for 4 weeks until the experiments were conducted. 2.2. Photosynthetically active radiation (PAR) measurements Light intensity in experimental tanks and in the field was measured using an Apogee QSO-E underwater electric calibrated sensor and Gemini voltage data logger. Field PAR data was collected from Loch Sween over four days to determine the ambient range of PAR experienced by Lithothamnion glaciale at that time of year (62 30 mmol m2 s1, mean SD, n ¼ 928, excludes night-time measurements). These data informed the experimental control level. Experimental PAR was regulated using 24 W T5 white fluorescent tubes, high intensity (14 000 K) 24 W T5 white fluorescent tubes and an Aquabeam 1000 HD LED light tile. The light produced by the Aquabeam tile decreased in intensity away from the center of the tank therefore thalli in this treatment were exposed to a light intensity range of 220e250 mmol m2 s1 within the experimental area (225 cm2). 2.3. Short-term acclimatory responses to brief PAR exposure Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was conducted. To determine the DMS(P)-manifested short-term acclimatory responses to PAR intensity, DMS(P) was quantified before and after 30 min exposure to four PAR treatments: 0, 70 (control intensity), 140 and 220e250 mmol m2 s1. Each PAR treatment was replicated in each of the three experimental tanks (thalli n ¼ 10 per tank, n ¼ 30 per treatment).
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2.4. Longer-term acclimatory responses to extended PAR exposure A time-series experiment was conducted to investigate the effect of PAR on DMS(P)-manifested longer-term acclimation responses in Lithothamnion glaciale over 98 h. Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was conducted. Experiments were conducted at 70 mmol m2 s1 (control treatment) and 220e250 mmol m2 s1 (high-PAR treatment) in separate tanks (n ¼ 2) with thalli (n ¼ 10) positioned to ensure an even distribution of PAR (the short-term acclimatory response experiments had shown no tank-effect on DMS(P) concentrations). Thalli were sampled in the dark (0 h) and after 0.5, 1, 1.5, 6, 50 and 98 h of PAR exposure under a 7:17 h light:dark regime. All replicate thalli were sampled at each sampling event, thus time was considered as a repeated measure. To examine the effect of increased PAR on DMS(P) concentration over an even longer period, additional thalli (n ¼ 10) were exposed to PAR treatments of 70 and 220e250 mmol m2 s1 (7:17 h, light:dark regime) and sampled once after 3 weeks (507 h). 2.5. Effect of burial on DMS(P) content To investigate the effect of burial on DMS(P) content, thalli (n ¼ 10) were half buried in carbonate sand sediment and exposed to 70 mmol m2 s1 PAR. Thalli were acclimated under control conditions for 48 h after transfer from the holding tank to the experimental tanks before the experiment was run. A control treatment of unburied thalli was run simultaneously in a separate tank and exposed to 70 mmol m2 s1 PAR (the short-term acclimatory response experiments had shown no tank-effect on DMS(P) concentrations). Thalli were sampled for DMS(P) after 3 weeks. 2.6. DMS(P) quantification For DMS(P) determination, w0.5 g of branch tips were sampled from each Lithothamnion glaciale thallus. Thalli tips were patted dry, cleaned to remove any attached sediment or debris and weighed. Thalli tips were quickly transferred to 14 ml vials containing 2000 ml of 10 M NaOH. NaOH hydrolysis results in a 1:1 conversion of algal DMSP to DMS, which diffuses into the vial headspace. Vials were immediately sealed using PharmaFix septa. Samples were incubated at room temperature in the dark for at least 48 h before analysis. This method does not differentiate between intracellular DMSP and DMS thus all measurements refer to intracellular DMS(P) concentration. DMS(P) was quantified using a Shimadzu 2014 gas chromatograph equipped with a flame photometric detector and capillary column (5% diphenyl-95% dimethyl polysiloxane; length 25 m; inner diameter 0.25 mm; film thickness 0.25 mm). The temperature of the injector, oven and detector were 45 C, 45 C, and 200 C, respectively. DMS retention time was w 1.5 min. Samples were analysed using direct injection of 100 ml from the vial headspace. Concentrations were calibrated against a DMSP standard (Research Plus Inc.) and normalised for algal biomass (5% of total mass for L. glaciale, as determined by Kamenos et al. (2008b)). The standard and sample detection limit was 960 ng of sulphur per headspace injection (sample peaks were w5 the magnitude of the detection limit) and precision was within 3%. 2.7. Statistical analysis All statistical analyses were performed using R v.2.12.1. Data in all experiments were log transformed to homogenise variance and meet assumptions of parametric testing. General linear models (GLMs) were used to analyse data from short-term acclimatory and
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burial experiments. Likelihood-ratio tests (LRTs) were used to compare models and determine the most parsimonious model. A repeated measures ANOVA was used to analyse the longer-term acclimatory experiment to account for the repeated sampling of the same thalli. All test assumptions were met without transformation. 3. Results 3.1. Field PAR measurements In Loch Sween, PAR at 6 m depth ranged from mmol m2 s1 in cloudy conditions and w20e80 w100e200 mmol m2 s1 in sunny conditions (Fig. 1). From these data, the experimental PAR treatments of 70 (control) 140, and 220e250 mmol m2 s1 (maximum field PAR) were chosen. 3.2. Short-term acclimatory responses to brief PAR exposure There was no difference in the mean intracellular DMS(P) concentration between PAR treatments after 30 min of PAR exposure (GLM: F3.116 ¼ 1.08, df ¼ 116, p ¼ 0.36) (Fig. 2). The mean (SE) intracellular concentration of DMS(P) in Lithothamnion glaciale ranged from 5.17 0.41 to 8.03 1.55 mg g1 biomass, with high variation in DMS(P) content among thalli (Fig. 2). Neither a tank effect (LRT: chi-sq ¼ 0.07, df ¼ 2, p ¼ 0.970), nor a tank-PAR interaction (LRT chi-sq ¼ 7.06, df ¼ 6, p ¼ 0.310) was observed. 3.3. Longer-term acclimatory responses to extended PAR exposure There was no significant difference in intracellular DMS(P) concentration in Lithothamnion glaciale with time during the longer-term acclimatory experiment under control conditions (70 mmol m2 s1) (F59 ¼ 0.95, p ¼ 0.33, Fig. 3). Under high-PAR conditions (220e250 mmol m2 s1), intracellular DMS(P) content of L. glaciale was significantly lower following exposure to high-PAR compared to the T0 measurement (F59 ¼ 6.89, p ¼ 0.01, Fig. 3). 3.4. Effect of burial on DMS(P) content No difference in intracellular DMS(P) was observed between unburied and partially buried Lithothamnion glaciale thalli (GLM: F1,18 ¼ 0.529, df ¼ 18, p ¼ 0.48) (Fig. 4).
Fig. 1. Photosynthetically active radiation (PAR, mmol m2 s1) recorded in Loch Sween over 4 days at 6 m chart datum in September 2010.
4. Discussion 4.1. Short-term acclimatory responses to brief PAR exposure PAR had no effect on the DMS(P) content of Lithothamnion glaciale in the short-term acclimatory response experiment (Fig. 2). The 30 min experimental interval may have been an insufficient amount of time to cause a response in DMS(P) synthesis in L. glaciale. While Slezak and Herndl (2003) observed an increase in DMS(P) content in Emiliania huxleyi after 6 h PAR exposure, changes in DMS(P) content in response to PAR have only been observed after several weeks in other marine algae (Karsten et al., 1992; Lyons et al., 2010). There is also evidence that changes in DMS(P) content in response to other environmental factors such as temperature (van Rijssel and Gieskes, 2002; Lyons et al., 2010) and salinity (Edwards et al., 1987, 1988) is a relatively slow process occurring over days to weeks rather than hours. These results support the proposal by Stefels (2000) that DMSP-synthesis (a high-energy process) is not actively regulated in response to shortterm acclimatory shock exposure to environmental change, but rather as a change in cell physiology to sustain growth in the longterm. 4.2. Longer-term acclimatory responses to extended PAR exposure Over the course of the longer-term acclimatory experiment, high-PAR exposure led to a significant lowering of intracellular DMS(P) concentration in Lithothamnion glaciale; an effect not observed in the control treatment (Fig. 3). Under a high-PAR regime, the production of reactive oxygen species (ROS) increases in other species (e.g. Ulva) (Barber and Andersson, 1992; Bischof et al., 2003). After T0, the relatively consistent DMS(P) concentrations in the high-PAR treatment may suggest a continued turnover of DMS(P) to combat antioxidant damage, perhaps mediated by the slow growth and low-light adaptation of red coralline algae (Foster, 2001). In the control treatment, lower ROS production may allow DMS(P) levels to sporadically replenish, leading to more variable intracellular DMS(P) concentrations. This study supports evidence that DMSP and DMS have antioxidant roles within algal cells (Sunda et al., 2002), but perhaps as a longer-term acclimatory mechanism for coping with high-PAR and increased ROS production in the longer-term. Other studies have shown a positive
Fig. 2. Intracellular DMS(P) (mg g1 biomass) in Lithothamnion glaciale after 30 min exposure to 0, 70, 140 and 220e250 mmol m2 s1 PAR. Data presented as mean standard error.
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Fig. 3. Normalised intracellular DMS(P) in Lithothamnion glaciale after 0, 0.5, 1, 1.5, 6, 50, 98 and 507 h exposure to 70 (black bars) or 220e250 (grey bars) mmol m2 s1 PAR under a 7:17 h light:dark regime. Data are normalised to T0 of each treatment and presented as mean standard error.
relationship between irradiance and DMSP content (Karsten et al., 1990, 1991, 1992; Matrai et al., 1995; Slezak and Herndl, 2003; Lyons et al., 2010). Time was also found to have a significant effect on mean intracellular DMS(P) content; high-PAR concentrations were more consistent than those under control conditions (Fig. 3). DMS(P) production and accumulation in L. glaciale appears to be highly variable and is likely affected by a complex interaction of biological and environmental factors. The effect of repeated sampling from thalli is believed to be negligible as red coralline algae reproduce through fragmentation (Foster, 2001), a mechanism that has been shown to have no effect on photosynthetic capacity in the red coralline algae species Phymatolithon calcareum (Wilson et al., 2004). The effect of light on DMS(P) production in marine algae may be influenced by factors other than intensity. In Antarctic green macroalgae, Karsten et al. (1990) found that at long day lengths, there was a positive relationship between DMSP content and increased PAR, but at short day lengths this effect was significantly reduced and DMSP content remained low and constant regardless of irradiance. Day length may be particularly important to consider in high latitude species such as L. glaciale, in which there is significant seasonal variation in the light cycle. The short day lengths used in
this experiment correspond to ambient winter conditions and it is possible that increased PAR would have had greater effect at longer day lengths (i.e. under a summer regime). 4.3. Effect of burial on DMS(P) content Red coralline algae typically inhabit disturbed habitats where they may experience partial burial for short periods of time by dead coralline algal fragments (Kamenos, pers. obs.). Partial burial in carbonate sediment had no significant effect on DMS(P) content after 3 weeks (Fig. 4). Previous studies have found burial to have a negative effect on the survival of red coralline algae, and this was been attributed to lack of light (Hall-Spencer and Moore, 2000; Riul et al., 2008). However, since red coralline algae including Lithothamnion glaciale, can survive long periods in the dark when unburied (Freiwald and Henrich, 1994; Wilson et al., 2004), it has been suggested that physical factors such as reduced water flow and gas exchange also impact coralline algal survival during burial (Wilson et al., 2004; Riul et al., 2008). Since L. glaciale was only 50% covered in this study, it is likely that sufficient light and water movement was present to prevent serious stress, at least over the three week experimental period. 5. Conclusions
Fig. 4. Intracellular DMS(P) (mg g1 biomass) in Lithothamnion glaciale after 3 weeks exposure to 70 mmol m2 s1 PAR: unburied (full exposure) and partial burial (50% thalli coverage with carbonate sand). Data presented as mean standard error.
Changes in PAR had an effect on DMS(P) content in Lithothamnion glaciale at time-scales greater than 30 min. This suggests that DMS(P) content in L. glaciale does not respond to short-term changes in irradiance/PAR. Therefore, in the field, DMS(P) content in L. glaciale is only likely to respond to increases in PAR when exposed for periods of hours to days, perhaps in response to an accumulation of ROS within the cells. Additionally, high variability between and within thalli suggests that irradiance alone does not fully explain the variation in DMS(P) content observed in L. glaciale; other biological or environmental factors may also play an important part in the natural variability of DMS(P) in red coralline algae. Lithothamnion glaciale is a dominant red coralline algal species in mid e high latitude shallow coastal waters and, like most coralline algae, is considered to be low-light adapted (Johansen, 1981). The importance of prolonged exposure in affecting DMSP concentrations suggests that a latitudinal gradient of DMSP content may be observed, with higher concentrations in polar samples where day length, irradiance and low water temperature may induce a cumulative, seasonal effect. L. glaciale has also been
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reported in 70 þ m water depth off the coast of Brazil (Foster et al., in press) e such thalli would be exposed to very low, seasonally consistent, irradiance levels and may, therefore exhibit no seasonal regulation of intracellular DMSP concentration. There is limited knowledge on the impact of coralline algal DMS(P) on dissolved DMS. Epithelial sloughing of coralline algae appears to be a primary factor in the intracellular release of DMSP to the water column and may have contributed to the large natural variation of intracellular DMS(P) concentrations found in this study (Kamenos et al., 2008b). Dissolved DMSP acts as a microbial respiratory substrate and promoting the formation of dissolved DMS. Coralline algae may be significant contributors to the dissolved DMSP/DMS load in coastal systems but this is still yet to be determined in the field. At present there is very little knowledge regarding the dynamics of DMS(P) synthesis in red coralline algae. Understanding the response of DMS(P) content in red coralline algae to environmental conditions will provide more insight into the physiological function of DMS(P) in red coralline algae as well as the role these algae play in the global biogeochemical sulphur cycle. Acknowledgements We thank Dan Haydon and Angela Hatton for analytical advice. This research was made partly possible by grants: Royal Society of Edinburgh/Scottish Government RSE 48704/1 to NAK and a Natural Environmental Research Council studentship NE/H525303/1 to HLB. Thanks also go to anonymous reviewers for helpful suggestions that improved the manuscript. References Andreae, M.O., 1990. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Marine Chemistry 30, 1e29. Archer, S., Cummings, D., Llewellyn, C., Fishwick, J., 2009. Phytoplankton taxa, irradiance and nutrient availability determine the seasonal cycle of DMSP in temperate shelf seas. Marine Ecology Progress Series 394, 111e124. Barber, J., Andersson, B., 1992. Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Sciences 17, 61e66. BIOMAERL, Barbera, C., Bordehore, C., Borg, J.A., Glemarec, M., Grall, J., HallSpencer, J.M., De la Huz, C., Lanfranco, E., Lastra, M., Moore, P.G., Mora, J., Pita, M.E., Ramos-Espla, A.A., Rizzo, M., Sanchez-Mata, A., Seva, A., Schembri, P.J., Valle, C., 2003. Conservation and management of northeast Atlantic and Mediterranean maerl beds. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S65eS76. Bischof, K., Janknegt, P.J., Buma, A.G.J., Rijstenbil, J.W., Peralta, G., Breeman, A.M., 2003. Oxidative stress and enzymartic scavenging of superoxide radicals induced by solar UV-B radiation in Ulva canopies from southern Spain. Scientia Marina (Barcelona) 67, 353e359. Blake, C., Maggs, C.A., 2003. Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from northern Europe. Phycologia 42, 606e612. Bosence, D., Wilson, J., 2003. Maerl growth, carbonate production rates and accumulation rates in the northeast Atlantic. Aquatic Conservation: Marine and Freshwater Ecosystems 13, S21eS31. Broadbent, A.D., Jones, G.B., 2004. DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef. Marine & Freshwater Research 55, 849e855. Broadbent, A.D., Jones, G.B., Jones, R.J., 2002. DMSP in corals and benthic algae from the Great Barrier Reef. Estuarine, Coastal and Shelf Science 55, 547e555. Challenger, F., Simpson, I., 1948. Studies on biological methylation. Part XII. A precursor of the dimethyl sulphide evolved by Polysiphonia fastigiata. dimethyl-2-carboxyethylsulphonium hydroxide and its salts. Journal of the Chemical Society 43, 1591e1597. Charlson, R.J., Lovelock, J.E., Andreae, M.O., Warren, S.G., 1987. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655e661. Edwards, D.M., Reed, R.H., Chudek, J.A., Foster, R., Stewart, W.D.P., 1987. Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Marine Biology 95, 583e592. Edwards, D.M., Reed, R.H., Stewart, W.D.P., 1988. Osmoacclimation in Enteromorpha intestinalis long-term effects of osmotic stress on organic solute accumulation. Marine Biology 98, 467e476. Foster, M.S., 2001. Rhodoliths: between rocks and soft places. Journal of Phycology 37, 659e667.
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