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Chapter 43 : The Marine Phosphorus Cycle

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Abstract:

Field investigation of the marine phosphorus (P) cycle requires the use of a variety of methods to measure the ambient concentrations of total dissolved and particulate (both organic and inorganic) matter to assess local inventories of P and to estimate P fluxes. The latter include the delivery to and losses from the ecosystem in question and the rates of microbial P uptake and microbial decomposition of P-containing organic matter. In seawater, the most commonly measured P pools are (i) soluble reactive P (SRP), (ii) total dissolved P (TDP), and (iii) particulate P (PP). The structure and function of the marine P cycle are both time and space (vertical and horizontal) variable; a comprehensive understanding will require a four-dimensional resolution of the key P inventories and fluxes. Measurements of P-ATP in marine ecosystems date back to the classic work of Holm-Hansen and Booth, who developed the theoretical basis for its use in total microbial biomass estimation. Marine microorganisms assimilate D-ATP for P and for purine salvage. The central portions of all major ocean basins are characterized as “marine deserts” because of the small standing stocks of photosynthetic organisms and small nutrient inventories.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43

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Bacteria and Archaea
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Mesopelagic Zone
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Marine Ecosystem
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Horizontal Gene Transfer
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Figures

Image of FIGURE 1
FIGURE 1

Schematic representation of the open ocean P cycle showing the major pools (boxes) and transformations and fluxes (arrows). The large box in the center, TDP, is comprised of phosphate (P), inorganic polyphosphate (poly-P), and DOP. The last group is usually the largest proportion of TDP in near-surface waters. Although the large DOP pool is poorly characterized, at least a portion of it is available as a source of P for microbial growth. Particulate P includes both living and nonliving organic P (POP) and PIP; POP is the dominant component. Ectoenzymatic activity (Ecto) may be important for the microbial assimilation of DOP into POP. Whereas euphotic-zone processes are dominated by the net conversion of P to organic P, subeuphotic-zone (>200 m) P cycle processes are dominated by the net remineralization of organic P to P. A number of physical processes, as shown, are responsible for redistributing P throughout the global oceans. In the marine environment, P is almost exclusively in the pentava-lent state (+5) as PO ; only under highly reduced conditions is P transformed to phosphine gas (PH).

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 2
FIGURE 2

Schematic representation of the stepwise analysis of P in seawater. From three direct measurements, SRP, TDP, and PP, one can derive total P (TDP + PP) and DOP (TDP – SRP). Additional analytical procedures exist for the measurement of inorganic polyphosphates, for the separation of PP into organic and inorganic components, and for partial chemical and/or molecular characterization of the TDP and PP pools. However, SRP, TDP, and PP are the most commonly measured P cycle constituents.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 3
FIGURE 3

Annual mean phosphate (SRP) concentrations at the ocean’s surface, based on the worldwide data set held at NODC. Surface SRP concentrations range from <0.1 µM in the oligotrophic, central gyres of the major ocean basins to >1 µM at high latitudes, especially in the Southern Ocean and North Pacific Ocean. (From the Data are publicly available at http://www.nodc.noaa.gov.)

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 4
FIGURE 4

Relationship between vertical distributions of SRP and dissolved oxygen (O) at Station ALOHA in the North Pacific gyre. (Left) Graph of SRP (µM) versus depth (m) showing the characteristic “nutrient-like” distribution of SRP, with regions of net P uptake and export near the surface and net P remineralization at greater depths. The inset shows these main P cycle processes, which are most intense in the upper 1,000 m of the water column. (Right, top) SRP and O concentration-versus-depth profile of the 300- to 700-m region of the water column at Station ALOHA showing the effects of net remineralization of organic matter. (Right, bottom) Model 2 linear regression analysis of SRP versus O suggesting an average consumption of 80 µmol liter O for each 1 µmol of P regenerated.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 5
FIGURE 5

SRP-versus-depth profiles for the North Atlantic Ocean (Bermuda Atlantic Time-Series Study [BATS]) and the North Pacific Ocean (HOT) showing significant interocean differences, including a steeper phosphocline gradient (i.e., a larger change in SRP concentration per meter in the upper mesopelagic zone region) and higher deep-water (>4,000 m) SRP concentrations for HOT. These differences in SRP inventories and gradients have significant implications for SRP fluxes into the euphotic zone.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 6
FIGURE 6

Map showing the locations of World Ocean Circulation Experiment program transects A-16 (Atlantic) and P-15 (Pacific). Data from these cruises were obtained from http://woce.nodc.noaa.gov, averaged over the depth range of 500 to 1,500 m, and then combined into 10° latitude bins and plotted as mean SRP concentrations (± 1 standard deviation). The resultant plot shows a systematic increase in SRP concentrations at midwater depths “down” the Atlantic and “up” the Pacific. This result is in accordance with the known pathways of deep water circulation and the increasing age of the deep water mass. The accumulation of SRP is a result of the time-integrated decomposition of organic matter. Deg, degrees.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 7
FIGURE 7

Concentration-versus-depth profiles for SRP (µM) and DOP (µM) at Station ALOHA. Also shown is DOP as a percentage of TDP.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 8
FIGURE 8

Concentration-versus-depth profiles of particulate P (nM) and biomass P (nM) at Station ALOHA. Biomass P was derived from P-ATP measurements, assuming a biomass P-to-ATP ratio of 6.1 (see the text for details). Also shown is biomass P as a percentage of PP.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 9
FIGURE 9

Changes in SRP inventories for samples collected at Station ALOHA during the period from 1989 to 2004. (Top) Contour plot of SRP concentrations in the upper 0 to 60 m of the water column. (Bottom) Depth-integrated (0 to 60 m) inventories of SRP showing a systematic loss of SRP from this ecosystem over the past 15 years.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 10
FIGURE 10

Changes in PP inventories and C:N:P stoichiometry of particulate matter collected at Station ALOHA during the period from 1989 to 2004. The solid trend lines are the best-fit linear regression analyses for each data set. The dashed lines in the PC:PP and PN:PP plots show the “ideal” elemental stoichiometry of 106 C:16 N:1 P described by Redfield et al. ( ).

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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Image of FIGURE 11
FIGURE 11

Temporal changes in the export of particulate matter at Station ALOHA during the period from 1989 to 2004, as measured by drifting sediment traps deployed at a reference depth of 150 m. The heavy lines represent the three-point running means of approximately monthly observations. Presented in the upper two plots are the PC and PN export fluxes showing coherent temporal trends. Presented in the lower plot is the PP export flux, showing a fundamentally different pattern, specifically a systematic decrease in PP export over time. d, day.

Citation: Karl D. 2007. The Marine Phosphorus Cycle, p 523-539. In Hurst C, Crawford R, Garland J, Lipson D, Mills A, Stetzenbach L (ed), Manual of Environmental Microbiology, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815882.ch43
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References

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1. Ammerman, J. W.,, and F. Azam. 1981. Dissolved cyclic adenosine monophosphate (cAMP) in the sea and uptake of cAMP by marine bacteria. Mar. Ecol. Prog. Ser. 5:8589.
2. Ammerman, J. W.,, R. R. Hood,, D. A. Case, and, J. B. Cotner. 2003. Phosphorus deficiency in the Atlantic: an emerging paradigm in oceanography. Eos 84:165, 170.
3. Armstrong, F. A.,, P. M. Williams, and, J. D. H. Strickland. 1966. Photo-oxidation of organic matter in seawater by ultraviolet radiation, analytical and other applications. Nature 211:481483.
4. Armstrong, F. A. J.,, C. R. Sterns, and, J. D. H. Strickland. 1967. The measurement of upwelling and subsequent biological processes by means of the Technicon autoanalyzer and associated equipment. Deep-Sea Res. 14:381389.
5. Atkins, W. R. G.,, and E. G. Wilson. 1926. The colorimetric estimation of minute amounts of compounds of silicon, of phosphorus, and of arsenic. Biochem. J. 20:12231228.
6. Azam, F.,, and R. E. Hodson. 1977. Dissolved ATP in the sea and its utilisation by marine bacteria. Nature 267:696698.
7. Benner, R.,, J. D. Pakulski,, M. McCarthy,, J. I. Hedges, and, P. G. Hatcher. 1992. Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255:15611564.
8. Berman, T.,, M. Nawrocki,, G. T. Taylor, and, D. M. Karl. 1987. Nutrient flux between bacteria, bacterivorous nanoplanktonic protists and algae. Mar. Microb. Food Webs 2:6982.
9. Björkman, K. M.,, and D. M. Karl. 2003. Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol. Oceanogr. 48:10491057.
10. Björkman, K. M.,, and D. M. Karl. 2005. Presence of dissolved nucleotides in the North Pacific subtropical gyre and their role in cycling of dissolved organic phosphorus. Aquat. Microb. Ecol. 39:193203.
11. Björkman, K.,, A. L. Thomson-Bulldis, and, D. M. Karl. 2000. Phosphorus dynamics in the North Pacific subtropical gyre. Aquat. Microb. Ecol. 22:185198.
12. Blake, R. E.,, J. R. O’Neil, and, A. V. Surkov. 2005. Biogeochemical cycling of phosphorus: insights from oxygen isotope effects of phosphoenzymes. Am. J. Sci. 305:596620.
13. Bossard, P.,, and D. M. Karl. 1986. The direct measurement of ATP and adenine nucleotide pool turnover in microorganisms: a new method for environmental assessment of metabolism, energy flux and phosphorus dynamics. J. Plankton Res. 8:113.
14. Broecker, W. S.,, and T.-H. Peng. 1982. Tracers in the Sea. Lamont-Doherty Geological Observatory, Columbia University, Palisades, N.Y.
15. Brum, J. R. 2005. Concentration, production and turnover of viruses and dissolved DNA pools at Stn ALOHA, North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 41:103113.
16. Cavender-Bares, K. K.,, D. M. Karl, and, S. W. Chisholm. 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. 48:23732395.
17. Christian, J. R.,, M. R. Lewis, and, D. M. Karl. 1997. Vertical fluxes of carbon, nitrogen and phosphorus in the North Pacific subtropical gyre near Hawaii. J. Geophys. Res. 102:15,66715,677.
18. Church, M. J.,, H. W. Ducklow, and, D. M. Karl. 2002. Multiyear increases in dissolved organic matter inventories at Station ALOHA in the North Pacific Subtropical Gyre. Limnol. Oceanogr. 47:110.
19. Clark, L. L.,, E. D. Ingall, and, R. Benner. 1998. Marine phosphorus is selectively remineralized. Nature 393:426.
20. Colman, A. S.,, R. E. Blake,, D. M. Karl,, M. L. Fogel, and, K. K. Turekian. 2005. Marine phosphate oxygen isotopes and organic matter remineralization in the oceans. Proc. Natl. Acad. Sci. USA 102:1302313028.
21. Conkright, M. E.,, W. W. Gregg, and, S. Levitus. 2000. Seasonal cycle of phosphate in the open ocean. Deep-Sea Res. I 47:159175.
22. Cotner, J. B.,, and R. G. Wetzel. 1992. Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton. Limnol. Oceanogr. 37:232243.
23. Cullen, J. J.,, P. J. S. Franks,, D. M. Karl, and, A. Longhurst. 2002. Physical influences on marine ecosystem dynamics, p. 297–336. In A. R. Robinson,, J. J. McCarthy, and, B. J. Rothschild (ed.), The Sea, vol. 12. John Wiley & Sons, Inc., New York, N.Y.
24. deDuve, C. 1991. Blueprint for a Cell: the Nature and Origin of Life. Neil Patterson Publishers, Burlington, N.C.
25. DeFlaun, M. F.,, and J. H. Paul. 1989. Detection of exogenous gene sequences in dissolved DNA from aquatic environments. Microb. Ecol. 18:2128.
26. DeFlaun, M. F.,, J. H. Paul, and, D. Davis. 1986. Simplified method for dissolved DNA determination in aquatic environments. Appl. Environ. Microbiol. 52:654659.
27. DeFlaun, M. F.,, J. H. Paul, and, W. H. Jeffrey. 1987. Distribution and molecular weight of dissolved DNA in subtropical estuarine and oceanic environments. Mar. Ecol. Prog. Ser. 38:6573.
28. DeLong, E. F.,, and D. M. Karl. 2005. Genomic perspectives in microbial oceanography. Nature 437:336342.
29. Denigès, G. 1921. Détermination quantitative des plus faibles quantités de phosphates dans les produits biologiques par la méthode céruléomolybdique. C. R. Soc. Biol. Paris 84:875877.
30. Doney, S. C.,, M. R. Abbott,, J. J. Cullen,, D. M. Karl, and, L. Rothstein. 2004. From genes to ecosystems: the ocean’s new frontier. Frontiers Ecol. Environ. 2:457466.
31. Dyhrman, S. T.,, and B. Palenik. 1999. Phosphate stress in cultures and field populations of the dinoflagellate Prorocentrum minimum detected by a single-cell alkaline phosphatase assay. Appl. Environ. Microbiol. 65:32053212.
32. Dyhrman, S. T.,, P. D. Chappell,, S. T. Haley,, J. W. Moffett,, E. D. Orchard,, J. B. Waterbury, and, E. A. Webb. 2006. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439:6871.
33. Fiske, C. H.,, and Y. Subbarow. 1925. The colorimetric determination of phosphorus. J. Biol. Chem. 66:375400.
34. Froelich, P. N.,, M. L. Bender,, N. A. Luedtke,, G. R. Heath, and, T. DeVries. 1982. The marine phosphorus cycle. Am. J. Sci. 282:474511.
35. Fu, F.-X.,, Y. Zhang,, K. Leblanc,, S. A. Sañudo-Wilhelmy, and, D. A. Hutchins. 2005. The biological and biogeochemical consequences of phosphate scavenging onto phytoplankton cell surfaces. Limnol. Oceanogr. 50:14591472.
36. Fuwa, K.,, W. Lei, and, K. Fujiwara. 1984. Colorimetry with a total-reflection long-capillary cell. Anal. Chem. 56:16401644.
37. Harrison, W. G. 1983. Uptake and recycling of soluble reactive phosphorus by marine microplankton. Mar. Ecol. Prog. Ser. 10:127135.
38. Haury, L. R.,, C. L. Fey, and, E. Shulenberger. 1994. Surface enrichment of inorganic nutrients in the North Pacific Ocean. Deep-Sea Res. 41:11911205.
39. Hecky, R. E.,, and P. Kilham. 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnol. Oceanogr. 33:796822.
40. Hicks, E.,, and J. P. Riley. 1980. The determination of dissolved total nucleic acids in natural waters including sea water. Anal. Chim. Acta 116:137144.
41. Holm-Hansen, O. 1969. Determination of microbial bio-mass in ocean profiles. Limnol. Oceanogr. 14:740747.
42. Holm-Hansen, O.,, and C. R. Booth. 1966. The measurement of adenosine triphosphate in the ocean and its ecological significance. Limnol. Oceanogr. 11:510519.
43. Holm-Hansen, O.,, W. H. Sutcliffe, Jr., and, J. Sharp. 1968. Measurement of deoxyribonucleic acid in the ocean and its ecological significance. Limnol. Oceanogr. 13:507514.
44. Hulett, H. R. 1970. Non-enzymatic hydrolysis of adenosine phosphates. Nature 225:12481249.
45. Hutchinson, G. E. 1971. A Treatise on Limnology. John Wiley & Sons, New York, N.Y.
46. Karl, D. M. 1980. Cellular nucleotide measurements and applications in microbial ecology. Microbiol. Rev. 44:739796.
47. Karl, D. M. 1999. A sea of change: biogeochemical variability in the North Pacific subtropical gyre. Ecosystems 2:181214.
48. Karl, D. M. 2000. Phosphorus, the staff of life. Nature 406:3132.
49. Karl, D. M. 2002. Nutrient dynamics in the deep blue sea. Trends Microbiol. 10:410418.
50. Karl, D. M.,, and M. D. Bailiff. 1989. The measurement and distribution of dissolved nucleic acids in aquatic environments. Limnol. Oceanogr. 34:543558.
51. Karl, D. M.,, N. R. Bates,, S. Emerson,, P. J. Harrison,, C. Jeandel,, O. Llinas,, K.-K. Liu,, J.-C. Marty,, A. F. Michaels,, J. C. Miquel,, S. Neuer,, Y. Nojiri, and, C. S. Wong. 2003. Temporal studies of biogeochemical processes determined from ocean time-series observations during the JGOFS era, p. 239–267. In M. J. R. Fasham (ed.), Ocean Biogeochemistry: the Role of the Ocean Carbon Cycle in Global Change. Springer, New York, N.Y.
52. Karl, D. M.,, and K. M. Björkman. 2001. Phosphorus cycle in seawater: dissolved and particulate pool inventories and selected phosphorus fluxes. Methods Microbiol. 30:239270.
53. Karl, D. M.,, and K. M. Björkman. 2002. Dynamics of DOP, p. 246–366. In D. Hansell and, C. Carlson (ed.), Biogeochemistry of Marine Dissolved Organic Matter. Elsevier Science, Amsterdam, The Netherlands.
54. Karl, D. M.,, K. M. Björkman,, J. E. Dore,, L. Fujieki,, D. V. Hebel,, T. Houlihan,, R. M. Letelier, and, L. M. Tupas. 2001. Ecological nitrogen-to-phosphorus stoichiometry at Station ALOHA. Deep-Sea Res. II 48:15291566.
55. Karl, D. M.,, and P. Bossard. 1985. Measurement and significance of ATP and adenine nucleotide pool turnover in microbial cells and environmental samples. J. Microbiol. Methods 3:125139.
56. Karl, D. M.,, J. R. Christian,, J. E. Dore,, D. V. Hebel,, R. M. Letelier,, L. M. Tupas, and, C. D. Winn. 1996. Seasonal and interannual variability in primary production and particle flux at Station ALOHA. Deep-Sea Res. II 43:539568.
57. Karl, D.,, R. Letelier,, L. Tupas,, J. Dore,, J. Christian, and, D. Hebel. 1997. The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388:533538.
58. Karl, D. M.,, and R. Lukas. 1996. The Hawaii Ocean Time-Series (HOT) Program: background, rationale and field implementation. Deep-Sea Res. II 43:129156.
59. Karl, D. M.,, and G. Tien. 1992. MAGIC: a sensitive and precise method for measuring dissolved phosphorus in aquatic environments. Limnol. Oceanogr. 37:105116.
60. Karl, D. M.,, and G. Tien. 1997. Temporal variability in dissolved phosphorus concentrations in the subtropical North Pacific Ocean. Mar. Chem. 56:7796.
61. Karl, D. M.,, and C. D. Winn. 1984. Adenine metabolism and nucleic acid synthesis: applications to microbiological oceanography, p. 197–215. In J. E. Hobbie and, P. J. L. Williams (ed.), Heterotrophic Activity in the Sea. Plenum Publishing Corp., New York, N.Y.
62. Karl, D. M.,, and K. Yanagi. 1997. Partial characterization of the dissolved organic phosphorus pool in the oligotrophic North Pacific Ocean. Limnol. Oceanogr. 42:13981405.
63. Lal, D.,, and T. Lee. 1988. Cosmogenic 32P and 33P used as tracers to study phosphorus recycling in the ocean. Nature 333:752754.
64. Lal, D.,, Y. Chung,, T. Platt, and, T. Lee. 1988. Twin cosmogenic radiotracer studies of phosphorus cycling and chemical fluxes in the upper ocean. Limnol. Oceanogr. 33:15591567.
65. Lorenz, M. G.,, and W. Wackernagel. 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58:563602.
66. Mackenzie, F. T.,, L. M. Ver, and, A. Lerman. 2002. Century-scale nitrogen and phosphorus controls of the carbon cycle. Chem. Geol. 190:1332.
67. Martin, J. H.,, G. A. Knauer,, D. M. Karl, and, W. W. Broenkow. 1987. VERTEX: carbon cycling in the Northeast Pacific. Deep-Sea Res. 34:267285.
68. McGrath, S. M.,, and C. W. Sullivan. 1981. Community metabolism of adenylates by microheterotrophs from the Los Angeles and Southern California coastal waters. Mar. Biol. 62:217226.
69. Meybeck, M. 1982. Carbon, nitrogen and phosphorus transport by world rivers. Am. J. Sci. 282:401450.
70. Mills, M. M.,, C. Ridame,, M. Davey,, J. La Roche, and, R. J. Geider. 2004. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292294.
71. Morton, S. C.,, and M. Edwards. 2005. Reduced phosphorus compounds in the environment. Crit. Rev. Environ. Sci. Technol. 35:333364.
72. Moutin, T.,, T. F. Thingstad,, F. Van Wambeke,, D. Marie,, G. Slawyk,, P. Raimbault, and, H. Claustre. 2002. Does competition for nanomolar phosphate supply explain the predominance of the cyanobacterium Synechococcus? Limnol. Oceanogr. 47:15621567.
73. Murphy, J.,, and J. P. Riley. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27:3136.
74. Orrett, K.,, and D. M. Karl. 1987. Dissolved organic phosphorus production and turnover in surface waters. Limnol. Oceanogr. 32:383395.
75. Pace, M. L.,, G. A. Knauer,, D. M. Karl, and, J. H. Martin. 1987. Primary production, new production and vertical flux in the eastern Pacific Ocean. Nature 325:803804.
76. Paul, J. H.,, M. E. Frischer, and, J. M. Thurmond. 1991. Gene transfer in marine water column and sediment microcosms by natural plasmid transformation. Appl. Environ. Microbiol. 57:15091515.
77. Proctor, C. M.,, and D. W. Hood. 1954. Determination of inorganic phosphate in sea water by an iso-butanol extraction procedure. J. Mar. Res. 13:122132.
78. Redfield, A.C.,, B. H. Ketchum, and, F. A. Richards. 1963. The influence of organisms on the composition of seawater p. 26–77. In M. N. Hill (ed.), The Sea, Ideas and Observations on Progress in the Study of the Seas, vol. 2. Interscience, New York, N.Y.
79. Redfield, R. J.,, M. R. Schrag, and, A. M. Dean. 1997. The evolution of bacterial transformation: sex with poor relations. Genetics 146:2738.
80. Ridal, J. J.,, and R. M. Moore. 1990. A re-examination of the measurement of dissolved organic phosphorus in sea-water. Mar. Chem. 29:1931.
81. Rigler, F. H. 1968. Further observations inconsistent with the hypothesis that the molybdenum blue method measures orthophosphate in lake water. Limnol. Oceanogr. 13:713.
82. Rothstein, L. M.,, J. J. Cullen,, M. Abbott,, E. Chassignet,, K. Denman,, S. Doney,, H. Ducklow,, K. Fennel,, M. Follows,, D. Haidvogel,, E. Hofmann,, D. Karl,, J. Kindle,, I. Lima,, M. Maltrud,, C. McClain,, D. McGillicuddy,, J. Olascoaga,, Y. Spitz,, J. Wiggert, and, J. Yoder. 2006. Modeling ocean ecosystems: the PARADIGM program. Oceanography 19:1745.
83. Ryther, J. H.,, and W. M. Dunstan. 1971. Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171:10081013.
84. Sakano, S.,, and A. Kamatani. 1992. Determination of dissolved nucleic acids in seawater by the fluorescence dye, ethidium bromide. Mar. Chem. 37:239255.
85. Scanlan, D. J.,, and W. H. Wilson. 1999. Application of molecular techniques to addressing the role of P as a key effector in marine ecosystems. Hydrobiologia 401:149175.
86. Strickland, J. D. H.,, and T. R. Parsons. 1972. A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada, Ottawa, Canada.
87. Suzumura, M.,, K. Ishikawa, and, H. Ogawa. 1998. Characterization of dissolved organic phosphorus in coastal seawater using ultrafiltration and phosphohydrolytic enzymes. Limnol. Oceanogr. 43:15531564.
88. Sverdrup, H. U. 1953. On conditions for the vernal blooming of phytoplankton. J. Cons. Int. Explor. Mer 18:287295.
89. Tarapchak, S. J.,, and R. A. Moll. 1990. Phosphorus sources for phytoplankton and bacteria in Lake Michigan. J. Plankton Res. 12:743758.
90. Turk, V.,, A.-S. Rehnstam,, E. Lundberg, and, A. Hagström. 1992. Release of bacterial DNA by marine nanoflagellates, an intermediate step in phosphorus regeneration. Appl. Environ. Microbiol. 58:37443750.
91. Tyrrell, T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525531.
92. Wackett, L. P.,, B. L. Wanner,, C. P. Venditti, and, C. T. Walsh. 1987. Involvement of the phosphate regulon and the psiD locus in carbon-phosphorus lyase activity of Escherichia coli K-12. J. Bacteriol. 169:17531756.
93. White, A. E.,, Y. H. Spitz,, D. M. Karl, and, R. M. Letelier. 2006. Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol. Oceanogr. 51:17771790.
94. Wilson, W. H.,, N. G. Carr, and, N. H. Mann. 1996. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32:506516.
95. Wu, J.,, W. Sunda,, E. A. Boyle, and, D. M. Karl. 2000. Phosphate depletion in the western North Atlantic Ocean. Science 289:759762.

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