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ARTICLE

Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance

F. Partensky, W. R. Hess, D. Vaulot
F. Partensky
Station Biologique, CNRS, INSU et Université Pierre et Marie Curie, F-29680 Roscoff, France, and
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W. R. Hess
Humboldt-Universität Berlin, Institut für Biologie/Genetik, D-10115 Berlin, Germany
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D. Vaulot
Station Biologique, CNRS, INSU et Université Pierre et Marie Curie, F-29680 Roscoff, France, and
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DOI: 10.1128/MMBR.63.1.106-127.1999
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Figures

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  • Fig. 1.
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    Fig. 1.

    First records of the occurrence ofProchlorococcus. (A) Electron microscope photograph of “type II cells” from deep samples of the North Atlantic ocean. Reprinted from reference 63 with permission of the publisher. ce, cell envelope; pb, polyhedral bodies; th, thylakoids. Scale bar, 0.5 μm. (B) Analysis of a pigment extract obtained by normal-phase HPLC showing the “unknown Chl a derivative,” indicated by a star. Reprinted from reference37 with permission of the publisher.

  • Fig. 2.
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    Fig. 2.

    Analysis of natural Prochlorococcuspopulations by flow cytometry. (Top) Side scatter (a function of cell size) plotted against red fluorescence of chlorophyll. (Bottom) Orange fluorescence of phycoerythrin plotted against red fluorescence of chlorophyll. All scales are 4-decades logarithmic from 1 to 10,000 (arbitrary units). (Left) Typical surface-layer sample (45 m, deep Equatorial Pacific, 7°S, 150°W, collected 10 November 94).Synechococcus is easily distinguished fromProchlorococcus by its orange phycoerythrin fluorescence. (Middle) Typical deep sample (105 m deep, Equatorial Pacific, 7°S, 150°W, collected 10 November 94). Synechococcus is virtually absent, and the chlorophyll fluorescence ofProchlorococcus is much higher than near the surface (compare the fluorescence of Prochlorococcus and that of the standard beads). Note also the weak orange fluorescence displayed byProchlorococcus at this depth. (Right) Example of twoProchlorococcus populations coexisting at the same depth (80 m deep, Mediterranean Sea, 37°5′N, 16°52′E, collected 20 June 1996).

  • Fig. 3.
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    Fig. 3.

    Locations of some of the availableProchlorococcus strains (see Table 1).

  • Fig. 4.
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    Fig. 4.

    Electron micrographs of longitudinal and cross sections of Prochlorococcus strain MIT9313 showing tightly appressed thylakoids at the periphery of the cell. Scale bar, 0.1 μm. Unpublished photographs courtesy of C. Ting, J. King, and S. W. Chisholm.

  • Fig. 5.
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    Fig. 5.

    Vertical distributions from bright and dimProchlorococcus populations in the subtropical Pacific Ocean off Hawaii. The insert represents the vertical profile of side scatter and red chlorophyll fluorescence of the totalProchlorococcus population measured by flow cytometry. Adapted from reference 17 with permission of the publisher.

  • Fig. 6.
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    Fig. 6.

    Diagram showing the thylakoid proteins inProchlorococcus and their putative organization by homology to the photosynthetic apparatus of cyanobacteria. The proteins whose genes have been sequenced partially or totally are shown in dark gray (see Table 3), and those which have been characterized only by immunoblotting (35, 90, 132) are shown in light gray. Although phycoerythrin is present in some strains such as SS120, it is not clear whether it is integrated in phycobilisomes, which, if present, would be very scarce. PS I is probably organized in trimers (35), but only one monomer is shown. The insert shows a detail of the Pcb protein which includes six transmembrane hydrophobic domains. For the electron transport chain, only the cytochromeb6-f complex is shown because the existence of other components (such as NADH dehydrogenase and plastoquinone) has not been demonstrated yet. Other probable components of the photosynthetic apparatus such as cytochrome oxidase or ATP synthase are not shown either, since they are still uncharacterized inProchlorococcus. Abbreviations: CP, chlorophyll-protein complex; Cyt, cytochrome; OEC, oxygen evolving complex.

  • Fig. 7.
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    Fig. 7.

    Concentrations Prochlorococcus integrated over the water column throughout the world oceans. Based on data from Table 5.

  • Fig. 8.
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    Fig. 8.

    Relationship between Prochlorococcusintegrated concentrations and surface temperature (A) and surface nitrate concentrations (B). Based on data from Table 5.

  • Fig. 9.
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    Fig. 9.

    Vertical distributions of Prochlorococcus (A) and Synechococcus (B). Based on data from Table 5.

  • Fig. 10.
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    Fig. 10.

    Typical vertical distributions ofProchlorococcus and Synechococcus. (A and B) Surface layer maximum. (C and D) Deep maximum. (E and F) Uniform distribution over the euphotic zone. (A and B) North tropical Atlantic, EUMELI3 cruise (129). (A) EU site, off the coast of Mauritania (20°N, 18°W). (B) MESO site (18°N, 21°W). (C) North Atlantic 30°N, 23°W (11). (D) Eastern Mediterranean Sea, 34°N 18°E, MINOS cruise (176). (E) Equatorial Pacific 150°W, 5°S (174). (F) Tropical Pacific 150°W, 16°S (174). (D and F) Prochlorococcus chlorophyll fluorescence was too weak to be detected at the surface.

  • Fig. 11.
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    Fig. 11.

    Phylogenetic relationship betweenProchlorococcus isolates and cyanobacteria inferred from 16S rRNA gene sequences. Reprinted from reference 166with permission of the publisher.

Tables

  • Figures
  • Table 1.

    Prochlorococcus strains isolated in culture for which published data are available

    StrainDerived cloneOther nameOriginDateaLatitudeLongitudeDepth (m)IsolatorRemarksReference(s)
    SARGLGSargasso Sea30/5/8828°59′N64°21′W120B. PalenikFirst strain to be isolated131
    SS120CCMP 1375L. R. MooreObtained by serial dilution20, 107
    PCC 9511R. RippkaFirst axenic strain143
    MEDDVNW Mediterranean8/1/8943°12′N6°52′E5D. Vaulot, F. Partensky131
    MED4CCMP 1378L. R. MooreObtained by serial dilution20, 107
    NATL1FP12N Atlantic1/4/9037°39′N40°1′W30F. Partensky131
    NATL2FP5N Atlantic1/4/9038°59′N40°33′W30F. Partensky145, 166
    MIT9107S Pacific8/8/9114°60′S134°60′W25J. A. Dusenberry166
    TATL 1EUM11E Tropical Atlantic19/10/9120°57′N31°6′W20F. Partensky145, 166
    TATL 2EUM17E Tropical Atlantic21/10/9120°25′N31°8′W30F. Partensky145, 166
    GP2W Pacific10/9/928°32′N136°31′E150A. Shimada155, 156
    SBSugura Bay, Japan21/10/9235°0′N138°30′E40A. Shimada156, 157
    PAC 1N Tropical Pacific1/4/9222°45′N158°0′W100L. Campbell145, 166
    MIT9201S Pacific26/9/9211°60′S145°25′W0B. Binder106
    MIT9202S Pacific26/9/9211°60′S145°25′W79B. Binder106
    MIT9211Equatorial Pacific10/4/920140°W83R. J. Olson106
    MIT9215Equatorial Pacific3/9/920140°W0B. Binder106
    MIT9302Sargasso Sea15/7/9334°45′N66°11′W100L. MooreSorted by flow cytometry 108
    MIT9303Sargasso Sea15/7/9334°45′N66°11′W100L. MooreSorted by flow cytometry 108, 166
    MIT9312N Atlantic17/7/9337°30′N68°14′W135L. MooreSorted by flow cytometry 108
    MIT9313N Atlantic17/7/9337°30′N68°14′W135L. MooreSorted by flow cytometry 108
    AS9601Arabian Sea1/11/9519°12′N67°10′E50R. J. Olson150
    • ↵a Day/month/year.

  • Table 2.

    Composition of media used for growing Prochlorococcusa

    ComponentConcn of component inb:
    CPTC-based (A)K/10-Cu (B)PC (C)PRO2 (D)PCR-S11 (E)
    Nutrients
     Urea20 μM50 μM100 μM
     NH4ClB,C,D or (NH4)2SO4E50 μM50 μM50 μM400 μM
     β-glycerol-phosphateA,C (or NaH2PO4)B,D,E10 μM10 μM10 μM10 μM50 μM
    Buffer
     HEPES1 mM
    Chelator/trace metals
     CPTC100 μM
     EDTA-Na211.7 μM11.7 μM1.2 μM8 μM
     FeSO4A or FeCl3B,C,D,E0.1 μM1.2 μM1.2 μM1.2 μM8 μM
     MnCl2A,B,C,D or MnSO4E10 nM90 nM90 nM90 nM30 nM
     ZnCl2B,C,D or ZnSO4E8 nM8 nM8 nM3 nM
     CoCl2B,C,D [or Co(NO3)2]E5 nM5 nM5 nM1.5 nM
     Na2MoO4A,B,C,D or (NH4)6 Mo7O24E10 nM3 nM3 nM3 nM1.5 nM Mo
     Na2SeO3B,C,D or SeO2E10 nM10 nM10 nM1.5 nM
     NiSO4 or NiCl2D,E10 nM10 nM1.5 nM
     Na2WO40.3 nM
     KBr3 nM
     KI1.5 nM
     Cd(NO3)21.5 nM
     CuSO41.5 nM
     Cr(NO3)30.3 nM
     VOSO40.3 nM
     KaI(SO4)23 nM
     H3BO3150 nM
    Vitamins
     Thiamine-HCl10 μM
     Biotin50 nM
     B1250 nM7 nM
    • ↵a When different forms of a chemical are used in different media, a letter code (A through E) is used to indicate which form is used in which medium.

    • ↵b CPTC-based medium (20), K/10-Cu (20), PC (2), PRO2 (105), and PCR-S11 (142) are described elsewhere.

  • Table 3.

    Genes sequenced in Prochlorococcus

    CategoryGene nameMolecule encodedLocalization or functionEMBL/GenBank accession no.Reference(s)
    PhotosynthesiscpeYPhycoerythrobilin, phycourobilin lyase?Light harvesting?AJ00123052
    cpeZPhycoerythrobilin, phycourobilin lyase?Light harvesting?AJ00123052
    mpeXBile pigment biosynthesis, coupling?Light harvesting?AJ00123052
    orf463Assembly of light-harvesting structures?Light harvesting?AJ00123052
    pcbChl a2 and Chl b2antennaPS II antennaU57660 , U5766177
    petBb -type cytochromeCytochrome b6-f complexAF001487 –AF001489166
    petDSubunit IVCytochrome b6-f complexAF001487 –AF001489166
    cpeAPhycoerythrin III α subunitLight harvesting?Z68890 , AJ00123055
    cpeBPhycoerythrin III β subunitLight harvesting?Z68890 , AJ00123055
    ppeCLinker polypeptide of phycoerythrinLight harvesting?Z92525 , AJ00123054
    psaAPsaAPS I core167
    psaBPsaBPS I core167
    psaFSubunit PsaF of PS IBinding of plastocyanin?167
    psaISubunit PsaI of PS ITrimerization of PS IZ98595 ,AJ002427168
    psaJSubunit PsaF of PS IBinding of plastocyanin?167
    psaLSubunit PsaL of PS ITrimerization of PS IZ98595 , AJ002427168
    psbAD1PS II coreZ4920157
    psbBCP47Internal antenna of PS IIAF001481 –AF001485166
    rbcLLarge subunit of RubiscoCarbon assimilationU93857 , U9385852, 133, 155
    General metabolismaroCChorismate synthaseAmino acid metabolismZ4920151
    aspAAspartoacylaseAmino acid metabolismZ8011051
    cpn60Chaperonin-60Protein foldingZ3773052
    dapADihydrodipicolinate synthaseAmino acid metabolismZ37733 , Z6812695
    rpoC1DNA-dependent RNA polymeraseBiosynthesis of RNAZ11160125
    rnpBRNase P ribozymeRNA processingY12789 , AJ00113553
    rncRNase IIIRNA processingAJ00113552
    rrn16S rRNAProtein synthesisX63140 ,AF001466 – AF001476165, 166
    trnRTransfer RNA arginine (CCU)TranslationY12789 ,AJ00113553
    Nutrient uptakepstSPhosphate-binding proteinPhosphorus assimilationU75514146
    Cell cyclednaADnaADNA replicationU44977139
    ftsZFtsZCell divisionAJ01102558
    uvrDDNA helicaseDNA replication and DNA repair processesAJ00123052
  • Table 4.

    Codon usage in P. marinus CCMP 1375 (6,365 codons)a

    Amino acidFirst and second positionsNo. of occurrences at third position
    ACGT
    AlaGC2477034255
    ArgCG2716552
    ArgAG12141
    AsnAA89222
    AspGA86259
    CysTG2143
    GlnCA15877
    GluGA244101
    GlyGG15210766167
    HisCA44131
    IleAT14572294
    LeuTT236106
    LeuCT1193629199
    LysAA239100
    PheTT123190
    ProCC1032210123
    SerTC1242720150
    SerAG65103
    ThrAC1116511137
    TyrTA50111
    ValGT1154036203
    StopTA64
    StopTG6
    Total2,1539336402,639
    • ↵a The absolute number of occurrences of each codon was computed from 17 genes (see Table 3 for references):aspA, cpeY, cpeZ cpn60,dapA, dnaA, mpeX, pcb,ppeA, ppeB, psaA, psaB,psbA, ppeC, rnc, uvrD, andorf463. The noninformative Trp and Met codons are omitted. For uvrD, only the first 518 codons are known.

  • Table 5.

    Oceanographic data used to construct Fig. 7 to 10

    Ocean or seaAreaCruiseShipYr(s)MonthsReference
    Atlantic OceanNorth Atlantic87022CSSHudson1987June88
    88026CSSHudson1988Sept87
    89003CSSBaffin1989Apr86
    NIOZ Natl 89RVTyro1989Aug–Sept179
    91001CSSHudson1991Apr81
    92037CSSHudson1992Sept83
    93002CSSHudson1993May83
    NOAA 93NOAA Malcolm Baldbridge1993July–Aug11
    Delaware 95RV Cape Henlopen1995Apr84
    95016CSSHudson1995July84
    Sargasso SeaCHLOMAXNOSuroit1987Sept–Oct116
    Lopez 96Launch1995June85
    Tropical AtlanticEUMELI 3NOAtalante1991Oct129
    EUMELI 4NOAtalante1992June129
    EUMELI 5NOAtalante1992Dec129
    Indian OceanArabian SeaArabian TTN043RVThomson1995Jan14
    Arabian TTN045RVThomson1995Mar–Apr14
    Arabian TTN049RVThomson1995July–Aug117
    Indian Ocean and Red SeaNIOZ Indian1992–1993May–Feb181
    Pacific OceanEquatorial PacificEQPAC TT007RVThomson1992Feb–Mar74
    EQPAC TT008RVThomson1992Mar–Apr7
    EQPAC TT008DRVThomson1992Mar–Apr27
    EQPAC TT011RVThomson1992Aug–Sept74
    EQPAC TT012RVThomson1992Sept–Oct27
    SURTROPAC 17NONoroit1992Aug8
    OLIPACNOAtalante1994Nov115
    FLUPACNOSuroit1994Sept–Oct115
    Tropical PacificHOTMoana Wave1990–199415
    Coast of JapanSuruga BayBoat1992–1993May–Oct157
    South PacificChile 95RVSonne1995June85
    West Tropical PacificAustraliaRVSohgen-Maru1990Nov–Dec154
    Mediterranean SeaEROS Discovery 89HMSDiscovery1989Jan178
    EROS Bannock 89Bannock1989July128
    POEM 91RV Bilim/RV Shikmona1991Oct89
    Eddy 92RV Shikmona1992Mar193
    EROS Valdivia 92Valdivia1992Mar97
    EROS Discovery 93HMSDiscovery1993July4
    Malaga 93Launch1993Jan33
    MINOSNOSuroit1995Jun176
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Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance
F. Partensky, W. R. Hess, D. Vaulot
Microbiology and Molecular Biology Reviews Mar 1999, 63 (1) 106-127; DOI: 10.1128/MMBR.63.1.106-127.1999

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Prochlorococcus, a Marine Photosynthetic Prokaryote of Global Significance
F. Partensky, W. R. Hess, D. Vaulot
Microbiology and Molecular Biology Reviews Mar 1999, 63 (1) 106-127; DOI: 10.1128/MMBR.63.1.106-127.1999
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KEYWORDS

Cyanobacteria
Seawater

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