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The phosphorus redox cycle

Phosphorus in the oceans cycles between +5 and +3 oxidation states. Most of the oceans' phosphorus is present as oxidized bioavailable phosphate (+5) compounds. Reduced organophosphorus compounds are also present but at much lower concentrations. Through field measurements in the western tropical North Atlantic Ocean and a series of laboratory incubations, Van Mooy et al. measured fast reduction rates of a small but appreciable amount of phosphates by plankton communities, forming phosphites and phosphonates (see the Perspective by Benitez-Nelson). On a global scale, this phosphorus redox cycle adds as much reduced phosphorus to the oceans as all pre-anthropogenic land runoff.
Science, this issue p. 783; see also p. 759

Abstract

Phosphorus in the +5 oxidation state (i.e., phosphate) is the most abundant form of phosphorus in the global ocean. An enigmatic pool of dissolved phosphonate molecules, with phosphorus in the +3 oxidation state, is also ubiquitous; however, cycling of phosphorus between oxidation states has remained poorly constrained. Using simple incubation and chromatography approaches, we measured the rate of the chemical reduction of phosphate to P(III) compounds in the western tropical North Atlantic Ocean. Colonial nitrogen-fixing cyanobacteria in surface waters played a critical role in phosphate reduction, but other classes of plankton, including potentially deep-water archaea, were also involved. These data are consistent with marine geochemical evidence and microbial genomic information, which together suggest the existence of a vast oceanic phosphorus redox cycle.
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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S4
Tables S1 to S3
References (3237)

Resources

File (van_mooy.sm.pdf)

References and Notes

1
Karl D. M., Microbially mediated transformations of phosphorus in the sea: New views of an old cycle. Annu. Rev. Mar. Sci. 6, 279–337 (2014).
2
Björkman K., Thomson-Bulldis A. L., Karl D. M., Phosphorus dynamics in the North Pacific subtropical gyre. Aquat. Microb. Ecol. 22, 185–198 (2000).
3
Young C. L., Ingall E. D., Marine dissolved organic phosphorus composition: Insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat. Geochem. 16, 563–574 (2010).
4
Clark L. L., Ingall E. D., Benner R., Marine phosphorus is selectively remineralized. Nature 393, 426 (1998).
5
Dyhrman S. T., Benitez-Nelson C. R., Orchard E. D., Haley S. T., Pellechia P. J., A microbial source of phosphonates in oligotrophic marine systems. Nat. Geosci. 2, 696–699 (2009).
6
Villarreal-Chiu J. F., Quinn J. P., McGrath J. W., The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front. Microbiol. 3, 19 (2012).
7
Metcalf W. W., Griffin B. M., Cicchillo R. M., Gao J., Janga S. C., Cooke H. A., Circello B. T., Evans B. S., Martens-Habbena W., Stahl D. A., van der Donk W. A., Synthesis of methylphosphonic acid by marine microbes: A source for methane in the aerobic ocean. Science 337, 1104–1107 (2012).
8
Dyhrman S. T., Chappell P. D., Haley S. T., Moffett J. W., Orchard E. D., Waterbury J. B., Webb E. A., Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71 (2006).
9
Martinez A., Tyson G. W., Delong E. F., Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metagenomic analyses. Environ. Microbiol. 12, 222–238 (2010).
10
Karl D. M., Beversdorf L., Björkman K. M., Church M. J., Martinez A., Delong E. F., Aerobic production of methane in the sea. Nat. Geosci. 1, 473–478 (2008).
11
Martínez A., Osburne M. S., Sharma A. K., DeLong E. F., Chisholm S. W., Phosphite utilization by the marine picocyanobacterium Prochlorococcus MIT9301. Environ. Microbiol. 14, 1363–1377 (2012).
12
Carini P., White A. E., Campbell E. O., Giovannoni S. J., Methane production by phosphate-starved SAR11 chemoheterotrophic marine bacteria. Nat. Commun. 5, 4346 (2014).
13
White A., Karl D., Björkman K., Beversdorf L., Letelier R., Production of organic matter by Trichodesmium IMS101 as a function of phosphorus source. Limnol. Oceanogr. 55, 1755–1767 (2010).
14
Beversdorf L. J., White A. E., Björkman K. M., Letelier R. M., Karl D. M., Phosphonate metabolism of Trichodesmium IMS101 and the production of greenhouse gases. Limnol. Oceanogr. 55, 1768–1778 (2010).
15
del Valle D. A., Karl D. M., Aerobic production of methane from dissolved water-column methylphosphonate and sinking particles in the North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 73, 93–105 (2014).
16
Feingersch R., Philosof A., Mejuch T., Glaser F., Alalouf O., Shoham Y., Béjà O., Potential for phosphite and phosphonate utilization by Prochlorococcus. ISME J. 6, 827–834 (2012).
17
Materials and methods are available as supplementary materials on Science Online.
18
Pech H., Vazquez M. G., Van Buren J., Shi L., Ivey M. M., Salmassi T. M., Pasek M. A., Foster K. L., Elucidating the redox cycle of environmental phosphorus using ion chromatography. J. Chromatogr. Sci. 49, 573–581 (2011).
19
McDowell M. M., Ivey M. M., Lee M. E., Firpo V. V., Salmassi T. M., Khachikian C. S., Foster K. L., Detection of hypophosphite, phosphite, and orthophosphate in natural geothermal water by ion chromatography. J. Chromatogr. A 1039, 105–111 (2004).
20
Pasek M. A., Sampson J. M., Atlas Z., Redox chemistry in the phosphorus biogeochemical cycle. Proc. Natl. Acad. Sci. U.S.A. 111, 15468–15473 (2014).
21
DeVries T., Liang J. H., Deutsch C., A mechanistic particle flux model applied to the oceanic phosphorus cycle. Biogeosciences 11, 5381–5398 (2014).
22
Paytan A., McLaughlin K., The oceanic phosphorus cycle. Chem. Rev. 107, 563–576 (2007).
23
Karner M. B., DeLong E. F., Karl D. M., Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).
24
Wuchter C., Abbas B., Coolen M. J., Herfort L., van Bleijswijk J., Timmers P., Strous M., Teira E., Herndl G. J., Middelburg J. J., Schouten S., Sinninghe Damsté J. S., Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U.S.A. 103, 12317–12322 (2006).
25
Mills M. M., Ridame C., Davey M., La Roche J., Geider R. J., Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292–294 (2004).
26
Sañudo-Wilhelmy S. A., Kustka A. B., Gobler C. J., Hutchins D. A., Yang M., Lwiza K., Burns J., Capone D. G., Raven J. A., Carpenter E. J., Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411, 66–69 (2001).
27
Van Mooy B. A. S., Hmelo L. R., Sofen L. E., Campagna S. R., May A. L., Dyhrman S. T., Heithoff A., Webb E. A., Momper L., Mincer T. J., Quorum sensing control of phosphorus acquisition in Trichodesmium consortia. ISME J. 6, 422–429 (2012).
28
Hmelo L. R., Van Mooy B. A. S., Mincer T. J., Characterization of bacterial epibionts on the cyanobacterium Trichodesmium. Aquat. Microb. Ecol. 67, 1–14 (2012).
29
Carpenter E. J., Subramaniam A., Capone D. G., Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical N Atlantic ocean. Deep-Sea Res. Part I 51, 173–203 (2004).
30
Rouco M., Warren H. J., McGillicuddy D. J., Waterbury J. B., Dyhrman S. T., Trichodesmium sp. clade distributions in the western North Atlantic Ocean. Limnol. Oceanogr. 59, 1899–1909 (2014).
31
Zhang N., Casida J. E., Novel synthesis of [33P]-(2-chloroethyl)phosphonic acid. J. Org. Chem. 66, 327–329 (2001).
32
Karl D. M., Tien G., MAGIC: A sensitive and precise method for measuring dissolved phosphorus in aquatic environments. Limnol. Oceanogr. 37, 105–116 (1992).
33
Van Mooy B. A. S., Fredricks H. F., Pedler B. E., Dyhrman S. T., Karl D. M., Koblízek M., Lomas M. W., Mincer T. J., Moore L. R., Moutin T., Rappé M. S., Webb E. A., Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009).
34
Martin P., Dyhrman S. T., Lomas M. W., Poulton N. J., Van Mooy B. A. S., Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc. Natl. Acad. Sci. U.S.A. 111, 8089–8094 (2014).
35
Orchard E. D., Ammerman J. W., Lomas M. W., Dyhrman S. T., Dissolved inorganic and organic phosphorus uptake in Trichodesmium and the microbial community: The importance of phosphate ester in the Sargasso Sea. Limnol. Oceanogr. 55, 1390–1399 (2010).
36
Perry M. J., Eppley R. W., Phosphate uptake by phytoplankton in the central North Pacific. Deep-Sea Res. Part A 28, 39–49 (1981).
37
Nowack B., Environmental chemistry of phosphonates. Water Res. 37, 2533–2546 (2003).

Information & Authors

Information

Published In

Science
Volume 348 | Issue 6236
15 May 2015

Submission history

Received: 30 January 2015
Accepted: 3 April 2015
Published in print: 15 May 2015

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Acknowledgments

We are grateful for the assistance of the officers and crew of the R/V Atlantic Explorer and the support of D. Polyviou (University of Southampton), J. Tagliaferre (Woods Hole Oceanographic Institution), and the entire PABST Cruise scientific party. We also thank T. Bibby, A. Hitchock, and C. M. Moore, (University of Southampton) as well as A. Santoro (University of Maryland), for insightful discussions and R. Johnson (Bermuda Institute of Ocean Sciences) for input on the execution of the IC methods at sea. Major support for this study was provided by grants from the NSF to B.A.S.V.M. and S.T.D. (OCE-13-32898 and OCE-13-32912). This work was also supported in part by grants from the Simons Foundation to B.A.S.V.M, S.T.D., and D.J.R. and is a contribution of the Simons Collaboration on Ocean Processes and Ecology. The data presented in all figures, as well as additional environmental data, are provided in tables S2 and S3.

Authors

Affiliations

B. A. S. Van Mooy* [email protected]
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
A. Krupke
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
S. T. Dyhrman
Department of Earth and Environmental Science and Lamont-Doherty Earth Observatory, Columbia University, New York, NY 10027, USA.
H. F. Fredricks
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
K. R. Frischkorn
Department of Earth and Environmental Science and Lamont-Doherty Earth Observatory, Columbia University, New York, NY 10027, USA.
J. E. Ossolinski
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
D. J. Repeta
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
M. Rouco
Department of Earth and Environmental Science and Lamont-Doherty Earth Observatory, Columbia University, New York, NY 10027, USA.
J. D. Seewald
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
S. P. Sylva
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

Notes

*Corresponding author. E-mail: [email protected]

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