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RESEARCH ARTICLE

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

Chengxuan Li A B C , Gui-Peng Yang A , David J. Kieber D , Jessie Motard-Côté B C and Ronald P. Kiene B C E
+ Author Affiliations
- Author Affiliations

A College of Chemistry and Chemical Engineering, Ocean University of China, Qingdao 266100, Shandong, P.R. China.

B Department of Marine Sciences, University of South Alabama, 5871 USA Drive North, Mobile, AL 36688, USA.

C Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, AL 36528, USA.

D Department of Chemistry, State University of New York, College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210, USA.

E Corresponding author. Email: rkiene@disl.org

Environmental Chemistry 13(2) 266-279 https://doi.org/10.1071/EN15052
Submitted: 7 March 2015  Accepted: 18 June 2015   Published: 17 September 2015

Environmental context. DMSP is one of the most important substrates for marine bacteria and its cycling contributes substantially to fluxes of carbon and sulfur in the ocean. Accurate determination of the concentration of DMSP available to bacteria is essential to quantifying DMSP consumption rates, and this work improves those determinations by identifying non-bioavailable pools of DMSP that have previously gone unrecognised. Improved estimates of DMSP consumption rates will lead to better understanding of its role in ocean food web and biogeochemical dynamics.

Abstract. Dissolved dimethylsulfoniopropionate (DMSPd) is an important substrate for marine microbes and a precursor of sulfur gases. We compared DMSPd turnover flux rates in coastal seawater measured with a 35S-DMSPd tracer to those obtained with the DMSP-uptake inhibitor glycine betaine (GBT). The 35S-DMSP tracer method yielded DMSPd turnover fluxes (35.7–215 nM day–1) that were 1.7 to 152 times higher than those obtained in parallel samples with the GBT inhibitor method (0.34–21.6 nM day–1). Tests confirmed that GBT functioned as planned by strongly inhibiting DMSPd degradation and that 35S-DMSPd gave accurate estimates of DMSPd loss rate constants. This left the initial DMSPd concentrations, determined by small volume drip filtration (SVDF) through Whatman GF/F filters (0.7-μm nominal retention) ([DMSPd]SVDF), as a potential cause of the discrepancy in rate estimates. Indeed, GF/F filtrate incubations showed that the initial [DMSPd]SVDF overestimated the bioavailable DMSPd concentrations for at least two reasons: (1) a significant fraction (10–37 %) of DMSP passing through GF/F filters was in particles >0.2 μm (likely bacteria) and therefore not dissolved, and (2) a significant pool (0.44–1.0 nM) of operationally dissolved, non-particle DMSP ([DMSPd]<0.2 μm), comprising 40–99 % of [DMSPd]SVDF, was refractory to degradation on a time scale of days. The nature of this refractory DMSP is currently unknown. Accounting for DMSP-containing particles and the refractory DMSP pool in GF/F filtrates is necessary to obtain the true bioavailable DMSPd concentrations, which we estimate to be very low (0.006–1.0 nM; mean of 0.41 nM) in the coastal waters examined, and to avoid overestimation of DMSPd turnover fluxes when using the 35S-DMSP tracer technique.

Additional keywords: bacteria, bioavailability, carbon and sulfur fluxes, climate, dimethylsulfide, DMSPd, filtration, GBT, glycine betaine, organic sulfur, phytoplankton, refractory, uptake inhibitor.


References

[1]  G. Blunden, S. M. Gordon, Betaines and their sulphonio analogues in marine algae, in Progress in Phycological Research (Eds F. E. Round, D. J. Chapman) 1986, pp. 39–80 (Biopress Ltd.: Bristol, UK).

[2]  J. Stefels, Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 2000, 43, 183.
Physiological aspects of the production and conversion of DMSP in marine algae and higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtb4%3D&md5=23897818cf9950bd364d15554611ea98CAS |

[3]  M. D. Keller, W. K. Bellows, R. R. L. Guillard, Dimethyl sulfide production in marine phytoplankton, in Biogenic sulfur in the environment (Eds E. Saltzman, W. J. Cooper) 1989, pp. 167–182 (American Chemical Society: New York).

[4]  G. O. Kirst, Osmotic adjustment in phytoplankton and macroalgae: the use of dimethylsulfoniopropionate (DMSP), in Biological and environmental chemistry of DMSP and related sulfonium compounds (Eds R. P. Kiene, P. T. Visscher, M. D. Keller, G. O. Kirst) 1996, pp. 121–129 (Plenum: New York).

[5]  W. Sunda, D. J. Kieber, R. P. Kiene, S. Huntsman, An antioxidant function for DMSP and DMS in marine algae. Nature 2002, 418, 317.
An antioxidant function for DMSP and DMS in marine algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlGms7k%3D&md5=1bcaa8d9ca44d13d4f343901c31cbed2CAS | 12124622PubMed |

[6]  U. Karsten, C. Weincke, G. O. Kirst, Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol. 1992, 12, 603.
Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature.Crossref | GoogleScholarGoogle Scholar |

[7]  S. Strom, G. Wolfe, A. Slajer, S. Lambert, J. Clough, Chemical defense in the microplankton II: Inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP). Limnol. Oceanogr. 2003, 48, 230.
Chemical defense in the microplankton II: Inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVGrurk%3D&md5=e5ea46aaf4035f67e08621ea3dc217aaCAS |

[8]  J. R. Seymour, R. Simo, T. Ahmed, R. Stocker, Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 2010, 329, 342.
Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosl2iu70%3D&md5=9160e8f0cec3e1f870bdb4bc1f5ff2baCAS | 20647471PubMed |

[9]  T. G. Bell, A. J. Poulton, G. Malin, Strong linkages between dimethylsulphoniopropionate (DMSP) and phytoplankton community physiology in a large subtropical and tropical Atlantic Ocean data set. Global Biogeochem. Cycles 2010, 24, GB3009.
Strong linkages between dimethylsulphoniopropionate (DMSP) and phytoplankton community physiology in a large subtropical and tropical Atlantic Ocean data set.Crossref | GoogleScholarGoogle Scholar |

[10]  F. C. van Duyl, W. W. C. Gieskes, A. J. Kop, W. E. Lewis, Biological control of short-term variation in the concentration of DMSP and DMS during a Phaeocystis spring bloom. J. Sea Res. 1998, 40, 221.
Biological control of short-term variation in the concentration of DMSP and DMS during a Phaeocystis spring bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVOjtQ%3D%3D&md5=71e2b839906448b79e58d694d362e074CAS |

[11]  J. W. H. Dacey, F. A. Howse, A. F. Michaels, S. G. Wakeham, Temporal variability of dimethylsulfide and dimethylsulfoniopropionate in the Sargasso Sea. Deep-Sea Res. 1998, 45, 2085.
Temporal variability of dimethylsulfide and dimethylsulfoniopropionate in the Sargasso Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFyjtg%3D%3D&md5=2b6f731fece8163c3026294a4fe21309CAS |

[12]  R. P. Kiene, D. Slezak, Low dissolved DMSP concentrations in seawater revealed by small volume gravity filtration and dialysis sampling. Limnol. Oceanogr. Methods 2006, 4, 80.
Low dissolved DMSP concentrations in seawater revealed by small volume gravity filtration and dialysis sampling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlWnt70%3D&md5=d76bee9995b6021df822bbc9b36611e1CAS |

[13]  P. A. Matrai, M. D. Keller, Dimethylsulfide in a large-scale coccolithophore bloom in the Gulf of Maine. Cont. Shelf Res. 1993, 13, 831.
Dimethylsulfide in a large-scale coccolithophore bloom in the Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |

[14]  S. Belviso, S. K. Kim, F. Rassoulzadegan, B. Krajka, B. C. Nguyen, N. Mihalopoulos, P. Buat-Menard, Production of dimethylsulfonium propionate (DMSP) and dimethylsulfide (DMS) by a microbial food web. Limnol. Oceanogr. 1990, 35, 1810.
Production of dimethylsulfonium propionate (DMSP) and dimethylsulfide (DMS) by a microbial food web.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvFylu70%3D&md5=2a27feb95b74ab34db56760a53b9e763CAS |

[15]  K. Tang, H. Damm, P. T. Visscher, Dimethylsulfoniopropionate (DMSP) in marine copepods and its relation with diets and salinity. Mar. Ecol. Prog. Ser. 1999, 179, 71.
Dimethylsulfoniopropionate (DMSP) in marine copepods and its relation with diets and salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1ektQ%3D%3D&md5=94af535ae06165c4b350c8c9c32a3f20CAS |

[16]  S. Besiktepe, K. W. Tang, M. Vila, R. Simó, Dimethylated sulfur compounds in seawater, seston and mesozooplankton in the seas around Turkey. Deep Sea Res. Part I Oceanogr. Res. Pap. 2004, 51, 1179.
Dimethylated sulfur compounds in seawater, seston and mesozooplankton in the seas around Turkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlSjs70%3D&md5=ac17b6d49b7b62ea69e43fbafc0cde0dCAS |

[17]  J. W. H. Dacey, S. G. Wakeham, Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 1986, 233, 1314.
Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlsFygu7c%3D&md5=05f3b25ed5af4f3abe50bc7f4c90ebfdCAS |

[18]  R. W. Hill, B. A. White, M. T. Cottrell, J. W. H. Dacey, Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquat. Microb. Ecol. 1998, 14, 1.
Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process.Crossref | GoogleScholarGoogle Scholar |

[19]  W. H. Wilson, S. Turner, N. H. Mann, Population dynamics of phytoplankton and viruses in a phosphate-limited mesocosm and their effect on DMSP and DMS production. Estuar. Coast. Shelf Sci. 1998, 46, 49.
Population dynamics of phytoplankton and viruses in a phosphate-limited mesocosm and their effect on DMSP and DMS production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFOjtbo%3D&md5=ecc584b373ce1b1e2b3bfe193e898e86CAS |

[20]  G. Yang, J. Zhang, L. Li, J. Qi, Dimethylsulfide in the surface water of the East China Sea. Cont. Shelf Res. 2000, 20, 69.
Dimethylsulfide in the surface water of the East China Sea.Crossref | GoogleScholarGoogle Scholar |

[21]  R. P. Kiene, L. J. Linn, Distribution and turnover of dissolved DMSP and its relationship with bacterial production in the Gulf of Mexico. Limnol. Oceanogr. 2000, 45, 849.
Distribution and turnover of dissolved DMSP and its relationship with bacterial production in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslerurw%3D&md5=2c4c9a097c6fe991fcea8b2ab530dfc4CAS |

[22]  M. V. Zubkov, B. M. Fuchs, S. D. Archer, R. P. Kiene, R. Amann, P. H. Burkill, Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 2002, 49, 3017.
Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlKntLg%3D&md5=e13228fcf9fe3b6647e298fc03fdd23bCAS |

[23]  R. Simó, M. Vila-Costa, L. Alonso-Sáez, C. Cardelús, O. Guadayol, E. Vazquez-Dominguez, J. M. Gasol, Annual DMSP contribution to S and C fluxes through phytoplankton and bacterioplankton in a NW Mediterranean coastal site. Aquat. Microb. Ecol. 2009, 57, 43.
Annual DMSP contribution to S and C fluxes through phytoplankton and bacterioplankton in a NW Mediterranean coastal site.Crossref | GoogleScholarGoogle Scholar |

[24]  M. V. Zubkov, B. M. Fuchs, S. D. Archer, R. P. Kiene, R. Amann, P. H. Burkill, Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionate in an algal bloom in the North Sea. Environ. Microbiol. 2001, 3, 304.
Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionate in an algal bloom in the North Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1eht7o%3D&md5=56fb73e3cfeb2e09258afbfb238db71fCAS | 11422317PubMed |

[25]  R. P. Kiene, L. J. Linn, J. A. Bruton, New and important roles for DMSP in marine microbial communities. J. Sea Res. 2000, 43, 209.
New and important roles for DMSP in marine microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtbw%3D&md5=789cb96d8406d5bbead908e442a540f1CAS |

[26]  R. Malmstrom, R. P. Kiene, D. L. Kirchman, Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico. Limnol. Oceanogr. 2004, 49, 597.
Identification and enumeration of bacteria assimilating dimethylsulfoniopropionate (DMSP) in the North Atlantic and Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFWnsrw%3D&md5=81599f3cff83d337c6f99e23c549dea2CAS |

[27]  R. R. Malmstrom, R. P. Kiene, M. Vila, D. L. Kirchman, Dimethylsulfoniopropionate (DMSP) assimilation by Synechococcus in the Gulf of Mexico and Northwest Atlantic Ocean. Limnol. Oceanogr. 2005, 50, 1924.
Dimethylsulfoniopropionate (DMSP) assimilation by Synechococcus in the Gulf of Mexico and Northwest Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWrsb7F&md5=34f0144c03ef36bce734f07335e43889CAS |

[28]  R. R. Malmstrom, R. P. Kiene, M. T. Cottrell, D. L. Kirchman, Contribution of SAR11 bacteria to dssolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic Ocean. Appl. Environ. Microbiol. 2004, 70, 4129.
Contribution of SAR11 bacteria to dssolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWntLg%3D&md5=db45c5bb58f39f93ec3803e278f793cdCAS | 15240292PubMed |

[29]  J. Pinhassi, R. Simó, J. M. Gonzalez, M. Vila, L. Alonso-Saez, R. P. Kiene, M. A. Moran, C. Pedrós-Alió, Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom. Appl. Environ. Microbiol. 2005, 71, 7650.
Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlehtL3I&md5=2e3b362564c875206655496feed9db66CAS | 16332737PubMed |

[30]  M. Vila-Costa, J. Pinhassi, C. Alonso, J. Pernthaler, R. Simó, An annual cycle of dimethylsulfoniopropionate-sulfur and leucine assimilating bacterioplankton in the coastal NW Mediterranean. Environ. Microbiol. 2007, 9, 2451.
An annual cycle of dimethylsulfoniopropionate-sulfur and leucine assimilating bacterioplankton in the coastal NW Mediterranean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1GqsL%2FM&md5=a8957051105db725f2d33ac2e6440915CAS | 17803771PubMed |

[31]  M. Vila-Costa, R. Simó, H. Harada, J. M. Gasol, D. Slezak, R. P. Kiene, Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 2006, 314, 652.
Dimethylsulfoniopropionate uptake by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 17068265PubMed |

[32]  R. P. Kiene, Microbial sources and sinks for methylated sulfur compounds in the marine environment, in Microbial growth on C1 compounds (Eds D. P. Kelly, J. C. Murrell) 1993, pp. 15–33 (Intercept Ltd.: London).

[33]  M. O. Andreae, W. R. Barnard, The marine chemistry of dimethylsulfide. Mar. Chem. 1984, 14, 267.
The marine chemistry of dimethylsulfide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXht1Kmtr0%3D&md5=75382396dbd0654c24a82d6b500b1c1aCAS |

[34]  A. J. Kettle, M. O. Andreae, D. Amouroux, T. W. Andreae, T. S. Bates, H. Berreshiem, H. Bingemer, R. Boniforti, M. A. J. Curran, G. R. DiTullio, G. Helas, G. B. Jones, M. D. Keller, R. P. Kiene, C. Leck, M. Levasseur, G. Malin, M. Maspero, P. Matrai, A. R. McTaggart, N. Mihalopoulos, B. C. Nguyen, A. Novo, J. P. Putaud, S. Rapsomanikis, G. Roberts, G. Schebeske, S. Sharma, R. Simó, R. Staubes, S. Turner, G. Uher, A global database of sea surface dimethylsulfide (DMS) measurements and a procedure to predict sea surface DMS as a function of latitude, longitude, and month. Global Biogeochem. Cycles 1999, 13, 399.
A global database of sea surface dimethylsulfide (DMS) measurements and a procedure to predict sea surface DMS as a function of latitude, longitude, and month.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOrurw%3D&md5=3e01efeae39142a226504b21f3453f02CAS |

[35]  A. J. Kettle, M. O. Andreae, Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models. J. Geophys. Res. 2000, 105, 26793.
Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovFGit7c%3D&md5=f9eb766ebcf418a31aafcb35e629ea5cCAS |

[36]  A. Lana, T. G. Bell, R. Simó, S. M. Vallina, J. Ballabrera-Poy, A. J. Kettle, J. Dachs, L. Bopp, E. S. Saltzman, J. Stefels, J. E. Johnson, P. S. Liss, An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean. Global Biogeochem. Cycles 2011, 25, GB1004.
An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean.Crossref | GoogleScholarGoogle Scholar |

[37]  R. J. Charlson, J. E. Lovelock, M. O. Andreae, S. G. Warren, Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate. Nature 1987, 326, 655.
Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitVWgsb8%3D&md5=24299dba1956a59c2726d9e91321070cCAS |

[38]  R. P. Kiene, L. J. Linn, The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP. Geochim. Cosmochim. Acta 2000, 64, 2797.
The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVKktL8%3D&md5=0187e2eab0851b1bf8fc20c33d7c3f4bCAS |

[39]  A. M. L. Merzouk, M. G. Scarratt, S. Michaud, R. B. Rivkin, M. S. Hale, R. P. Kiene, N. M. Price, W. K. W. Li, DMSP and DMS dynamics during a mesoscale iron fertilization experiment in the Northeast Pacific. Part II: bacterial cycling. Deep Sea Res. Part II Top. Stud. Oceanogr. 2006, 53, 2370.
DMSP and DMS dynamics during a mesoscale iron fertilization experiment in the Northeast Pacific. Part II: bacterial cycling.Crossref | GoogleScholarGoogle Scholar |

[40]  D. Slezak, R. P. Kiene, D. A. Toole, R. Simó, D. J. Kieber, Effects of solar radiation on the fate of dissolved DMSP and conversion to DMS in seawater. Aquat. Sci. 2007, 69, 377.
Effects of solar radiation on the fate of dissolved DMSP and conversion to DMS in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ajtrjE&md5=51283ff554b23394d2790b20e69b0889CAS |

[41]  R. P. Kiene, G. Gerard, Evaluation of glycine betaine as an inhibitor of dissolved dimethylsulphoniopropionate degradation in marine waters. Mar. Ecol. Prog. Ser. 1995, 128, 121.
Evaluation of glycine betaine as an inhibitor of dissolved dimethylsulphoniopropionate degradation in marine waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsFKmtbo%3D&md5=97cde06ba3bb2f904a3d4d43bdc090eeCAS |

[42]  A. Merzouk, M. Levasseur, M. Scarratt, S. Michaud, M. Lizotte, R. B. Rivkin, R. P. Kiene, Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the Northwest Atlantic. Mar. Ecol. Prog. Ser. 2008, 369, 1.
Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the Northwest Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOqsbvJ&md5=7bb2d8e1028ef4b05771493528410440CAS |

[43]  R. H. White, Analysis of dimethyl sulfonium compounds in marine algae. J. Mar. Res. 1982, 40, 529.
| 1:CAS:528:DyaL38Xlt1els7g%3D&md5=1657d1ce54c874e8423abb24fca257e7CAS |

[44]  R. P. Kiene, L. P. Hoffmann Williams, J. E. Walker, Seawater microorganisms have a high affinity glycine betaine uptake system which also recognizes dimethylsulfoniopropionate. Aquat. Microb. Ecol. 1998, 15, 39.
Seawater microorganisms have a high affinity glycine betaine uptake system which also recognizes dimethylsulfoniopropionate.Crossref | GoogleScholarGoogle Scholar |

[45]  R. P. Kiene, L. J. Linn, Filter type and sampling handling affect determination of organic substrate uptake by bacterioplankton. Aquat. Microb. Ecol. 1999, 17, 311.
Filter type and sampling handling affect determination of organic substrate uptake by bacterioplankton.Crossref | GoogleScholarGoogle Scholar |

[46]  S. H. Lee, Y. C. Kang, J. A. Fuhrman, Imperfect retention of natural bacterioplankton cells by glass fiber filters. Mar. Ecol. Prog. Ser. 1995, 119, 285.
Imperfect retention of natural bacterioplankton cells by glass fiber filters.Crossref | GoogleScholarGoogle Scholar |

[47]  R. Simó, S. D. Archer, C. Pedrós-Alió, L. Gilpin, C. E. Stelfox-Widdicombe, Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic. Limnol. Oceanogr. 2002, 47, 53.
Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic.Crossref | GoogleScholarGoogle Scholar |

[48]  A. N. Rellinger, R. P. Kiene, D. A. del Valle, D. J. Kieber, D. Slezak, H. Harada, J. Bisgrove, J. Brinkley, Occurrence and turnover of DMSP and DMS in the deep waters of the Ross Sea, Antarctica. Deep Sea Res. Part I Oceanogr. Res. Pap. 2009, 56, 686.
Occurrence and turnover of DMSP and DMS in the deep waters of the Ross Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVCnsb8%3D&md5=d4d26f8b58b307fa86716c84ed5c3bf7CAS |

[49]  G. V. Wolfe, Accumulation of dissolved DMSP by marine bacteria and its degradation via bactivory, in Biological and environmental chemistry of DMSP and related sulfonium compounds (Eds R. P. Kiene, P. T. Visscher, M. D. Keller, G. O. Kirst) 1996, pp. 277–291 (Plenum: New York).

[50]  M. Vila, R. Simó, R. P. Kiene, J. Pinhassi, J. M. Gonzalez, M. A. Moran, C. Pedrós-Alió, Use of microautoradiography combined with fluorescence in situ hybridization to determine dimethylsulfoniopropionate incorporation by marine bacterioplankton taxa. Appl. Environ. Microbiol. 2004, 70, 4648.
Use of microautoradiography combined with fluorescence in situ hybridization to determine dimethylsulfoniopropionate incorporation by marine bacterioplankton taxa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1eltbk%3D&md5=c7560cd963631104dda8f15e2440ee19CAS | 15294798PubMed |

[51]  S. M. Turner, G. Malin, P. S. Liss, D. S. Harbour, P. M. Holligan, The seasonal variation of dimethyl sulfide and dimethylsulfoniopropionate concentrations in nearshore waters. Limnol. Oceanogr. 1988, 33, 364.
The seasonal variation of dimethyl sulfide and dimethylsulfoniopropionate concentrations in nearshore waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkvFygt7s%3D&md5=deae18f647e05dba7cb4a990e561c36dCAS |

[52]  J. Stefels, M. Steinke, S. Turner, G. Malin, S. Belviso, Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling. Biogeochemistry 2007, 83, 245.
Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlakt7s%3D&md5=e41afa264a0a44bd66f7dcc3f8a02455CAS |

[53]  M. P. de Souza, D. C. Yoch, Comparative physiology of dimethylsulfide production by dimethylsulfoniopropionate lyase in Pseudomonas doudoroffii and Alcaligenes sp. strain M3A. Appl. Environ. Microbiol. 1995, 61, 3986.
| 1:CAS:528:DyaK2MXptFGgtLo%3D&md5=a31d3e8989b3766111b9e611c4795c76CAS | 16535162PubMed |

[54]  D. C. Yoch, J. H. Ansede, K. S. Rabinowitz, Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl. Environ. Microbiol. 1997, 63, 3182.
| 1:CAS:528:DyaK2sXlt1Wis7w%3D&md5=9046cc9f269ab7780976cf9b22ce0350CAS | 16535674PubMed |

[55]  J. Stefels, L. Dijkhuizen, Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae). Mar. Ecol. Prog. Ser. 1996, 131, 307.
Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XislGksrg%3D&md5=93855c69f1750d5e0f87b746cb73d430CAS |

[56]  G. V. Wolfe, E. B. Sherr, B. F. Sherr, Release and consumption of DMSP from Emiliania huxleyi during grazing by Oxyrrhis marina.. Mar. Ecol. Prog. Ser. 1994, 111, 111.
Release and consumption of DMSP from Emiliania huxleyi during grazing by Oxyrrhis marina..Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFKrsrY%3D&md5=b3f696f73aa5c1a5928eb347ba9f8ed5CAS |

[57]  D. Laroche, A. F. Vezina, M. Levasseur, M. Gosselin, J. Stefels, M. D. Keller, P. A. Matrai, R. L. J. Kwint, DMSP synthesis and exudation in phytoplankton: a modeling approach. Mar. Ecol. Prog. Ser. 1999, 180, 37.
DMSP synthesis and exudation in phytoplankton: a modeling approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1ertg%3D%3D&md5=d13cf057303fadfaa785a0e61751044eCAS |

[58]  S. L. Strom, G. V. Wolfe, K. J. Bright, Responses of marine planktonic protists to amino acids: feeding inhibition and swimming behavior in the ciliate Favella sp. Aquat. Microb. Ecol. 2007, 47, 107.
Responses of marine planktonic protists to amino acids: feeding inhibition and swimming behavior in the ciliate Favella sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsFyjsbs%3D&md5=8a438f8c78c5b08d6e6cde71dec67f36CAS |

[59]  A. Calbet, M. R. Landry, Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 2004, 49, 51.
Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVelt74%3D&md5=d52a95bf92d29aab6372970c87107af6CAS |

[60]  V. Saló, R. Simó, M. Vila-Costa, A. Calbet, Sulfur assimilation by Oxyrrhis marina feeding on a 35S-DMSP-labeled prey. Environ. Microbiol. 2009, 11, 3063.
Sulfur assimilation by Oxyrrhis marina feeding on a 35S-DMSP-labeled prey.Crossref | GoogleScholarGoogle Scholar | 19659553PubMed |

[61]  P. A. Matrai, M. Vernet, R. Hood, A. Jennings, E. Brody, S. Saemundsdottir, Light dependence of carbon and sulfur production by polar clones of the genus Phaeocystis.. Mar. Biol. 1995, 124, 157.
Light dependence of carbon and sulfur production by polar clones of the genus Phaeocystis..Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsV2mtA%3D%3D&md5=238b73fa5468be0ca4ece6df0d553300CAS |

[62]  R. G. Keil, D. B. Montlucon, F. G. Prahl, J. I. Hedges, Sorptive preservation of labile organic matter in marine sediments. Nature 1994, 370, 549.
Sorptive preservation of labile organic matter in marine sediments.Crossref | GoogleScholarGoogle Scholar |

[63]  L. Mayer, Surface area control of organic carbon accumulated in continental shelf sediments. Geochim. Cosmochim. Acta 1994, 58, 1271.
Surface area control of organic carbon accumulated in continental shelf sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXislGktbs%3D&md5=17027160e3bb4ff502d5163ae4754281CAS |

[64]  J. I. Hedges, J. A. Baldock, Y. Gelinas, C. Lee, M. Peterson, S. G. Wakeham, Evidence for non-selective preservation of organic matter in sinking marine particles. Nature 2001, 409, 801.
Evidence for non-selective preservation of organic matter in sinking marine particles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFCjsbY%3D&md5=d849fa85faa3510e8d6b3441007d2d73CAS | 11236989PubMed |

[65]  R. P. Kiene, Microbial cycling of organosulfur gases in marine and freshwater environments, in Cycling of reduced gases in the hydrosphere (Eds D. Adams, S. Seitzinger, P. Crill) 1996, pp. 137–151 (E. Schweitzerbart'sche Verlagsbuchhandlung (Naglele u. Obermiller): Stuttgart).

[66]  J. A. Amador, M. Alexander, R. G. Zika, Sequential photochemical and microbial degradation of organic molecules bound to humic acid. Appl. Environ. Microbiol. 1989, 55, 2843.
| 1:CAS:528:DyaK3cXms1Wg&md5=c0de97105a60712fbac919dda4f6a513CAS | 16348046PubMed |

[67]  S. Schuster, J. M. Arrieta, G. J. Herndl, Adsorption of dissolved free amino acids on colloidal DOM enhances colloidal DOM utilization but reduces amino acid uptake by orders of magnitude in marine bacterioplankton. Mar. Ecol. Prog. Ser. 1998, 166, 99.
Adsorption of dissolved free amino acids on colloidal DOM enhances colloidal DOM utilization but reduces amino acid uptake by orders of magnitude in marine bacterioplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsl2nu7c%3D&md5=da698fc16a6ffc9a3f5778d15823f8afCAS |

[68]  D. A. Gage, D. Rhodes, K. D. Nolte, W. A. Hicks, T. Leustek, A. J. L. Cooper, A. D. Hanson, A new route for the synthesis of dimethylsulfoniopropionate in marine algae. Nature 1997, 387, 891.
A new route for the synthesis of dimethylsulfoniopropionate in marine algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkt1Grsrw%3D&md5=441518b2ce8d4017694094bb4f0de178CAS | 9202120PubMed |

[69]  H. Nakamura, M. Ohtoshi, O. Sampei, Y. Akashi, A. Murai, Synthesis and absolute configuration of (+)-Gonyauline: a modulating substance of bioluminescent circadian rhythm in the unicellular alga Gonyaulax polyedra. Tetrahedron Lett. 1992, 33, 2821.
Synthesis and absolute configuration of (+)-Gonyauline: a modulating substance of bioluminescent circadian rhythm in the unicellular alga Gonyaulax polyedra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFaksb0%3D&md5=0be29d606a2792b33151be08ab855776CAS |

[70]  B. Gebser, G. Pohnert, Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs 2013, 11, 2168.
Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton.Crossref | GoogleScholarGoogle Scholar | 23774888PubMed |

[71]  R. Anderson, M. Kates, B. E. Volcani, Sulphonium analogue of lecithin in diatoms. Nature 1976, 263, 51.
Sulphonium analogue of lecithin in diatoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhtlGksA%3D%3D&md5=ca2cc2c345ec1701001b0a57b6c07db0CAS | 958463PubMed |

[72]  M. Kates, B. E. Volcani, Biosynthetic pathways for phosphatidylsulfocholine, the sulfonium analogue of phophatidylcholine, in diatoms, in Biological and environmental chemistry of DMSP and related sulfonium compounds (Eds R. P. Kiene, P. T. Visscher, M. D. Keller, G. O. Kirst) 1996, pp. 109–119 (Plenum Press: New York).

[73]  P. Bisseret, S. Ito, P. A. Tremblay, B. E. Volcani, D. Dessort, M. Kates, Occurrence of phosphatidylsulfocholine, the sulfonium analog of phosphatidylcholine in some diatoms and algae. Biochim. Biophys. Acta 1984, 796, 320.
Occurrence of phosphatidylsulfocholine, the sulfonium analog of phosphatidylcholine in some diatoms and algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXnsFentw%3D%3D&md5=ac6945804fdb28623b80a077695d0543CAS | 6542425PubMed |

[74]  D. A. Gage, A. D. Hanson, Characterization of 3-dimethylsulfoniopropionate (DMSP) and its analogs with mass spectrometry, in Biological and environmental chemistry of DMSP and related sulfonium compounds (Eds R. P. Kiene, P. T. Visscher, M. D. Keller, G. O. Kirst) 1996, pp. 29–44 (Plenum Press: New York).

[75]  T. D. Colmer, F. Corradini, G. R. Cawthray, M. L. Otte, Analysis of dimethylsulphoniopropionate (DMSP), betaines, and other organic solutes in plant tissue extracts using HPLC. Phytochem. Anal. 2000, 11, 163.
Analysis of dimethylsulphoniopropionate (DMSP), betaines, and other organic solutes in plant tissue extracts using HPLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2ju7s%3D&md5=15b03d9ea762614b7e232e1665ea2af1CAS |

[76]  A. Spielmeyer, G. Pohnert, Direct quantification of dimethylsulfoniopropionate (DMSP) with hydrophilic interaction liquid chromatography/mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2010, 878, 3238.
Direct quantification of dimethylsulfoniopropionate (DMSP) with hydrophilic interaction liquid chromatography/mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVGrtrvE&md5=cc705d452de44a6d04cd676ff7833ca5CAS | 21030323PubMed |

[77]  R. P. Kiene, Turnover of dissolved DMSP in estuarine and shelf waters from the Northern Gulf of Mexico, in Biological and environmental chemistry of DMSP and related sulfonium compounds (Eds R. P. Kiene, P. T. Visscher, M. D. Keller, G. O. Kirst) 1996, pp. 337–349 (Plenum Press: New York).

[78]  L. Guo, P. H. Santschi, T. S. Bianchi, Dissolved organic matter in estuaries of the Gulf of Mexico, in Biogeochemistry of Gulf Coast Estuaries (Eds T. S. Bianchi, J. R. Pennock, R. R. Twilley) 1999, pp. 269–299 (Wiley: New York).

[79]  M. Vila-Costa, R. P. Kiene, R. Simó, Seasonal variability of the dynamics of dimethylated sulfur compounds in a coastal northwest Mediterranean site. Limnol. Oceanogr. 2008, 53, 198.
Seasonal variability of the dynamics of dimethylated sulfur compounds in a coastal northwest Mediterranean site.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvVGjs7g%3D&md5=500934abaea61df6f1b0b44b61a0ecbeCAS |

[80]  J. Motard-Côté, A. N. Rellinger, D. J. Kieber, R. P. Kiene, Influence of the Mississippi River plume and non-bioavailable DMSP on dissolved DMSP turnover in the northern Gulf of Mexico. Environ. Chem. 2015, in press
A. N. Rellinger, D. J. Kieber, R. P. Kiene, Influence of the Mississippi River plume and non-bioavailable DMSP on dissolved DMSP turnover in the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |