Exopolysaccharides produced by bacteria isolated from the pelagic Southern Ocean - Role in Fe binding, chemical reactivity, and bioavailability

Marine Chemistry

Volumn 123, Issue 1-4, 2011, Pages 88-98

  Hassler, C S ^a,d   Alasonati, E ^b   Mancuso Nichols, C A ^c   Slaveykova, V I ^b  

^a BUREAU OF METEOROLOGY   (Australia)

^b EPFL   (Switzerland)

^c CSIRO   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

AFlFFF; Bioavailability; EPS; Fe; Voltammetry

Indexed keywords

BACTERIUM; BIOAVAILABILITY; EUPHOTIC ZONE; FUNCTIONAL GROUP; IRON; MARINE ECOSYSTEM; METAL BINDING; NUTRIENT LIMITATION; POLYSACCHARIDE; POPULATION SIZE; PRIMARY PRODUCTION; REACTIVATION; SOLUBILITY; SPECIATION (CHEMISTRY);

SOUTHERN OCEAN;

PSEUDOALTEROMONAS SP.;

EID: 78650308181     PISSN: 03044203     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.marchem.2010.10.003     Document Type: Article

References (77)

1. Alasonati E., Stolpe B., Benincasa M.-A., Hassellöv M., Slaveykova V.I. Asymmetrical flow field-flow fractionation-multidetection system as a tool for studying metal-alginate interactions. Environ. Chem. 2006, 3:192-198.
2. Alasonati E., Benincasa M.-A., Slaveykova V.I. Asymmetrical flow field-flow fractionation coupled to multi-angle light scattering detector: optimization of crossflow rate, carrier characteristics and injected mass in alginate separation. J. Sep. Sci. 2007, 30(14):2332-2340.
3. Alasonati E., Dubascoux S., Lespes G., Slaveykova V.I. Assessment of metal - extracellular polymeric substances interactions by asymmetrical flow field-flow fractionation coupled to inductively coupled plasma-mass spectrometry. Environ. Chem. 2010, 7:215-223.
4. Aluwihare L.I., Repeta D.J., Chen R.F. A major biopolymeric component to dissolved organic carbon in surface seawater. Nature 1997, 387:166-169.
5. Becquevort S., Lancelot C., Schoemann V. The role of Fe in the bacterial degradation of organic matter derived from Phaeocystis antarctica. Biogeochemistry 2007, 83:119-135.
6. Benner R., Pakulski J.D., MacCarthy M., Hedges J.I., Hatcher P.G. Bulk chemical characteristics of dissolved organic matter in the ocean. Science 1992, 255:1561-1564.
7. Blumenkrantz N., Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal. Biochem. 1973, 54:484-489.
8. Boyd P.W., Jickells T., Law C.S., Blain S., Boyle E.A., Buesseler K.O., Coale K.H., Cullen J.J., de Baar H.J.W., Follows M., Harvey M., Lancelot C., Levasseur M., Pollard R., Rivkin R.B., Sarmiento J., Schoemann V., Smetacek V., Takeda S., Tsuda A., Turner S., Watson A.J. Mesoscale iron enrichment experiments 1993-2005: synthesis and future directions. Science 2007, 315:612-617.
9. Boyé M., van den Berg C.M.G. Iron availability and the release of iron-complexing ligands by Emiliania huxleyi. Mar. Chem. 2000, 70:277-287.
10. Boyé M., van den Berg C.M.G., De Jong J.T.M., Leach H., Croot P., De Baar H.J.W. Organic complexation of iron in the Southern Ocean. Deep Sea Res. I 2001, 48:1477-1497.
11. Busnel J., Degoulet C., Nicolai T., Woodley W., Patin P. Multiangle light scattering angle and viscosimetric detector for size-exclusion chromatography. J Phys III France 1995, 5:1501-1512.
12. Castruita M., Shaked Y., Elmegreen L.A., Stiefel E.I., Morel F.M.M. Availability of iron from iron-storage proteins to marine phytoplankton. Limnol. Oceanogr. 2008, 53:890-899.
13. Chen M., Wang W.-X., Guo L. Phase partitioning and solubility of iron in natural seawater controlled by dissolved organic matter. Glob. Biogeochem. Cycles 2004, 18:GB4013. 10.1029/2003GB002160.
14. Croot P.L., Johansson M. Determination of iron speciation by cathodic stripping voltammetry in seawater using the competing ligand 2-(2-thiazolylazo)-p-cresol (TAC). Electroanalysis 2000, 12:565-576.
15. Cullen J., Bergquist B., Moffett J. Thermodynamic characterization of the partitioning of iron between soluble and colloidal species in the Atlantic Ocean. Mar. Chem. 2006, 98:295-303.
16. De Jong J., Schoemann V., Mattielli N., Lannuzel D. High-accuracy determination of iron in seawater by isotope dilution multiple collector inductively coupled plasma mass spectrometry (ID-MC-ICP-MS) using nitrilotriacetic acid chelating resin for pre-concentration and matrix separation. Anal. Chim. Acta 2008, 623:126-139. 10.1016/j.aca.2008.06.013.
17. Decho A.W. Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr Mar Biol Annu Rev 1990, 73-153. Aberdeen Univ Press, Aberdeen. M. Barnes (Ed.).
18. Ding Q., Jiang S., Zhang L., Wu C. Laser light-scattering studies of pachyman. Carbohydr. Res. 1998, 308:339-343.
19. Engel A., Thoms S., Riebesell U., Rochelle-Newall E., Zondervan I. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 2004, 428:929-932.
20. Filisetti-Cozzi T.M.C.C., Carpita N.C. Measurement of uronic acid without interference of neutral sugars. Anal. Biochem. 1991, 197:157-162.
21. Freire-Nordi C.S., Vieira A.A.H., Nakaie C.R., Nascimento O.R. The metal binding capacity of Anabaena spiroides extracellular polysaccharides: an EPR study. Process Biogeochemistry 2005, 40:2215-2224.
22. Gledhill M., van den Berg C.M.G. Determination of complexation of iron(III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar. Chem. 1994, 47:41-54.
23. Gledhill M., McCormack P., Ussher S., Achterberg E.P., Mantoura R.F.C., Worsfold P.J. Production of siderophore type chelates by mixed bacterioplankton populations in nutrient enriched seawater incubations. Mar. Chem. 2004, 88:75-83.
24. Gyurcsik B., Nagy L. Carbohydrates as ligands: coordination equilibria and structure of the metal complexes. Coord. Chem. Rev. 2000, 203:81-149.
25. Hassler C.S., Schoemann V. Discriminating between intra- and extracellular metals using chemical extraction - the case of Fe. Limnol. Oceanogr. Meth. 2009, 7:479-489.
26. Hassler C.S., Schoemann V. Bioavailability of organically bound Fe to model phytoplankton of the Southern Ocean. Biogeosciences 2009, 6:2281-2296.
27. Hassler C.S., Havens S.M., Bullerjahn G.S., McKay R.M.L., Twiss M.R. Iron speciation in western Lake Superior measured using combined physical, chemical and biological assessment. Limnol. Oceanogr. 2009, 54:987-1001.
28. Hoagland K.D., Rosowski J.R., Gretz M.R., Roemer S.C. Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J. Phycol. 1993, 29:537-566.
29. Hudson R.J.M., Morel F.M.M. Iron transport in marine phytoplankton: kinetics of cellular and medium coordination reactions. Limnol. Oceanogr. 1990, 35:1002-1020.
30. Hung C.-C., Guo L., Schultz G.E., Pinckney J.L., Santschi P.H. Production and flux of carbohydrate species in the Gulf of Mexico. Glob. Biogeochem. Cycles 2003, 17:1055. 10.1029/2002GB001988.
31. Hutchins D.A., Witter A.E., Butler A., Luther III G.W. Competition among marine phytoplankton for different chelated iron species. Nature 1999, 400:858-861.
32. Ibisanmi E., Sander S.G., Boyd P.W., Bowie A.R., Hunter K.A., in press. Vertical distributions of iron(III) complexing ligands in the Southern Ocean. Deep Sea Res II. (accepted 26 August 2009).
33. Kirchman D.L., Meon B., Cottrell M.T., Hutchins D.A., Weeks D., Bruland K.W. Carbon versus iron limitation of bacterial growth in the California upwelling regime. Limnol. Oceanogr. 2000, 45:1681-1688.
34. Lannuzel D., Remenyi T., Lam P., Townsend A., Ibisanmi E., Butler E., Wagener T., Schoemann V., Bowie A.R., in press. Distributions of dissolved and particulate iron in the sub-Antarctic and Polar Frontal Southern Ocean (Australian sector). Deep Sea Res II. (accepted 17 December 2009).
35. Lijour Y., Gentric E., Deslandes E., Guezennec J. Estimation of the sulfate content of hydrothermal vent bacterial polysaccharides by Fourier Transform Infrared Spectroscopy. Anal. Biochem. 1994, 220:244-248.
36. Maldonado M.T., Strzepek R.F., Sander S., Boyd P.W. Acquisition of Fe bound to strong organic complexes, with different Fe binding groups and photochemical reactivities, by plankton communities in Fe-limited subantarctic waters. Glob. Biogeochem. Cycles 2005, 19:GB4S23. 10.1029/2005GB002481.
37. Mancuso Nichols C., Garon S., Bowman J.P., Raguénès G., Guezennec J. Production of exopolysaccharides by Antarctic marine bacterial isolates. J. Appl. Microbiol. 2004, 96:1057-1066.
38. Mancuso Nichols C., Lardière S.G., Bowman J.P., Nichols P.D., Gibson J., Guézennec J. Chemical characterization of exopolysaccharides from Antarctic marine bacteria. Microb. Ecol. 2005, 49:578-589.
39. Marchetti A., Parker M.S., Moccia L.P., Lin E.O., Arrieta A.L., Ribalte F., Murphy M.E.P., Maldonado M.T., Armbrust E.V. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 2009, 457:467-470.
40. Mawji E., Gledhill M., Milton J.A., Tarran G.A., Ussher S., Thompson A., Wolff G.A., Worsfold P.J., Achterberg E.P. Hydroxamate siderophores: occurrence and importance in the Atlantic ocean. Environ. Sci. Technol. 2008, 42:8675-8680.
41. Mioni C.E., Handy S.M., Ellwood M.J., Twiss M.R., McKay R.M.L., Boyd P.W., Wilhelm S.W. Tracking changes in bioavailable Fe within high-nitrate low-chlorophyll oceanic waters: a first estimate using a heterotrophic bacterial bioreporter. Glob. Biogeochem. Cycles 2005, 19:GB4S25. 10.1029/2005GB002476.
42. Morel F.M.M., Rueter J.J.G., Anderson D.M., Guillard R.R.L. AQUIL: a chemically defined phytoplankton culture medium for trace metal studies. J. Phycol. 1979, 15:135-141.
43. Morel F.M.M., Kustka A.B., Shaked Y. The role of unchelated Fe in the Fe nutrition of phytoplankton. Limnol. Oceanogr. 2008, 53:400-404.
44. Morillo Pérez J.A., Garcia-Ribera R., Quesada T., Aguilera M., Ramos-Cormenzana A., Monteoliva-Sanchez M. Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J. Microbiol. Biotechnol. 2008, 24:2699-2704.
45. Nagy L., Yamaguchi T., Yoshida K. Application of EXAFS and XANES methods in coordination chemistry of carbohydrates and their derivatives. Struct. Chem. 2003, 14:77-84.
46. Obernosterer I., Christaki U., Lefėvre D., Catala P., van Wambeke F., Lebaron P. Rapid bacterial mineralization of organic carbon produced during a phytoplankton bloom induced by natural iron fertilisation in the Southern Ocean. Deep Sea Res. II 2008, 55:777-789.
47. Öztürk M., Croot P.L., Bertilsson S., Abrahamsson K., Karlson B., David R., Fransson A., Sakshaug E. Iron enrichment and photoreduction of iron under UV and PAR in the presence of hydroxycarboxylic acid: implications for phytoplankton growth in the Southern Ocean. Deep Sea Res. II 2004, 51:2841-2856.
48. Panagiotopoulos C., Repeta D.J., Johnson C.G. Characterization of methyl sugars, 3-deoxysugars and methyl deoxysugars in marine high molecular weight dissolved organic matter. Org. Geochem. 2007, 38:884-896.
49. Passow U. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography 2002, 55:287-333.
50. Plude J.L., Parker D.L., Schommer O.J., Timmerman R.J., Hagstrom S.A., Joers J.M., Hnasko R. Chemical characterization of polysaccharide from the slime layer of the Cyanobacterium Microcystis flos-aquae C3-40. Appl. Environ. Microbiol. 1991, 57:1696-1700.
51. Price N.M., Harrison G.I., Hering J.G., Hudson R.J., Nirel P.M.V., Palenik B., Morel F.M.M. Preparation and chemistry of the artificial algal culture medium AQUIL. Biol. Oceanogr. 1988/1989, 6:443-461.
52. Raguénès G., Pignet P., Gauthier G., Peres A., Christen R., Rougeaux H., Barbier G., Guezennec J. Description of a new polymer-secreting bacterium from a deep-sea hydrothermal vent, Alteromonas macleodii subsp. fijiensis, and preliminary characterization of the polymer. Appl. Environ. Microbiol. 1996, 62:67-73.
53. Rendleman J.A. Metal-polysaccharide complexes-Part 1. Food Chem. 1978, 3:47-79.
54. Rijkenberg M.J.A., Gerringa L.J.A., Timmermans K.R., Fischer A.C., Kroon K.J., Buma A.G.J., Wolterbeek B.T., de Baar H.J.W. Enhancement of the reactive iron pool by marine diatoms. Mar. Chem. 2008, 109:29-44.
55. Rimington C. The carbohydrate complex of the serum proteins. II: improved method for isolation and redetermination of structure, isolation of glucosaminodimannose from proteins of ox blood. Biochem. J. 1931, 25:1062-1071.
56. Rose A.L., Salmon T.P., Lukondeh T., Neilan B.A., Waite T.D. Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lynbya majuscule. Environ. Sci. Technol. 2005, 39:3708-3715.
57. Rougeaux H., Guezennec J., Carlson R.W., Kervarec N., Pichon R., Talaga P. Structural determination of the exopolysaccharide of Pseudoalteromonas strain HYD 721 isolated from a deep-sea hydrothermal vent. Carbohydr. Res. 1999, 315:273-285.
58. Roy E.G., Wells M.L., King D.W. Persistence of iron(II) in surface waters of the western subarctic Pacific. Limnol. Oceanogr. 2008, 53:89-98.
59. Rue E.L., Bruland K.W. Complexation of iron(III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar. Chem. 1995, 50:117-138.
60. Santschi P.H., Hung C.-C., Schultz G., Alvarado-Quiroz N., Guo L., Pinckney J., Walsh I. Control of acid polysaccharide production and 234Th and POC export fluxes by marine organisms. Geophys. Res. Lett. 2003, 30:1044. 10.1029/2002GL016046.
61. Sarthou G., Timmermans K.R., Blain S., Treguer P. Growth physiology and fate of diatoms in the ocean: a review. J. Sea Res. 2005, 53:25-42.
62. Scherrer R., Berlin E., Gerhardt P. Density, porosity, and structure of dried cell walls isolated from Bacillus megaterium and Saccharomyces cerevisiae. J. Bacteriol. 1977, 129:1162-1164.
63. Schimpf M., Caldwell K., Giddings J.C. Field-flow fractionation handbook 2000, John Wiley & Sons, Ltd, New York.
64. Schoemann V., Becquevort S., Stefels J., Rousseau V., Lancelot C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res. 2005, 53:43-66.
65. Smith P.K., Krohn R.I., Hermanson G., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
66. Sreeram K.J., Yamini Shrivastava H., Nair B.U. Studies on the nature of interaction of iron(III) with alginates. Biochim. Biophys. Acta 2004, 1670:121-125.
67. Steen A.D., Hamdan L.J., Arnosti C. Dynamics of dissolved carbohydrates in the Chesapeake Bay: insights from enzyme activities, concentrations, and microbial metabolism. Limnol. Oceanogr. 2008, 53:936-947.
68. Steigenberger S., Statham P.J., Völker C., Passow U. The role of polysaccharides and diatom exudates in the redox cycling of Fe and the photoproduction of hydrogen peroxide in coastal seawaters. Biogeosci. Discuss. 2009, 6:7789-7819.
69. Tanford C. Physical chemistry of macromolecules 1961, Wiley, New York.
70. Tang D., Morel F.M.M. Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Mar. Chem. 2006, 98:18-30.
71. Town R.M., van Leeuwen H.P. Measuring marine iron(III) complexes by CLE-AdSV. Environ. Chem. 2005, 2:80-84.
72. van Oijen T., Veldhuis M.J.W., Gorbunov M.Y., Nishioka J., van Leeuwe M.A., de Baar H.J.W. Enhanced carbohydrate production by Southern ocean phytoplankton in response to in situ iron fertilization. Mar. Chem. 2005, 93:33-52.
73. Verdugo P., Alldredge A.L., Azam F., Kirchmand D.L., Passow U., Santschi P.H. The oceanic gel-phase: a bridge in the DOM-POM continuum. Mar. Chem. 2004, 92:67-85.
74. Vong L., Laës A., Blain S. Determination of iron-porphyrin-like complexes at nanomolar levels in seawater. Anal. Chim. Acta 2007, 588:237-244.
75. Wang D., Henrichs S.M., Guo L. Distributions of nutrients, dissolved organic carbon and carbohydrates in the western Arctic Ocean. Cont. Shelf Res. 2006, 26:1654-1667.
76. Witter A.E., Luther G.W. Variation in Fe-organic complexation with depth in the Northwester Atlantic Ocean as determined using a kinetic approach. Mar. Chem. 1998, 62:241-258.
77. Worms I.A., Al-Gorani Szigeti Z., Dubascoux S., Lespes G., Traber J., Sigg L., Slaveykova V.I. Colloidal organic matter from wastewater treatment plant effluents: characterization and role in metal distribution. Water Res. 2010, 44:340-350.