A novel inhibitory interaction between dimethylsulfoniopropionate (DMSP) and the denitrification pathway

Biogeochemistry

Volumn 107, Issue 1-3, 2012, Pages 393-408

  Magalhaes C ^a   Kiene, R P ^b,c   Buchan, A ^d   Machado, A ^e   Teixeira, C ^a,e   Wiebe, W J ^f   Bordalo, A A ^a,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

^c DAUPHIN ISLAND SEA LAB   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

^e UNIVERSITY OF PORTO   (Portugal)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

Denitrification; DMSP; Estuarine sediments; Nitrogen; Organic sulfur; Ruegeria pomeroyi

Indexed keywords

ACCUMULATION RATE; ALGA; BACTERIUM; BIOACCUMULATION; BIOFILM; CHEMICAL POLLUTANT; CLIMATE CHANGE; DENITRIFICATION; DIMETHYLSULFONIOPROPIONATE; ESTUARINE SEDIMENT; EUTROPHICATION; GREENHOUSE GAS; INHIBITION; NITROGEN; NITROUS OXIDE; NUTRIENT AVAILABILITY; PRIMARY PRODUCTION; SEDIMENT POLLUTION;

PORTUGAL;

ALGAE; AVES; BACTERIA (MICROORGANISMS); RUEGERIA;

EID: 83555177633     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-010-9560-0     Document Type: Article

References (93)

1. Bange HW, Rapsomanikis S, Andreae MO (1996) Nitrous oxide in coastal waters. Glob Biogeoch Cycles 10: 197-207.
2. Barnard WR, Andreae MO, Iverson RL (1984) Dimethylsulfide and Phaeocystis pouchetii in the southeastern Bering Sea. Cont Shelf Res 3: 103-113.
3. Cantoni GL, Anderson DG (1956) Enzymatic cleavage of dimethylpropiothetin by Polysiphonia Lanosa. J Biol Chem 222: 171-177.
4. Casciotti KL, Ward BB (2005) Phylogenetic analysis of nitric oxide reductase gene homologues from aerobic ammonia-oxidizing bacteria. FEMS Microbiol Ecol 52: 197-205.
5. Charlson RJ, Lovelock JE, Andreae MO, Warren SH (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326: 655-661.
6. Clarke KR, Warwick RM (1994) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth, UK.
7. Codispoti LA, Christensen JP (1985) Nitrifcation, denitrication and nitrous oxide cycling in the eastern tropical South Pacifc. Ocean Mar Chem 16: 277-300.
8. Curson ARJ, Rogers R, Todd JD, Brearley CA, Johnston AWB (2008) Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-change gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter sphaeroides. Environ Microbiol 10: 757-767.
9. Dacey JWH, Wakeham SG, Howes BL (1984) Henry's Law constants for dimethylsulfide in freshwater and seawater. Geophys Res Lett 11: 991-994.
10. de Jonge VN, van Raaphorst W (1995) Eutrophication of the Dutch Wadden Sea (Western Europe), and estuarine area controlled by the River Rhine. In: McComb AJ (ed) Eutrophic shallow estuaries and lagoons. CRC Press, Boca Raton, pp 129-149.
11. Del Valle D, Kieber DJ, Kiene RP (2007) Depth-dependent fate of biologically-consumed dimethylsulfide in the Sargasso Sea. Mar Chem 103: 197-208.
12. Dickinson RE, Cicerone RJ (1986) Future global warming from atmospheric trace gases. Nature 319: 109-115.
13. Díez S, Lacorte S, Viana P, Barceló D, Bayona JM (2005) Survey of organotin compounds in rivers and coastal environments in Portugal 1999-2000. Environ Pollut 136: 525-536.
14. Gonçalves EPR, Boaventura RAR, Mouvet C (1992) Sediments and aquatic mosses as pollution indicators for heavy metals in the Ave River basin (Portugal). Sci Total Environ 114: 7-24.
15. González J, Kiene RP, Moran M (1999) Transformations of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the Proteobacteria. Appl Environ Microbiol 65: 3810-3819.
16. González JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA (2003) Silibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53: 1261-1269.
17. Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, Wenying Ye, González JM, Mace K, Joye SB, Kiene RP, Whitman WB, Moran MA (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314: 649-652.
18. Howard EC, Sun S, Biers EJ, Moran MA (2008) Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ Microbiol 10: 2397-2410.
19. Jickells TD (1998) Nutrient biogeochemistry in the coastal zone. Science 281: 217-222.
20. Jonkers HM, Koopmans GF, van Gemerden H (1998) Dynamics of dimethyl sulfide in a marine microbial mat. Microb Ecol 36: 93-100.
21. Joye SB, Smith SV, Hollibaugh JT, Paerl HW (1996) Estimating denitrification rates in estuarine sediments: a comparison of stoichiometric and acetylene based methods. Biogeochemistry 33: 197-215.
22. Keller MD, Bellows WK, Guillard RRL (1989) Dimethyl sulphide production in marine phytoplankton. In: Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment. American Chemical Society, Washington, DC, pp 167-182.
23. Kiene RP (1988) Dimethyl sulfide metabolism in salt marsh sediments. FEMS Microbiol Ecol 53: 71-78.
24. Kiene RP (1991) Evidence for the biological turnover of thiols in anoxic marine sediments. Biogeochemistry 13: 117-135.
25. Kiene RP (1996a) Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar Chem 54: 69-83.
26. Kiene RP (1996b) Microbial cycling of organosulfur gases in marine and freshwater environments. In: Adams D, Seitzinger S, Crill P (eds) Cycling of reduced gases in the hydrosphere. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Mitteilungen. E. Schweitzerbart'sche Verlagsbuchhandlung (Naglele u. Obermiller), Stuttgart, pp 137-151.
27. Kiene RP, Bates TS (1990) Biological removal of dimethyl sulphide from seawater. Nature 345: 702-705.
28. Kiene RP, Linn LJ (2000a) Turnover of dissolved DMSP and its relationship with bacterial production in the Gulf of Mexico. Limnol Oceanogr 45: 849-861.
29. Kiene RP, Linn LJ (2000b) The fate of dissolved dimethylsulfoniopropionate (DMSP) in seawater: tracer studies using 35S-DMSP. Geoch Cosmoch Acta 64: 797-2810.
30. Kiene RP, Service SK (1991) Decomposition of dissolved DMSP and DMS in estuarine waters: dependence on temperature and substrate concentration. Mar Ecol Prog Ser 76: 1-11.
31. Kiene RP, Taylor BF (1988) Demethylation of dimethylsulfoniopropionate and production of thiols in anoxic marine sediments. Appl Environ Microbiol 54: 2208-2212.
32. Kiene RP, Visscher PT (1987) Production and fate of methylated sulfur compounds from methionine and dimethylsulfoniopropionate in anoxic salt marsh sediments. Appl Environ Microbiol 53: 2426-2434.
33. Kiene RP, Linn LJ, González J, Moran MA, Bruton JA (1999) Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine. Bacterioplankton 65: 4549-4558.
34. Kiene RP, Linn LJ, Bruton JA (2000) New and important roles for DMSP in marine microbial communities. J Sea Res 43: 209-224.
35. Kieskamp WM, Lohse L, Epping E, Helder W (1991) Seasonal variation in denitrifcation rates and nitrous oxide fluxes in intertidal sediments of the western Wadden Sea. Mar Ecol Prog Ser 72: 145-151.
36. Kirst GO (1989) Salinity tolerance of eukaryotic marine algae. Annu Rev Plant Physiol Plant Mol Biol 40: 21-53.
37. Kirst GO, Wolff CH, Nothnagel J, Wanzek M, Ulmke R (1991) Dimethyl-sulfonioipropionate (DMSP) in ice algae and its possible biological role. Mar Chem 35: 381-388.
38. Lawrence MG (1993) An empirical analysis of the strength of the phytoplankton-dimethylsulfide-cloud-climate feedback cycle. J Geophys Res 98: 20663-20673.
39. Magalhães C, Bordalo AA, Wiebe WJ (2002) Temporal and spatial patterns of intertidal sediment-water nutrient and oxygen fluxes in the Douro River estuary, Portugal. Mar Ecol Prog Ser 233: 55-71.
40. Magalhães CM, Wiebe WJ, Joye SB, Bordalo AA (2005a) Inorganic nitrogen dynamics in intertidal rocky biofilms and sediments of the Douro River estuary (Portugal). Estuaries 28: 592-606.
41. Magalhães C, Joye SB, Moreira R, Wiebe WJ, Bordalo AA (2005b) Salinity and inorganic effects on nitrification and denitrification rates in intertidal sediments and rocky biofilms. Wat Res 39: 1783-1794.
42. Magalhães C, Teixeira C, Teixeira R, Machado A, Azevedo I, Bordalo AA (2008) Dissolved organic and inorganic carbon and nitrogen dynamics in the Douro River estuary, Portugal. Ciencias Marinas 34: 271-282.
43. Mopper K, Taylor BF (1986) Biogeochemical cycling of sulfur: thiols in marine sediments. In: Sohn M (ed) Organic marine geochemistry. American Chemical Society symposium series no. 305. American Chemical Society, Washington, D. C., pp 324-339.
44. Moran MA, Buchan A, Gonzáléz JM, Heidelberg JF, Henriksen J, Whitman WB, Kiene RP, Eisen JA, King G, Belas MR, Fuqua C, Rahe E, Sheldon W, Ye W, Carlton J, Brinkac L, Lewis M, Johri S, Weaver B, Rasko D, Paulsen I, Ren Q, Ward N (2004) Genome sequence from an ecologically significant marine bacterial taxon. Nature 432: 910-913.
45. Mucha APM, Vasconcelos TSD, Bordalo AA (2003) Macrobenthic community in the Douro estuary: relations with trace metals and natural sediment characteristics. Environ Pollut 121: 169-180.
46. Nedwell DB, Shabbeer MT, Harrison RM (1994) Dimethyl sulphide in North Sea waters and sediments. Est Coast Shelf Sci 39: 209-217.
47. Nixon SW (1981) Remineralization and nutrient cycling in coastal marine ecosystems. In: Neilson BJ, Cronin LE (eds) Estuaries and nutrients. Humana Press, Clifton, NJ, pp 111-138.
48. Nixon SW, Granger SL, Nowicki BL (1995) An assessment of the annual mass balance of carbon, nitrogen, and phosphorus in Narragansett Bay. Biogeochemistry 31: 15-61.
49. Ogilvie B, Nedwell DB, Harrison RM, Robinson A, Sage A (1997) High nitrate, muddy estuaries as nitrogen sinks: the nitrogen budget of the River Colne estuary (United Kingdom). Mar Ecol Prog Ser 150: 217-228.
50. Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55: 1919-1925.
51. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943-948.
52. Poth M, Focht DD (1985) Nitrogen-15 kinetic analysis of nitrous oxide production by Nitrosomonas europaea: an examination of nitrifierdenitrification. Appl Environ Microbiol 49: 1134-1141.
53. Przyjazny A, Janicki WA, Chrzanowski W, Staszewski R (1983) Headspace gas chromatographic determination of distribution coefficients of selected organosulfur compounds and their dependence on some parameters. J Chromatogr 280: 249-260.
54. 2O): the dominant ozone-depliting substance emitted in the 21st century. Science 326: 123-125.
55. Reed RH (1983) Measurement and osmotic significance of P dimethylsulfoniopropionate in marine macroalgae. Mar Biol Lett 34: 173-181.
56. Ritchie GAF, Nicholas DJ (1972) Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochemistry 126: 1181-1191.
57. 2O emission to the atmosphere: the estuary of the River Colne, Essex, UK. Mar Ecol Progr Ser 164: 58-71.
58. Ryther J, Dunstan W (1971) Nitrogen, phosphorus, and eutrophication in coastal marine environment. Science 171: 1008-1013.
59. Schäfer H (2007) Isolation of Methylophaga spp. from marine dimethylsulfide-degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl Environ Microbiol 73: 2580-2591.
60. Schlessinger WH (1997) Biogeochemistry: analysis of global change. Academic Press, San Diego, CA.
61. 2O. In: Dickinson RE (ed) Geophysiology of Amazonia. Vegetation and climate interactions. John Wiley and Sons, New York, pp 133-160.
62. Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecossistems: ecological and geochemical significance. Limnol Oceanogr 33: 702-724.
63. Seitzinger SP (2000) Scaling up: site-specific measurements to global-scale estimates of denitrification. In: Hobbie JE (ed) Estuarine science: a synthetic approach to research and practice. Island Press, Washington, DC, pp 211-241.
64. Seitzinger SP, Nixon SW (1983) Eutrophication and the rate of denitrifcation and N2O production in coastal marine sediments. Limnol Oceanogr 30: 1332-1339.
65. Seitzinger SP, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16: 2064-2090.
66. 2S on dissimilatory nitrate reduction. Est Coast Shelf Sci 67: 231-238.
67. Soares HMVM, Boaventura RAR, Machado AASC, Esteves da Silva JCG (1999) Sediments monitors of heavy metal contamination in the Ave river basin (Portugal): multivariate analysis of data. Environ Pollut 105: 311-323.
68. Sørensen J, Tiedje JM, Firestone RB (1980) Inhibition by sulfide of nitric and nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Appl Environ Microbiol 39: 105-108.
69. Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43: 183-197.
70. Stefels J, van Boekel WHM (1993) Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystls sp. Mar Ecol Prog Ser 97: 11-18.
71. 2O emissions from streams in the Neuse River watershed, North Carolina. Environ Sci Technol 39: 6999-7004.
72. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can, 167.
73. Sunda WG, Kieber DJ, Kiene RP et al (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418: 317-320.
74. Sundback K, Miles A, Hulth S, Pihl L, Engstrom P, Selander E, Svenson A (2003) Importance of benthic nutrient regeneration during initiation of macroalgal blooms in shallow bays. Mar Ecol Prog Ser 246: 115-126.
75. Taylor BF, Gilchrist DC (1991) New routes for aerobic biodegradation of dimethylsulfoniopropionate. Appl Environ Microbiol 57: 3581-3584.
76. Todd JD, Rogers R, Li YG, Wexler M, Bond PL, Sun L, Curson ARJ, Malin G, Steinke M, Johnston AWB (2007) Structural and regulatory genes required to make the gas dimethyl sulphide in bacteria. Science 315: 665-669.
77. Todd JD, Curson ARJ, Dupont CL, Nicholson P, Johnston AWB (2009) The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ Microbiol 11: 1376-1385.
78. Trimmer M, Nedwell DB, Sivyer DB, Malcolm SJ (2000) Seasonal organic mineralization and denitrifcation in intertidal sediments and is relationship to the abundance of Enteromorpha sp. and Ulva sp. Mar Ecol Prog Ser 203: 67-80.
79. Turner SM, Malin G, Liss PS, Harbour DS, Holligan PM (1988) The seasonal variation of dimethyl sulfide and dimethylsulfoniopropionate concentrations in nearshore waters. Limnol Oceanogr 33: 364-375.
80. Tyler AC, McGlathery KJ, Anderson IC (2001) Macroalgae mediation of dissolved organic nitrogen fluxes in a temperate coastal lagoon. Est Coast Shelf Sci 53: 155-168.
81. Vallina SM, Simó R (2007) Strong relationship between DMS and the solar radiation dose over the global surface ocean. Science 315: 506-508.
82. van Duyl FC, Gieskes WWC, Kop AJ, Lewis WE (1998) Biological control of short-term variations in the concentration of DMSP and DMS during a Phaecystis spring bloom. J Sea Res 40: 221-231.
83. Vieira MEC, Bordalo AA (2000) The Douro estuary (Portugal): a mesotidal salt wedge. Oceanol Acta 23: 585-594.
84. Vila-Costa M, Del Valle D, Gonzalez JM, Slezak D, Kiene RP, Sanchez O, Simó R (2006) Phylogenetic identification and metabolism of marine dimethylsulfide-consuming bacteria. Environ Microbiol 8: 2189-2200.
85. Visscher PT, van Gemerden H (1991) Production and consumption of dimethylsulfoniopropionate in marine microbial mats. Appl Environ Microbiol 57: 3237-3242.
86. White RH (1982) Analysis of dimethylsulfonium compounds in marine algae. J Mar Res 40: 529-536.
87. Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role pf nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33: 1723-1732.
88. Yang G-P, Tsunogai S, Watanabe S (2005) Biogeochemistry of DMSP in the surface microlayer and subsurface seawater of Funka Bay, Japan. J Oceanogr 61: 69-78.
89. Yi H, Lim YW, Chun J (2007) Taxonomic evaluation of the genera Ruegeria and Silicibacter: a proposal to transfer the genus Silicibacter Petursdottir and Kristjansson 1999 to the genus Ruegeria Uchino et al. 1999. Int J Syst Evol Microbiol 57: 815-819.
90. Yoch DC (2002) Dimethylsulfoniopropionate: Its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microbiol 68: 5804-5815.
91. Yoshinari T, Knowles R (1976) Acetylene inhibition of nitrous oxide reduction by denitrifying bacteria. Biochem Biophys Res Commun 69: 705-710.
92. Zar JH (1996) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ, USA.
93. Zubkov MV, Fuchs BM, Archer SD, Kiene RP, Amann R, Burkill PH (2002) Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea. Deep-Sea Res 49: 3017-3038.