DOI: 10.1111/j.1462-2920.2007.01324.x. Microbial control of phosphate in the nutrient‐depleted North Atlantic subtropical gyre

Microbial control of phosphate in the nutrient‐depleted North Atlantic subtropical gyre

10.1111/j.1462-2920.2007.01324.x

Crossref journal-article

Wiley

Environmental Microbiology (311)

Abstract

SummaryLittle is known about the dynamics of dissolved phosphate in oligotrophic areas of the world's oceans, where concentrations are typically in the nanomolar range. Here, we have budgeted phosphate uptake by the dominant microbial groups in order to assess the effect of the microbial control of this depleted nutrient in the North Atlantic gyre. Low concentrations (2.2 ± 1.2 nM) and rapid microbial uptake (2.1 ± 2.4 nM day−1) of bioavailable phosphate were repeatedly determined in surface waters of the North Atlantic oligotrophic gyre during spring and autumn research cruises, using a radiotracer dilution bioassay technique. Upper estimates of the concentration of bioavailable phosphate were 7–55% of the dissolved mineral phosphate suggesting that a considerable part of the chemically measured nanomolar phosphate was in a form unavailable for direct microbial uptake. A 1:1 relationship (r2 = 0.96, P < 0.0001) was observed between the bioavailable total phosphate uptake and the phosphate uptake of all the flow sorted bacterioplankton cells, demonstrating that bacterioplankton were the main consumers of phosphate. Within the bacterioplankton a group of heterotrophic bacteria and Prochlorococcus phototrophic cyanobacteria, were the two major competing groups for bioavailable phosphate. These heterotrophic bacteria had low nucleic acid content and 60% of them comprised of SAR11 clade cells based on the results of fluorescence in situ hybridization. Each of the two competing bacterial groups was responsible for an average of 45% of the phosphate uptake, while Synechococcus cyanobacteria (7%) and picoplanktonic algae (0.3%) played minor roles in direct phosphate uptake. We have demonstrated that phosphate uptake in the oligotrophic gyre is rapid and dominated by two bacterial groups rather than by algae.

Bibliography

Zubkov, M. V., Mary, I., Woodward, E. M. S., Warwick, P. E., Fuchs, B. M., Scanlan, D. J., & Burkill, P. H. (2007). Microbial control of phosphate in the nutrientâdepleted North Atlantic subtropical gyre. Environmental Microbiology, 9(8), 2079â2089. Portico.

Authors 7

Mikhail V. Zubkov (first)
Isabelle Mary (additional)
E. Malcolm S. Woodward (additional)
Phillip E. Warwick (additional)
Bernhard M. Fuchs (additional)
David J. Scanlan (additional)
Peter H. Burkill (additional)

References 44 Referenced 96

10.1128/jb.172.2.762-770.1990
10.1029/2003EO180001
10.1038/nature04159
10.4319/lo.2003.48.5.1721
10.1128/AEM.69.9.5519-5529.2003
10.1016/S0723-2020(99)80053-8
10.4319/lo.1984.29.2.0258
10.1126/science.1114057
10.1128/jb.140.2.508-517.1979 / J Bacteriol / Regulation of phosphate accumulation in the unicellular cyanobacterium Synechococcus by Grillo J.F. (1979)
10.4319/lo.2002.47.5.1525
10.4319/lo.2003.48.5.1732
10.1111/j.0022-3646.2003.03-090.x
10.1126/science.1118052
10.1038/41474
10.1038/35054051
10.3354/ame017311
10.4319/lo.1994.39.1.0169
10.3354/meps123245
10.1128/AEM.63.1.186-193.1997
10.1073/pnas.0601301103
10.3354/ame045107
10.1038/nature02550
10.3354/ame039257
10.1038/nature01240
10.4319/lo.2002.47.5.1562
{'key': 'e_1_2_6_27_1', 'first-page': '175', 'volume-title': 'Handbook of Methods in Aquatic Microbial Ecology.', 'author': 'Olson R.J.', 'year': '1993'} / Handbook of Methods in Aquatic Microbial Ecology. by Olson R.J. (1993)
10.1128/AEM.70.9.5426-5433.2004
10.1128/AEM.68.6.3094-3101.2002
10.1038/35075041
10.1128/AEM.65.3.1259-1267.1999
10.1126/science.1112632
10.1073/pnas.0600540103
10.1128/AEM.65.6.2585-2591.1999
10.1099/00221287-147-7-1731
{'key': 'e_1_2_6_36_1', 'volume-title': 'Nutrient Analysis Techniques.', 'author': 'Woodward E.M.S.', 'year': '1994'} / Nutrient Analysis Techniques. by Woodward E.M.S. (1994)
{'key': 'e_1_2_6_37_1', 'first-page': '92', 'article-title': 'Nanomolar detection of phosphate and nitrate using liquid waveguard technology', 'volume': '83', 'author': 'Woodward E.M.S.', 'year': '2002', 'journal-title': 'EOS'} / EOS / Nanomolar detection of phosphate and nitrate using liquid waveguard technology by Woodward E.M.S. (2002)
10.2307/1932984
10.1126/science.289.5480.759
10.1002/cyto.a.20332
10.3354/ame040241
10.1016/S0079-6611(00)00008-2
10.1016/j.femsec.2004.06.009
10.1093/plankt/fbl059
10.1111/j.1462-2920.2007.01246.x

Dates

Type	When
Created	18 years, 3 months ago (May 28, 2007, 3:49 a.m.)
Deposited	1 year, 11 months ago (Sept. 28, 2023, 12:15 p.m.)
Indexed	2 months, 3 weeks ago (June 13, 2025, 4:06 a.m.)
Issued	18 years, 3 months ago (May 28, 2007)
Published	18 years, 3 months ago (May 28, 2007)
Published Online	18 years, 3 months ago (May 28, 2007)
Published Print	18 years, 1 month ago (Aug. 1, 2007)

Funders 0

None

BibTeX

@article{Zubkov_2007, title={Microbial control of phosphate in the nutrient‐depleted North Atlantic subtropical gyre}, volume={9}, ISSN={1462-2920}, url={http://dx.doi.org/10.1111/j.1462-2920.2007.01324.x}, DOI={10.1111/j.1462-2920.2007.01324.x}, number={8}, journal={Environmental Microbiology}, publisher={Wiley}, author={Zubkov, Mikhail V. and Mary, Isabelle and Woodward, E. Malcolm S. and Warwick, Phillip E. and Fuchs, Bernhard M. and Scanlan, David J. and Burkill, Peter H.}, year={2007}, month=may, pages={2079–2089} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        13
      ]
    ],
    "date-time": "2025-06-13T08:06:27Z",
    "timestamp": 1749801987975
  },
  "reference-count": 44,
  "publisher": "Wiley",
  "issue": "8",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2007,
            5,
            28
          ]
        ],
        "date-time": "2007-05-28T00:00:00Z",
        "timestamp": 1180310400000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "ami-journals.onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2007,
        8
      ]
    ]
  },
  "abstract": "<jats:title>Summary</jats:title><jats:p>Little is known about the dynamics of dissolved phosphate in oligotrophic areas of the world's oceans, where concentrations are typically in the nanomolar range. Here, we have budgeted phosphate uptake by the dominant microbial groups in order to assess the effect of the microbial control of this depleted nutrient in the North Atlantic gyre. Low concentrations (2.2\u2003\u00b1\u20031.2\u2003nM) and rapid microbial uptake (2.1\u2003\u00b1\u20032.4\u2003nM\u2003day<jats:sup>\u22121</jats:sup>) of bioavailable phosphate were repeatedly determined in surface waters of the North Atlantic oligotrophic gyre during spring and autumn research cruises, using a radiotracer dilution bioassay technique. Upper estimates of the concentration of bioavailable phosphate were 7\u201355% of the dissolved mineral phosphate suggesting that a considerable part of the chemically measured nanomolar phosphate was in a form unavailable for direct microbial uptake. A 1:1 relationship (<jats:italic>r</jats:italic><jats:sup>2</jats:sup>\u2003=\u20030.96, <jats:italic>P</jats:italic>\u2003&lt;\u20030.0001) was observed between the bioavailable total phosphate uptake and the phosphate uptake of all the flow sorted bacterioplankton cells, demonstrating that bacterioplankton were the main consumers of phosphate. Within the bacterioplankton a group of heterotrophic bacteria and <jats:italic>Prochlorococcus</jats:italic> phototrophic cyanobacteria, were the two major competing groups for bioavailable phosphate. These heterotrophic bacteria had low nucleic acid content and 60% of them comprised of SAR11 clade cells based on the results of fluorescence <jats:italic>in situ</jats:italic> hybridization. Each of the two competing bacterial groups was responsible for an average of 45% of the phosphate uptake, while <jats:italic>Synechococcus</jats:italic> cyanobacteria (7%) and picoplanktonic algae (0.3%) played minor roles in direct phosphate uptake. We have demonstrated that phosphate uptake in the oligotrophic gyre is rapid and dominated by two bacterial groups rather than by algae.</jats:p>",
  "DOI": "10.1111/j.1462-2920.2007.01324.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        5,
        28
      ]
    ],
    "date-time": "2007-05-28T07:49:07Z",
    "timestamp": 1180338547000
  },
  "page": "2079-2089",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 96,
  "title": "Microbial control of phosphate in the nutrient\u2010depleted North Atlantic subtropical gyre",
  "prefix": "10.1111",
  "volume": "9",
  "author": [
    {
      "given": "Mikhail V.",
      "family": "Zubkov",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Isabelle",
      "family": "Mary",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "E. Malcolm S.",
      "family": "Woodward",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Phillip E.",
      "family": "Warwick",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Bernhard M.",
      "family": "Fuchs",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "David J.",
      "family": "Scanlan",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Peter H.",
      "family": "Burkill",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2007,
        5,
        28
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_6_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.172.2.762-770.1990"
    },
    {
      "key": "e_1_2_6_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1029/2003EO180001"
    },
    {
      "key": "e_1_2_6_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature04159"
    },
    {
      "key": "e_1_2_6_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.2003.48.5.1721"
    },
    {
      "key": "e_1_2_6_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.69.9.5519-5529.2003"
    },
    {
      "key": "e_1_2_6_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0723-2020(99)80053-8"
    },
    {
      "key": "e_1_2_6_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.1984.29.2.0258"
    },
    {
      "key": "e_1_2_6_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1114057"
    },
    {
      "key": "e_1_2_6_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "508",
      "DOI": "10.1128/jb.140.2.508-517.1979",
      "article-title": "Regulation of phosphate accumulation in the unicellular cyanobacterium Synechococcus",
      "volume": "140",
      "author": "Grillo J.F.",
      "year": "1979",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "e_1_2_6_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.2002.47.5.1525"
    },
    {
      "key": "e_1_2_6_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.2003.48.5.1732"
    },
    {
      "key": "e_1_2_6_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.0022-3646.2003.03-090.x"
    },
    {
      "key": "e_1_2_6_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1118052"
    },
    {
      "key": "e_1_2_6_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/41474"
    },
    {
      "key": "e_1_2_6_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/35054051"
    },
    {
      "key": "e_1_2_6_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/ame017311"
    },
    {
      "key": "e_1_2_6_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.1994.39.1.0169"
    },
    {
      "key": "e_1_2_6_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/meps123245"
    },
    {
      "key": "e_1_2_6_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.63.1.186-193.1997"
    },
    {
      "key": "e_1_2_6_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0601301103"
    },
    {
      "key": "e_1_2_6_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/ame045107"
    },
    {
      "key": "e_1_2_6_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature02550"
    },
    {
      "key": "e_1_2_6_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/ame039257"
    },
    {
      "key": "e_1_2_6_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature01240"
    },
    {
      "key": "e_1_2_6_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.4319/lo.2002.47.5.1562"
    },
    {
      "key": "e_1_2_6_27_1",
      "first-page": "175",
      "volume-title": "Handbook of Methods in Aquatic Microbial Ecology.",
      "author": "Olson R.J.",
      "year": "1993"
    },
    {
      "key": "e_1_2_6_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.70.9.5426-5433.2004"
    },
    {
      "key": "e_1_2_6_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.68.6.3094-3101.2002"
    },
    {
      "key": "e_1_2_6_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/35075041"
    },
    {
      "key": "e_1_2_6_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.65.3.1259-1267.1999"
    },
    {
      "key": "e_1_2_6_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1112632"
    },
    {
      "key": "e_1_2_6_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0600540103"
    },
    {
      "key": "e_1_2_6_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/AEM.65.6.2585-2591.1999"
    },
    {
      "key": "e_1_2_6_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00221287-147-7-1731"
    },
    {
      "key": "e_1_2_6_36_1",
      "volume-title": "Nutrient Analysis Techniques.",
      "author": "Woodward E.M.S.",
      "year": "1994"
    },
    {
      "key": "e_1_2_6_37_1",
      "first-page": "92",
      "article-title": "Nanomolar detection of phosphate and nitrate using liquid waveguard technology",
      "volume": "83",
      "author": "Woodward E.M.S.",
      "year": "2002",
      "journal-title": "EOS"
    },
    {
      "key": "e_1_2_6_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.2307/1932984"
    },
    {
      "key": "e_1_2_6_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.289.5480.759"
    },
    {
      "key": "e_1_2_6_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/cyto.a.20332"
    },
    {
      "key": "e_1_2_6_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3354/ame040241"
    },
    {
      "key": "e_1_2_6_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0079-6611(00)00008-2"
    },
    {
      "key": "e_1_2_6_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.femsec.2004.06.009"
    },
    {
      "key": "e_1_2_6_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/plankt/fbl059"
    },
    {
      "key": "e_1_2_6_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1462-2920.2007.01246.x"
    }
  ],
  "container-title": "Environmental Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1462-2920.2007.01324.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "http://onlinelibrary.wiley.com/wol1/doi/10.1111/j.1462-2920.2007.01324.x/fullpdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        9,
        28
      ]
    ],
    "date-time": "2023-09-28T16:15:43Z",
    "timestamp": 1695917743000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://sfamjournals.onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2007.01324.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2007,
        5,
        28
      ]
    ]
  },
  "references-count": 44,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2007,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1462-2920.2007.01324.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1462-2920.2007.01324.x",
  "relation": {},
  "ISSN": [
    "1462-2912",
    "1462-2920"
  ],
  "subject": [],
  "container-title-short": "Environmental Microbiology",
  "published": {
    "date-parts": [
      [
        2007,
        5,
        28
      ]
    ]
  },
  "assertion": [
    {
      "value": "2007-05-28",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}