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RESEARCH ARTICLE

Effects of temperature and nutrients on the emissions of biogenic volatile sulfur compounds from Ulva prolifera during the bloom decline period

Lu Han A B , Pei-Feng Li A , Chun-Ying Liu https://orcid.org/0000-0002-9052-2800 A B C and Gui-Peng Yang https://orcid.org/0000-0002-0107-4568 A B C
+ Author Affiliations
- Author Affiliations

A Frontiers Science Center for Deep Ocean Multispheres and Earth System, Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, and College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, China.

B Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China.

C Corresponding authors. Email: roseliu@ouc.edu.cn; gpyang@ouc.edu.cn

Environmental Chemistry 18(6) 214-225 https://doi.org/10.1071/EN21072
Submitted: 1 June 2021  Accepted: 26 September 2021   Published: 25 October 2021

Environmental context. Blooms of Ulva prolifera have recurred annually in the Yellow Sea since 2007, causing economic losses and severe ecological problems. We conducted laboratory incubation experiments to examine the effects of temperature and nutrients on its biogenic sulfur emissions during its decline period. Increasing temperature and nutrients affected the decay of U. prolifera, resulting in respective decreased and increased emission of biogenic sulfur compounds.

Abstract. The Ulva prolifera blooms have recurred annually in the Yellow Sea (YS) since 2007, causing huge economic losses and severe ecological problems. So far, few studies have investigated the release of volatile biogenic sulfur compounds by the U. prolifera blooms. In this study, laboratory incubation experiments were conducted to examine the effects of temperature and nutrient concentrations on the emissions of biogenic sulfur compounds during the green tide decline period. Under simulated conditions, higher incubation temperatures and nutrient concentrations promoted the decay of U. prolifera. When the incubation temperature was increased from 20 °C to 25 °C, the mean concentrations of dimethylsulfide (DMS), dissolved dimethylsulfoniopropionate (DMSPd) and particulate dimethylsulfoniopropionate (DMSPp) in the culture medium decreased by ~20 %, 55 % and 20 % respectively; in addition, these values increased by ~40 %, 70 % and 240 % respectively when exogenous nutrients were added to the culture medium. Moreover, a high concentration of nitrate (NO3) (>50 μM) could promote the release of biogenic sulfur by U. prolifera in the absence of other nutrients. The findings of this study provide insight into the roles of macroalgae on changes to the environment and shed light on the potential impact of DMSP and other degradation products of DMS produced by the green tide on the environment and ecosystem.

Keywords: Ulva prolifera, dimethylsulfide (DMS), dimethylsulfoniopropionate (DMSP), green tide, temperature, nutrients, Yellow Sea.


References

Andreae MO, Barnard WR (1983). Determination of trace quantities of dimethyl sulfide in aqueous solutions. Analytical Chemistry 55, 608–612.
Determination of trace quantities of dimethyl sulfide in aqueous solutions.Crossref | GoogleScholarGoogle Scholar |

Barrón C, Apostolaki ET, Duarte CM (2014). Dissolved organic carbon fluxes by seagrass meadows and macroalgal beds. Frontiers in Marine Science 1, 42
Dissolved organic carbon fluxes by seagrass meadows and macroalgal beds.Crossref | GoogleScholarGoogle Scholar |

Berges JA, Franklin DJ, Harrison PJ (2001). Evolution of an Artificial Seawater Medium: Improvements in Enriched Seawater, Artificial Water Over the Last Two Decades. Journal of Phycology 37, 1138–1145.
Evolution of an Artificial Seawater Medium: Improvements in Enriched Seawater, Artificial Water Over the Last Two Decades.Crossref | GoogleScholarGoogle Scholar |

Cao Y, Wu Y, Fang Z, Cui X, Liang J, Song X (2019). Spatiotemporal Patterns and Morphological Characteristics of Ulva prolifera Distribution in the Yellow Sea, China in 2016–2018. Remote Sensing 11, 445
Spatiotemporal Patterns and Morphological Characteristics of Ulva prolifera Distribution in the Yellow Sea, China in 2016–2018.Crossref | GoogleScholarGoogle Scholar |

Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987). Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655–661.
Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate.Crossref | GoogleScholarGoogle Scholar |

Cui J, Shi J, Zhang J, Wang L, Fan S, Xu Z, Huo Y, Zhou Q, Lu Y, He P (2018). Rapid expansion of Ulva blooms in the Yellow Sea, China through sexual reproduction and vegetative growth. Marine Pollution Bulletin 130, 223–228.
Rapid expansion of Ulva blooms in the Yellow Sea, China through sexual reproduction and vegetative growth.Crossref | GoogleScholarGoogle Scholar | 29866551PubMed |

Dacey JWH, Blough NV (1987). Hydroxide decomposition of dimethylsulfoniopropionate to form dimethylsulfide. Geophysical Research Letters 14, 1246–1249.
Hydroxide decomposition of dimethylsulfoniopropionate to form dimethylsulfide.Crossref | GoogleScholarGoogle Scholar |

Dacey JWH, Wakeham SG (1986). Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233, 1314–1316.
Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Deng X, Liu T, Liu C, Liang S, Hu Y, Jin Y, Wang X (2018). Effects of Ulva prolifera blooms on the carbonate system in the coastal waters of Qingdao. Marine Ecology Progress Series 605, 73–86.
Effects of Ulva prolifera blooms on the carbonate system in the coastal waters of Qingdao.Crossref | GoogleScholarGoogle Scholar |

Ding Y-M (2014). Migration and transformation of biogenic elements and their effects on ecological environment in the green tide of Yellow Sea. PhD dissertation, Graduate School of Chinese Academy of Sciences (Institute of Oceanology).

Evans G (1972). ‘The quantitative analysis of plant growth.’ (Blackwell Scientific Publications: Oxford)

Feng L, Shi X, Chen Y, Tang H, Wang L (2021). Effects of Temperature on the Nitrate Reductase Activity and Growth of Ulva prolifera. Journal of Phycology 57, 955–966.
Effects of Temperature on the Nitrate Reductase Activity and Growth of Ulva prolifera.Crossref | GoogleScholarGoogle Scholar | 33544874PubMed |

Han L, Deng X, Li PF, Gao XC, Liu CY (2018). Effects of temperature on biogenic sulfur production of Ulva prolifera during the decline period. Acta Oceanologica Sinica 40, 110–118. [in Chinese with English abstract]

Han L, Yang G-P, Liu C-Y, Jin Y-M, Liu T (2021). Emissions of biogenic sulfur compounds and their regulation by nutrients during an Ulva prolifera bloom in the Yellow Sea. Marine Pollution Bulletin 162, 111885
Emissions of biogenic sulfur compounds and their regulation by nutrients during an Ulva prolifera bloom in the Yellow Sea.Crossref | GoogleScholarGoogle Scholar | 33302126PubMed |

Keller MD, Bellows WK, Guillard RRL (1989). Dimethylsulfide production in marine phytoplankton. In ‘Biogenic sulphur in the environment’. (Eds ES Saltzman, WJ Cooper) pp. 167–182. (American Chemical Society: Washington DC)

Kiene RP, Linn LJ (2000). The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP. Geochimica et Cosmochimica Acta 64, 2797–2810.
The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP.Crossref | GoogleScholarGoogle Scholar |

Kiene RP, Service SK (1991). Decomposition of dissolved DMSP and DMS in estuarine waters: dependence on temperature and substrate concentration. Marine Ecology Progress Series 76, 1–11.
Decomposition of dissolved DMSP and DMS in estuarine waters: dependence on temperature and substrate concentration.Crossref | GoogleScholarGoogle Scholar |

Lana A, Bell TG, Simó R, Vallina SM, Ballabrera‐Poy J, Kettle AJ, Dachs J, Bopp L, Saltzman ES, Stefels J, Johnson JE, Liss PS (2011). An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean. Global Biogeochemical Cycles 25, GB1004
An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean.Crossref | GoogleScholarGoogle Scholar |

Li H, Zhang Y, Han X, Shi X, Rivkin RB, Legendre L (2016). Growth responses of Ulva prolifera to inorganic and organic nutrients: Implications for macroalgal blooms in the southern Yellow Sea, China. Scientific Reports 6, 26498
Growth responses of Ulva prolifera to inorganic and organic nutrients: Implications for macroalgal blooms in the southern Yellow Sea, China.Crossref | GoogleScholarGoogle Scholar | 27199215PubMed |

Liu D, Zhou M (2018). Green tides of the Yellow Sea: massive free-floating blooms of Ulva prolifera, In ‘Global ecology and oceanography of harmful algal blooms’. (Eds P Glibert, E Berdalet, M Burford, G Pitcher, M Zhou) pp. 317–326. (Springer International Publishing: Cham)10.1007/978-3-319-70069-4_16

Liu D, Keesing JK, He P, Wang Z, Shi Y, Wang Y (2013). The world’s largest macroalgal bloom in the Yellow Sea, China: Formation and implications. Estuarine, Coastal and Shelf Science 129, 2–10.
The world’s largest macroalgal bloom in the Yellow Sea, China: Formation and implications.Crossref | GoogleScholarGoogle Scholar |

Liu C-Y, Xu G-B, Deng X, Zhang H-H, Liu T, Yang G-P (2020). Changes in concentrations of biogenic sulfur compounds in coastal waters off Qingdao, China during an Ulva prolifera bloom. Marine Pollution Bulletin 152, 110940
Changes in concentrations of biogenic sulfur compounds in coastal waters off Qingdao, China during an Ulva prolifera bloom.Crossref | GoogleScholarGoogle Scholar | 32479301PubMed |

Malin G, Turner SM, Liss PS (1992). Sulfur: the plankton/climate connection. Journal of Phycology 28, 590–597.
Sulfur: the plankton/climate connection.Crossref | GoogleScholarGoogle Scholar |

McLenon AL, DiTullio GR (2012). Effects of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum. Biogeochemistry 110, 17–29.
Effects of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum.Crossref | GoogleScholarGoogle Scholar |

Nevitt GA, Veit RR, Kareiva P (1995). Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376, 680–682.
Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds.Crossref | GoogleScholarGoogle Scholar |

Nguyen BC, Mihalopoulos N, Putaud JP, Gaudry A, Gallet L, Keene WC, Galloway JN (1992). Covariations in oceanic dimethyl sulfide, its oxidation products and rain acidity at Amsterdam Island in the Southern Indian Ocean. Journal of Atmospheric Chemistry 15, 39–53.
Covariations in oceanic dimethyl sulfide, its oxidation products and rain acidity at Amsterdam Island in the Southern Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Ouyang L-J, Gao Y-H, Lin R-C, Liang J-R (2006). The Production of DMS by Emiliania huxleyi (Haptophyceae) Under Different Salinity and Temperature Conditions. Journal of Xiamen University (Natural Science) 45, 221–224.
The Production of DMS by Emiliania huxleyi (Haptophyceae) Under Different Salinity and Temperature Conditions.Crossref | GoogleScholarGoogle Scholar | [in Chinese with English abstract]

Park K-T, Jang S, Lee K, Yoon YJ, Kim M-S, Park K, Cho H-J, Kang J-H, Udisti R, Lee B-Y, Shin K-H (2017). Observational evidence for the formation of DMS-derived aerosols during Arctic phytoplankton blooms. Atmospheric Chemistry and Physics 17, 9665–9675.
Observational evidence for the formation of DMS-derived aerosols during Arctic phytoplankton blooms.Crossref | GoogleScholarGoogle Scholar |

Qu B, Yang G-P, Guo L-Y, Zhao L (2020). The satellite derived environmental factors and their relationships with dimethylsulfide in the East Marginal Seas of China. Journal of Marine Systems 204, 103305
The satellite derived environmental factors and their relationships with dimethylsulfide in the East Marginal Seas of China.Crossref | GoogleScholarGoogle Scholar |

Quinn PK, Bates TS (2011). The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480, 51–56.
The case against climate regulation via oceanic phytoplankton sulphur emissions.Crossref | GoogleScholarGoogle Scholar | 22129724PubMed |

Shi X, Qi M, Tang H, Han X (2015). Spatial and temporal nutrient variations in the Yellow Sea and their effects on Ulva prolifera blooms. Estuarine, Coastal and Shelf Science 163, 36–43.
Spatial and temporal nutrient variations in the Yellow Sea and their effects on Ulva prolifera blooms.Crossref | GoogleScholarGoogle Scholar |

Shooter D, Brimblecombe P (1989). Dimethylsulphide oxidation in the ocean. Deep-Sea Research. Part A, Oceanographic Research Papers 36, 577–585.
Dimethylsulphide oxidation in the ocean.Crossref | GoogleScholarGoogle Scholar |

Simó R (2001). Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends in Ecology & Evolution 16, 287–294.
Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links.Crossref | GoogleScholarGoogle Scholar |

Singh SP, Singh P (2015). Effect of temperature and light on the growth of algae species: a review. Renewable & Sustainable Energy Reviews 50, 431–444.
Effect of temperature and light on the growth of algae species: a review.Crossref | GoogleScholarGoogle Scholar |

Smetacek V, Zingone A (2013). Green and golden seaweed tides on the rise. Nature 504, 84–88.
Green and golden seaweed tides on the rise.Crossref | GoogleScholarGoogle Scholar | 24305152PubMed |

Song W, Li Y, Fang S, Wang Z, Xiao J, Li R, Fu M, Zhu M, Zhang X (2015). Temporal and spatial distributions of green algae micro-propagules in the coastal waters of the Subei Shoal, China. Estuarine, Coastal and Shelf Science 163, 29–35.
Temporal and spatial distributions of green algae micro-propagules in the coastal waters of the Subei Shoal, China.Crossref | GoogleScholarGoogle Scholar |

Spielmeyer A, Pohnert G (2012). Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Marine Environmental Research 73, 62–69.
Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 22130520PubMed |

Steinke M, Malin G, Liss PS (2002). Trophic Interactions in the Sea: An Ecological Role for Climate Relevant Volatiles?. Journal of Phycology 38, 630–638.
Trophic Interactions in the Sea: An Ecological Role for Climate Relevant Volatiles?.Crossref | GoogleScholarGoogle Scholar |

Sun K-M, Li R, Li Y, Xin M, Xiao J, Wang Z, Tang X, Pang M (2015). Responses of Ulva prolifera to short-term nutrient enrichment under light and dark conditions. Estuarine, Coastal and Shelf Science 163, 56–62.
Responses of Ulva prolifera to short-term nutrient enrichment under light and dark conditions.Crossref | GoogleScholarGoogle Scholar |

Sun J, Todd JD, Thrash JC, Qian Y, Qian MC, Temperton B, Guo J, Fowler EK, Aldrich JT, Nicora CD, Lipton MS, Smith RD, De Leenheer P, Payne SH, Johnston AWB, Davie-Martin CL, Halsey KH, Giovannoni SJ (2016). The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nature Microbiology 1, 16065
The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol.Crossref | GoogleScholarGoogle Scholar | 27573103PubMed |

Sunda WG, Hardison R, Kiene RP, Bucciarelli E, Harada H (2007). The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications. Aquatic Sciences 69, 341–351.
The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications.Crossref | GoogleScholarGoogle Scholar |

Tan T-T, Liu C-Y, Liu T, Xu G-B, Zhang L, Deng X, Lu X-L (2018). Effects of environmental factors on growth of Ulva prolifera and its biogenic sulfur release. Oceanologia et Limnologia Sinica 49, 793–801.

Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K (1997). Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42, 1105–1118.
Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences.Crossref | GoogleScholarGoogle Scholar |

Van Alstyne KL, Puglisi MP (2007). DMSP in marine macroalgae and macroinvertebrates: Distribution, function, and ecological impacts. Aquatic Sciences 69, 394–402.
DMSP in marine macroalgae and macroinvertebrates: Distribution, function, and ecological impacts.Crossref | GoogleScholarGoogle Scholar |

Van Alstyne KL, Gifford S-A, Dohman JM, Savedo MM (2016). Effects of environmental changes, tissue types and reproduction on the emissions of dimethyl sulfide from seaweeds that form green tides. Environmental Chemistry 13, 220–230.
Effects of environmental changes, tissue types and reproduction on the emissions of dimethyl sulfide from seaweeds that form green tides.Crossref | GoogleScholarGoogle Scholar |

Wada S, Hama T (2013). The contribution of macroalgae to the coastal dissolved organic matter pool. Estuarine, Coastal and Shelf Science 129, 77–85.
The contribution of macroalgae to the coastal dissolved organic matter pool.Crossref | GoogleScholarGoogle Scholar |

Wang C, Qiao H, Pan G, Zhang B, Niu J, Wang G, Sun S, Zhou B (2008). Studies on the parameters of physiology of Enteromorpha prolifera collected from the Qingdao Olympic sailing center. Marketing Science 32, 13–15. [in Chinese with English abstract]

Wang Z, Xiao J, Fan S, Li Y, Liu X, Liu D (2015). Who made the world’s largest green tide in China? An integrated study on the initiation and early development of the green tide in Yellow Sea. Limnology and Oceanography 60, 1105–1117.
Who made the world’s largest green tide in China? An integrated study on the initiation and early development of the green tide in Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Wang C, Su R, Guo L, Yang B, Zhang Y, Zhang L, Xu H, Shi W, Wei L (2019). Nutrient absorption by Ulva prolifera and the growth mechanism leading to green-tides. Estuarine, Coastal and Shelf Science 227, 106329
Nutrient absorption by Ulva prolifera and the growth mechanism leading to green-tides.Crossref | GoogleScholarGoogle Scholar |

Wu X, Li P-F, Liu C-Y, Zhang H-H, Yang G-P, Zhang S-H, Zhu M-X (2017). Biogeochemistry of Dimethylsulfide, Dimethylsulfoniopropionate, and Acrylic Acid in the Changjiang Estuary and the East China Sea. Journal of Geophysical Research. Oceans 122, 10245–10261.
Biogeochemistry of Dimethylsulfide, Dimethylsulfoniopropionate, and Acrylic Acid in the Changjiang Estuary and the East China Sea.Crossref | GoogleScholarGoogle Scholar |

Yang H, Kirst GO (1997). Effect of UV-radiation on DMSP content and DMS formation of Phaeocystis antarctica. Polar Biology 18, 402–409.
Effect of UV-radiation on DMSP content and DMS formation of Phaeocystis antarctica.Crossref | GoogleScholarGoogle Scholar |

Yang G-P, Zhang S-H, Zhang H-H, Yang J, Liu C-Y (2015). Distribution of biogenic sulfur in the Bohai Sea and northern Yellow Sea and its contribution to atmospheric sulfate aerosol in the late fall. Marine Chemistry 169, 23–32.
Distribution of biogenic sulfur in the Bohai Sea and northern Yellow Sea and its contribution to atmospheric sulfate aerosol in the late fall.Crossref | GoogleScholarGoogle Scholar |

Yoch DC (2002). Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Applied and Environmental Microbiology 68, 5804–5815.
Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide.Crossref | GoogleScholarGoogle Scholar | 12450799PubMed |

Zhao S, Xu B, Yao Q, Burnett WC, Charette MA, Su R, Lian E, Yu Z (2021). Nutrient-rich submarine groundwater discharge fuels the largest green tide in the world. The Science of the Total Environment 770, 144845
Nutrient-rich submarine groundwater discharge fuels the largest green tide in the world.Crossref | GoogleScholarGoogle Scholar | 33736390PubMed |

Zhu R, Zhang H-H, Zhang J, Yang G (2018). Experimental study on the production of dimethylsulfide and dimethylsulfoniopropionate by two marine microalgae with different ratios of nitrogen to phosphorus and iron concentrations. Periodical of Ocean University of China 48, 62–70.

Zimmer-Faust RK, de Souza MP, Yoch DC (1996). Bacterial Chemotaxis and its Potential Role in Marine Dimethylsulfide Production and Biogeochemical Sulfur Cycling. Limnology and Oceanography 41, 1330–1334.
Bacterial Chemotaxis and its Potential Role in Marine Dimethylsulfide Production and Biogeochemical Sulfur Cycling.Crossref | GoogleScholarGoogle Scholar |