Dissolved phosphorus pools and alkaline phosphatase activity in the euphotic zone of the western North Pacific Ocean

Frontiers in Microbiology

Volumn 3, Issue MAR, 2012, Pages

  Suzumura, Masahiro ^a   Hashihama, Fuminori ^b   Yamada, Namiha ^a   Kinouchi, Shinko ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Alkaline phosphatase activity; Dissolved inorganic phosphorus; Dissolved organic phosphorus; Euphotic zone; North pacific ocean; Phosphorus

Indexed keywords

EID: 84871998165     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00099     Document Type: Article

References (61)

1. Ammerman, J. B. (1991). "Role of ecto-phosphohydrolases in phosphorus regeneration in estuarine and coastal ecosystems", in Microbial Enzymes in Aquatic Environments, ed. R. J. Chrost (NewYork: Springer-Verlag), 165-186.
2. Björkman, K. M., and Karl, D. M. (1994). Bioavailability of inorganic and organic phosphorus compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Mar. Ecol. Prog. Ser. 111, 265-273.
3. Björkman, K. M., and Karl, D. M. (2003). Bioavailability of dissolved organic phosphorus in the euphotic zone at station ALOHA, North Pacific subtropical gyre. Limnol. Oceanogr. 48, 1049-1057.
4. Björkman, K. M., and Karl, D. M. (2005). Presence of dissolved nucleotides in the North Pacific Subtropical Gyre and their role in cycling of dissolved organic phosphorus. Aquat. Microb. Ecol. 39, 193-203.
5. Cavender-Bares, K. K., Karl, D. M., and Chisholm, S. W. (2001). Nutrient gradients in the western North Atlantic Ocean: relationship to microbial community structure and comparison to patterns in the Pacific Ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 48, 2373-2395.
6. Cembella, A. D., Antia, N. J., and Harrison, P. J. (1984). The utilization of inorganic and organic phosphorus-compounds as nutri ents by eukaryotic microalgae-a multidisciplinary perspective. Part 1. Crit. Rev. Microbiol. 10, 317-391.
7. Chichester, K. D., Sebastián, M., Ammerman, J. W., and Colyer, C. L. (2008). Enzymatic assay of marine bacterial phosphatases by capillary electrophoresis with laser-induced fluorescence detection. Electrophoresis 29, 3810-3816.
8. Cotner, J. B., Ammerman, J. W., Peele, E. R., and Bentzen, E. (1997). Phosphorus-limited bacterio-plankton growth in the Sargasso Sea. Aquat. Microb. Ecol. 13, 141-149.
9. Duhamel, S., Björkman, K. M., Van Wambeke, F., Moutin, T., and Karl, D. M. (2011). Characterization of alkaline phosphatase activity in the North and South Pacific subtropical gyres: implications for phosphorus cycling. Limnol Oceanogr. 56, 1244-1254.
10. Duhamel, S., Dyhrman, S. T., and Karl, D. M. (2010). Alkaline phosphatase activity and regulation in the North Pacific subtropical gyre. Limnol. Oceanogr. 55, 1414-1425.
11. Dyhrman, S. T., Ammerman, J. W., and Van Mooy, B. A. S. (2007). Microbes and the marine phosphorus cycle. Oceanography 20,110-116.
12. Dyhrman, S. T., and Palenik, B. (2003). Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi. J. Plankton Res. 25,1215-1225.
13. Dyhrman, S. T., and Ruttenberg, K. C. (2006). Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus rem-ineralization. Limnol Oceanogr. 51, 1381-1390.
14. Dyhrman, S. T., Webb, E. A., Anderson, D. M., Moffett, J. W., and Waterbury, J. B. (2002). Cell-specific detection of phosphorus stress in Trichodesmium from the Western North Atlantic. Limnol. Oceanogr. 47,1832-1836.
15. Feuillade, M., and Dorioz, J. M. (1992). Enzymatic release of phosphate in sediments of various origins. Water Res.26, 1195-1201.
16. González-Gil, S., Keafer, B. A., Jovine, R. V M., Aguilera, A., Lu, S., and Anderson, D. M. (1998). Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton. Mar. Ecol. Prog. Ser. 164, 21-35.
17. Hansen, H. P., and Koroleff, E (1999). "Determination of nutrients", in Methods of Seawater Analysis, eds K. Grasshoff, K. Lremling, and M. Ehrhardt (Weinheim: Wiley-VCH), 159-228.
18. Hashihama, F., Furuya, K., Kitajima, S., Takeda, S., Takemura, T., and Kanda, J. (2009). Macro-scale exhaustion of surface phosphate by dinitrogen fixation in the western North Pacific. Geophys. Res. Lett. 36, L03610.
19. Hashihama, F., Horimoto, N., Kanda, J., Furuya, K., Ishimaru, T., and Saino, T. (2008). Temporal variation in phytoplankton composition related to water mass properties in the central part of Sagami Bay. J. Oceanogr. 64, 23-37.
20. Hoppe, H.-G. (1983). Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar. Ecol. Prog. Ser. 11,299-308.
21. Hoppe, H.-G. (2003). Phosphatase activity in the sea. Hydrobiology 493, 187-200.
22. Hoppe, H.-G., and Ullrich, S. (1999). Profiles of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone. Aquat. Microb. Ecol. 19, 139-148.
23. Karl, D. M. (2000). Phosphorus, the staff of life. Nature 406, 31-32.
24. Karl, D. M. (2007). The marine phosphorus cycle, in Manual of Environmental Microbiology, ed. C. J. Hurst (Washington, DC: ASM Press), 523-539.
25. Karl, D. M., and Björkman, K. M. (2002). "Dynamics of DOP", in Bio-geochemistry of Marine Dissolved Organic Matter, eds D. A. Hansell and C. A. Carlson (Boston, MA: Elsevier Science), 249-366.
26. Karl, D.M., and Tien, G. (1997). Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar. Chem. 56, 77-96.
27. Koike, I., and Nagata, T. (1997). High potential activity of extracellular alkaline phosphatase in deep waters of the central Pacific. Deep Sea Res. Part II Top. Stud. Oceanogr. 44, 2283-2294.
28. Kolowith, L. C., Ingall, E. D., and Benner, R. (2001). Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46, 309-320.
29. Kuznetsova, M., and Lee, C. (2001). Enhanced extracellular enzymatic peptide hydrolysis in the sea-surface microlayer. Mar. Chem. 73, 319-332.
30. Labry, C., Delmas, D., and Herb-land, A. (2005). Phytoplankton and bacterial alkaline phosphatase activities in relation to phosphate and DOP availability within the Gironde plume waters (Bay of Biscay). J. Exp. Mar. Biol. Ecol. 318, 213-225.
31. Lebo, M. E. (1990). Phosphate uptake along a coastal estuary. Limnol. Oceanogr. 35,1279-1289.
32. Lomas, M. W., Burke, A. L., Lomas, D. A., Bell, D. W., Shen, C., Dyhrman, S. T., and Ammerman, J. W (2010). Sargasso Sea phosphorus biogeo-chemistry: an important role fordis-solved organic phosphorus (DOP). Biogeosciences 7, 695-710.
33. Luo, H., Benner, R., Long, R. A., and Hu, J. (2009). Subcellular localization of marine bacterial alkaline phos-phatases. Proc. Natl. Acad. Sci. U.S.A. 160,21219-21233.
34. Marine Information Service Office, Oceanographic Data and Information Division, Hydrographic and Oceanographic Department, Japan Coast Guard (2010). Quick Bulletin of Ocean Conditions No. 132. Available at: http://www1.kaiho.mlit.go.jp/KANKYO/KAIYO/qboc/2010cal/Jul/20100715.html
35. Mather, R., Reynolds, S., Wolff, G., Williams, R. G., Torres-Valdes, S., Woodward, E. M. S., Landolfi, A., Pan, X., Sanders, R. W., and Achter-berg, E. (2008). Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres. Nat. Geosci. 1, 439-443.
36. Moutin, T., Karl, D. M., Duhamel, S., Rimmelin, P., Raimbault, P., Van Mooy, B. A. S., and Claustre, H. (2008). Phosphate availability and the ultimate control of new nitrogen input by nitrogen fixation in the tropical Pacific Ocean. Biogeosciences 5,95-109.
37. Moutin, T., Van Den Broeck, N., Beker, B., Dupouy, C., Rimmelin, P., and Le Bouteiller, A. (2005). Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean. Mar. Ecol. Prog. Ser. 297, 15-21.
38. Nausch, M. (1998). Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea). Aquat. Microb. Ecol. 16, 87-94.
39. Orrett, K., and Karl, D. M. (1987). Dissolved organic phosphorus production in surface seawaters. Limnol. Oceanogr. 32, 383-395.
40. Paytan, A., and McLaughlin, K. (2007). The oceanic phosphorus cycle. Chem. Rev. 107, 563-576.
41. Porter, K. G., and Feig, Y. S. (1980). The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943-948.
42. Ridal, J. J., and Moore, R. M. (1990). A re-examination of the measurement of dissolved organic phosphorus in seawater. Mar. Chem. 29, 19-31.
43. Rivkin, R., and Swift, E. (1980). Characterization of alkaline phosphatase and organic phosphorous utilization in the oceanic dinoflagellate, Pyrocystis noctiluca. Mar. Biol. 61, 1-8.
44. Sebastián, M., Arístegui, J., Montero, M. E, and Niell, F. X. (2004). Kinetics of alkaline phosphatase activity, and effect of phosphate enrichment: a case study in the NW African upwelling region. Mar. Ecol. Prog. Ser. 270, 1-13.
45. Sebastián, M., and Niell, E X. (2004). Alkaline phosphatase activity in marine oligotrophic environments: implications of single-substrate addition assays for potential activity estimations. Mar. Ecol. Prog. Ser. 277,285-290.
46. Strickland, J. D. H., and Parsons, T. R. (1972). A Practical Handbook of Seawater Analysis, 2nd Edn. Ottawa: Fisheries Research Board of Canada.
47. Suzuki, R., and Ishimaru, T. (1990). An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. J. Oceanogr. 46, 190-194.
48. Suzumura, M., and Ingall, E. D. (2004). Distribution and dynamics of various forms of phosphorus in seawater: insights from field observations in the Pacific Ocean and a laboratory experiment. Deep Sea Res. Part I Oceanogr. Res. Pap. 51, 113-1,130.
49. Suzumura, M., Ishikawa, K., and Ogawa, H. (1998). Characterization of dissolved organic phosphorus in coastal seawater using ultrafiltration and phosphohydrolytic enzymes. Limnol. Oceanogr. 43, 1553-1564.
50. Tanaka, T., Henriksen, P., Lignell, R., Olli, K., Seppälä, J., Tamminen, T., and Thingstad, T. F. (2006). Specific affinity for phosphate uptake and specific alkaline phosphatase activity as diagnostic tools for detecting phosphorus-limited phytoplankton and bacteria. Estuaries Coast 29, 1226-1241.
51. Tanaka, T., Thingstad, T. F., Christaki, U., Colombet, J., Cornet-Barthaux, V., Courties, C., Grattepanche, J.-D., Lagaria, A., Nedoma, J., Oriol, L., Psarra, S., Pujo-Pay, M., and Van Wambeke, E. (2011). Lack of P-limitation of phytoplankton and heterotrophic prokaryotes in surface waters of three anticyclonic eddies in the stratified Mediterranean Sea. Biogeosciences 8, 525-538.
52. Thingstad, T. F. (2005). Simulating the response to phosphate additions in the oligotrophic eastern Mediterranean using an idealized four-member microbial food web model. Deep Sea Res. Part II Top. Stud. Oceanogr. 52, 3074-3089.
53. Thingstad, T. F., Krom, M. D., Man-toura, R. F. C., Flaten, G. A. F., Groom, S., Herut, B., Kress, N., Law, C. S., Pasternak, A., Pitta, P., Psarra, S., Rassoulzadegan, F., Tanaka, T., Tselepides, A., Wass-mann, P., Woodward, E. M. S., Wex-els Riser, C.,Zodiatis, G.,and Zohary, T. (2005). Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309, 1068-1071.
54. Thingstad, T. F., Skojoldal, E. F., and Bohne, R. A. (1993). Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway. Mar. Ecol Prog. Ser. 99, 239-259.
55. Thingstad, T. F., Zweifel, U. L., and Rassoulzadegan, E (1998). P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol. Oceanogr. 43, 88-94.
56. Tholosan, O., Lamy, F., Garcin, J., Polychronaki, Y., and Bianchi, A. (1999). Biphasic extracellular proteolytic enzyme activity in benthic water and sediment in the northwestern Mediterranean Sea. Appl. Environ. Microbiol. 65, 1619-1626.
57. Turner, B. L., McKelvie, I. D., and Haygarth, P. M. (2002). Characterisation of water-extractable soil organic phosphorus by phosphatase hydrolysis. Soil Biol Biochem. 34, 27-35.
58. Van Wambeke, F., Christaki, U., Gian-nakourou, A., Moutin, T., and Souvemerzoglou, K. (2002). Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb. Ecol. 43, 119-133.
59. White, A. E. (2009). New insights into bacterial acquisition of phosphorus in the surface ocean. Proc. Natl. Acad. Sci. U.S.A. 106, 21013-21014.
60. Wu, J., Sunda, W., Boyle, E., and Karl, D. (2000). Phosphate depletion in the western North Atlantic Ocean. Science 289, 759-762.
61. Young, C. L., and Ingall, E. D. (2010). Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat. Geochem. 16, 563-574.