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Review

Ecological Genomics of Marine Picocyanobacteria

D. J. Scanlan, M. Ostrowski, S. Mazard, A. Dufresne, L. Garczarek, W. R. Hess, A. F. Post, M. Hagemann, I. Paulsen, F. Partensky
D. J. Scanlan
1Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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  • For correspondence: d.j.scanlan@warwick.ac.uk
M. Ostrowski
1Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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S. Mazard
1Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom
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A. Dufresne
2UPMC-Université Paris 06, Station Biologique, BP 74, 29682 Roscoff Cedex, France
3CNRS, UMR 7144, Groupe Plancton Océanique, BP 74, 29682 Roscoff Cedex, France
4Université Rennes 1, UMR 6553 EcoBio, IFR90/FR2116, CAREN, 35042 Rennes, France
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L. Garczarek
2UPMC-Université Paris 06, Station Biologique, BP 74, 29682 Roscoff Cedex, France
3CNRS, UMR 7144, Groupe Plancton Océanique, BP 74, 29682 Roscoff Cedex, France
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W. R. Hess
5University Freiburg, Faculty of Biology, Schänzlestrasse 1, D-79104 Freiburg, Germany
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A. F. Post
6H. Steinitz Marine Biology Laboratory, The Interuniversity Institute for Marine Science, POB 469, Eilat 88103, Israel
7Marine Biological Laboratory, Woods Hole, Massachusetts
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M. Hagemann
8Universität Rostock, Inst. Biowissenschaften, Pflanzenphysiologie, Einsteinstr. 3, D-18051 Rostock, Germany
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I. Paulsen
9Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, New South Wales, Australia
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F. Partensky
2UPMC-Université Paris 06, Station Biologique, BP 74, 29682 Roscoff Cedex, France
3CNRS, UMR 7144, Groupe Plancton Océanique, BP 74, 29682 Roscoff Cedex, France
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DOI: 10.1128/MMBR.00035-08
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  • FIG. 1.
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    FIG. 1.

    Neighbor-joining tree, based on 16S rRNA gene sequences, indicating the phylogenetic relationships among marine picocyanobacteria that are the subject of this review. Bootstrap values of >70% are shown. Strains with sequenced genomes are in boldface.

  • FIG. 2.
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    FIG. 2.

    Genome sizes of marine picocyanobacteria compared to a representative selection of other cyanobacteria.

  • FIG. 3.
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    FIG. 3.

    Genome plot of recently acquired genomic islands in marine Synechococcus and Prochlorococcus strains. For each genome predicted islands are highlighted in gray, except for the phycobilisome gene cluster, which is highlighted in orange. The frequency with which an ortholog appears among the 14 genomes (11 Synechococcus and three Prochlorococcus) of the curated Cyanorak database (http://www.sb-roscoff.fr/Phyto/cyanorak/ ) is represented by a black bar (a core gene is present in 14 genomes). Giant ORFs are highlighted in blue. Tetranucleotide frequency in overlapping 5,000 bp intervals was transformed by principal-component analysis, and the deviation in tetranucleotide frequency is plotted in the box below each genome as the first principal component (PC1). The positions of tRNA genes (purple bars) and mobility genes, such as those encoding phage integrases and transposases, are also indicated (green bars). While for marine Synechococcus strains and Prochlorococcus sp. strain MIT9313 the deviation in tetranucleotide frequency correlates well with genomic regions bounded by mobility genes and containing unique genes or orthologs common to few genomes, for the streamlined, rapidly evolving A+T-rich genomes of Prochlorococcus there is a poor correlation between tetranucleotide frequency and predicted islands. (Modified from reference 56 with permission of the publisher.)

  • FIG. 4.
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    FIG. 4.

    Dot blot hybridization data showing the distribution of HLI, HLII, and LL Prochlorococcus ecotypes and Synechococcus clades II to IV in the euphotic zone along an Atlantic Meridional cruise track (AMT 15). Contour plots indicate the percent relative hybridization. For each panel the y axis is the light intensity (percent surface irradiance) and the x axis the latitude (degrees north or south of the equator). Black contour lines indicate the depth in meters, and black dots represent sampling points. (Adapted from reference 340 with permission of Wiley-Blackwell.)

  • FIG. 5.
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    FIG. 5.

    Synechococcus pigment types and associated phycobilisome structures. (A) Photograph of cultures representative of the three main pigment types (1 to 3) and subtypes (3a to 3c). Pigment type 3d corresponds to type IV chromatic adapters that modify their pigmentation from subtype 3b (in green light) to 3c (in blue light). (B) Models of the phycobilisome structures of the three main pigment types. (Adapted from reference 263 with permission of the publisher.)

  • FIG. 6.
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    FIG. 6.

    Neighbor-joining tree indicating the phylogenetic relatedness of the different peroxiredoxins found in marine picocyanobacteria. The Cyanorak cluster numbers are indicated for each peroxiredoxin type. Color coding: green, Prochlorococcus; orange, marine Synechococcus; blue, other cyanobacteria.

  • FIG. 7.
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    FIG. 7.

    Phylogenetic analysis of PII proteins in unicellular marine (Synechococcus and Prochlorococcus) and unicellular freshwater (Synechocystis sp. strain PCC6803 and Synechococcus elongatus PCC7942) cyanobacteria. The two PII proteins of E. coli were chosen as outgroups. Bootstrap values are given at nodes if at least 60. The two paralogs of Synechococcus sp. strain WH5701 are indicated in boldface. Color coding: green, Prochlorococcus; orange, marine Synechococcus; blue, other cyanobacteria; black, E. coli.

  • FIG. 8.
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    FIG. 8.

    Multiple sequence alignment of cyanobacterial PII of marine Synechococcus strains (Syn), selected Prochlorococcus strains (Pro), and the two freshwater strains Synechocystis sp. strain PCC6803 and Synechococcus elongatus PCC7942 and of the two E. coli PII proteins. Sites that belong to a previously suggested cyanobacterial signature (216) are indicated by arrows. #, the functionally relevant residue Arg45, required for interaction with NAGK; $, Ser49, which becomes phosphorylated in S. elongatus PCC 7942 (78). Asterisks and numbers above the sequences mark every 10th position.

  • FIG. 9.
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    FIG. 9.

    Partial alignment of a genomic fragment containing the gene clusters for assimilation pathways of major N sources for marine Synechococcus strains organized according to phylogenetic clusters (56), i.e., urea (blue), nitrate (green), nitrite (pink), and cyanate (yellow), in addition to N metabolism genes (purple), other nonrelated genes (white), and fully conserved genes flanking this region (red). Genes encoding the enzyme central to each pathway are in dark color, while genes involved in accessory functions (acquisition/cofactor biosynthesis) are in light color. Dotted lines and block arrows indicate mobile fragments of 10 to 25 genes in size that are subject to deletion/insertion events in different lineages. The upper panel presents the relevant genomic regions in Synechococcus sp. strain WH5701.

  • FIG. 10.
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    FIG. 10.

    Neighbor-joining tree based on the amino acid sequences of PstS and SphX from marine and freshwater cyanobacteria. Three families of phosphate-binding proteins are evident in marine Synechococcus (PstSI, PstSII, and SphX), which suggests that these proteins are functionally distinct (e.g., they may display different affinities for the same substrate). The PstS sequences of HL and LL Prochlorococcus strains, freshwater cyanobacteria, and marine Synechococcus strains form separate clusters, while the SphX sequences all cluster together. The tree was constructed from an alignment using Clustal X v1.83. The bootstrap values were obtained through 1,000 repetitions. The tree was rooted on the PstS sequence of E. coli K-12. Sequences were extracted from BLAST searches of GenBank (www.ncbi.nlm.nih.gov/BLAST ) or using Cyanorak (http://www.sb-roscoff.fr/Phyto/cyanorak/ ) or Cyanobase (www.kazusa.or.jp/cyanobase/ ). The scale bar represents 10 substitutions per 100 nucleotides. Color coding: green, Prochlorococcus; orange, marine Synechococcus; blue, other cyanobacteria; black, cyanophage sequences.

  • FIG. 11.
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    FIG. 11.

    Schematic representation of the different domain structures of phosphatases present in marine and freshwater cyanobacterial genomes. At least five different families of phosphatases are represented. Notable features include the variable domain structure of the large PhoA-type phosphatases which contain UshA and 5′ nucleotidase domains. SynWH7803_0111 includes an N-terminal insertion of a phytase-like domain (COG4222), homologous to SYNW0762, which is also represented in MED4_ 0708 and MIT9312_0720. COG3391 is a potential Zn-binding domain, which suggests a requirement for Zn as a cofactor. PhoX (332) and PhoD (64) homologs are also represented in a subset of strains. The approximate molecular mass is indicated by the scale at the bottom. Color coding of sequence names: green, Prochlorococcus; orange, marine Synechococcus; blue, other cyanobacteria; black, other bacteria. a, this ORF contains a potential frameshift; b, this ORF is truncated and hence is a probable pseudogene; c, this ORF spans only the N-terminal portion of PhoX; d, this ORF is truncated at its N terminus. (Adapted from reference 192 with permission of the publisher.)

  • FIG. 12.
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    FIG. 12.

    Multiple-sequence alignment, using ClustalX v1.83, of the N-terminal region of the PhoR histidine kinase in marine picocyanobacteria. Differences in the N-terminal sequences suggest alternative subcellular locations for PhoR in different strains of picocyanobacteria. Shown at the bottom is the probability of a transmembrane domain for the first 100 amino acids (aa) of the N-terminal regions (predicted by the TMHMM server) for the three groups of organisms defined in the text.

  • FIG. 13.
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    FIG. 13.

    Phylogenetic relationships among CRP family regulators of marine picocyanobacteria. The identified CRP regulators form four distinct clusters, i.e., NtcA, cluster 2049, cluster 1390, and PtrA, with decreasing levels of conservation and a further diverse group mostly composed of cluster 2546. Color coding: green, Prochlorococcus; orange, marine Synechococcus.

  • FIG. 14.
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    FIG. 14.

    Marine picocyanobacterial genomic regions centered on a potential Fe regulator of the CRP family (cluster 1390). The genomic region for Synechococcus sp. strain CC9605 is essentially the same as for CC9902/BL107 except that petF, encoding ferredoxin, is located downstream of ferritin and upstream of the hypothetical proteins. For Synechococcus at least, these genes are located in a genomic island (WH7805-ISL3, BL107-ISL6, CC9605-ISL12, CC9902-ISL-11, RS9916 ISL4). futA, ABC-type iron transporter, periplasmic iron-binding protein; futB, ABC-type iron transporter, ATP-binding component; futC, ABC-type iron transporter, membrane component; feoB, ferrous iron uptake protein; isiB, flavodoxin; som, porin; trxB, thioredoxin reductase; A, putative Fe-regulated hydroxylase; B, ABC molybdenum transporter-binding component; C, HupE hydrogenase component; chp, conserved hypothetical protein.

  • FIG. 15.
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    FIG. 15.

    Phylogenetic relationships among marine picocyanobacterial sigma factors. A total of 136 sigma factors from 22 strains of marine picocyanobacteria (11 Synechococcus [Syn] and 11 Prochlorococcus [Pro] strains) were analyzed. The vegetative major sigma factor SigA and the four alternative type 2 sigma factors from Synechocystis sp. strain PCC6803 were included for orientation. Clades A to E refer to different classes of closely related sigma factors from picocyanobacteria. Bootstrap numbers are given for major nodes. Color coding: green, Prochlorococcus; orange, marine Synechococcus; blue, other cyanobacteria. (See Fig. 16 for more information on clade D.)

  • FIG. 16.
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    FIG. 16.

    Phylogenetic relationships among clade D (Fig. 15) type 2 alternative sigma factors. All Synechococcus factors are indicated in boldface. For easier identification, GenBank tags are given and the respective part indicating the strain is underlined. The genes encoding these proteins are probably rapidly evolving, since a series of independent duplications (black dots) in the progenitors of single strains or two strains, respectively, is suggested by similarity and phylogenetic analysis. The proteins BL107_06099 and SynCC9902_0139 differ only by a single conservative exchange (identity at DNA level, 87%). Bootstrap numbers are given for all nodes. Color coding: green, Prochlorococcus; orange, marine Synechococcus.

  • FIG. 17.
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    FIG. 17.

    DNA integration into the tmRNA gene of Synechococcus sp. strain WH8102. The start of genomic island 1 is indicated, and the positions of three phage integrase genes are given by the blue boxes, together with their sequence ID. The order of ssrA acceptor (tRNA-like) and coding (mRNA-like) segments is reversed in picocyanobacteria compared to most other bacteria (94). The genetic element Synw12X (325) is integrated into the 3′ end of ssrA, far from the tRNA-like segment. Within the triplicated 33-bp attB sequences resides an inverted repeat able to fold into a secondary structure (arrows). These elements exhibit compensatory base pair changes, indicating the functional importance of the stem-loop formed by this repeat.

  • FIG. 18.
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    FIG. 18.

    Predicted secondary structures of the six selected ncRNAs from Synechococcus sp. strain CC9311 belonging to the Yfr2 to -5 class. A characteristic motif is the conserved sequence 5′-GAAAC(U/A)AGG(C/U/A)AA-3′ in the single-stranded loop region labeled by the doughnut. This motif is similarly conserved between all members of this ncRNA class throughout the cyanobacterial radiation. The structures were drawn with mfold (339).

Tables

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  • TABLE 1.

    Summary of the different Prochlorococcus and Synechococcus genomes sequenced to date

    Genus and strainRCC no.aSubcluster or ecotypebClade no.cGenome size (Mb)No. of protein-coding genesGC (%)Status and accession no.dReference
    Synechococcus
        CC931110865.1BI2.612,89252[C]:CP000435 214
        CC96057535.1AII2.512,64559[C]:CP000110 56
        WH81025395.1AIII2.432,51959[C]:BX548020 212
        CC99025.1AIV2.232,35854[C]:CP000097 56
        BL1075155.1AIV2.282,55354[WGS]:AATZ00000000 56
        WH78037525.1BV2.372,58660[C]:CT971583 56
        WH780510855.1BVI2.622,93457[WGS]:AAOK00000000 56
        RS99175565.1BVIII2.582,82065[WGS]:AANP00000000 56
        RS99165555.1BIX2.663,00960[WGS]:AAUA00000000 56
        WH570110845.22.863,12966[WGS]:AANO00000000 56
        RCC3073075.32.222,58361[C]:CT978603 56
    Prochlorococcus
        MED4151HLHLI1.661,71631[C]:BX548174 239
        MIT9515HLHLI1.701,90831[C]:CP000552 136
        MIT9301HLHLII1.641,90731[C]:CP000576 136
        AS9601HLHLII1.671,92631[C]:CP000551 136
        MIT9215HLHLII1.741,98931[C]:CP000825 136
        MIT9312HLHLII1.711,96231[C]:CP000111 136
        NATL1ALLLLI1.862,20135[C]:CP000553 136
        NATL2A314LLLLI1.842,15835[C]:CP000095 136
        SS120154LLLLII1.751,88436[C]:AE017126 57
        MIT9211LLLLIII1.691,85538[C]:CP000878 136
        MIT9303LLLLIV2.683,02250[C]:CP000554 136
        MIT9313407LLLLIV2.412,27551[C]:BX548175 239
    • ↵ a RCC, Roscoff Culture Collection.

    • ↵ b 5.1A and 5.1B, subcluster number as defined in reference 56.

    • ↵ c For Synechococcus, clade number as defined in reference 83; for Prochlorococcus, ecotype number as defined in reference 136.

    • ↵ d [C]:, complete genome sequence; [WGS]:, incomplete genome sequence (estimated coverage, >99.8%).

  • TABLE 2.

    Overview of the broad ecological conditions under which specific picocyanobacterial clades/ecotypes are most frequent

    Species (subcluster) and cladeEcological conditions of largest relative abundanceReferences
    Synechococcus (5.1)a
        ICoastal and/or temperate mesotrophic open ocean waters largely above 30°N and below 30°S 34, 340, 341
        IIOffshore, continent shelf, oligotrophic tropical or subtropical waters between 30°N and 30°S 2, 83-85, 294, 340, 341
        IIIUltraoligotrophic open-ocean waters 84, 85, 341
        IVCoastal and/or temperate mesotrophic open ocean waters largely above 30°N and below 30°S 34, 340, 341
        V/VI/VIIbRelatively wide distribution but in low abundance in various oceanic waters; have been seen to dominate mesotrophic upwelling regions, e.g., Arabian Sea, while clade VII genotypes specifically have been shown to dominate in the Costa Rica upwelling dome 39, 84, 245, 341
    Prochlorococcus
        HLI (eMED4)More weakly stratified surface waters, particularly between 35° and 48°N and 35° and 40°S 26, 128, 321
        HLII (eMIT9312)Strongly stratified surface waters, particularly tropical and subtropical regions between 30°N and 30°S 3, 26, 128, 321, 322
        LLI (eNATL2A)Occupies an “intermediate” position in the water column in stratified waters; at high latitude (above 40°N/30°S), these cells can be found throughout the euphotic zone up to the surface 128, 335, 336
        LLIV (eMIT9313)Widely distributed within the 40°N to 35°S latitudinal range but largely restricted to the deep euphotic zone 84, 128, 321, 322, 335, 336, 340, 341
        LLII (eSS120) and LLIII (eMIT9211)Present in deep waters at very low concentrations 90, 128, 335
    • ↵ a The low levels of environmental detection of subcluster 5.1 clades VIII and IX, subcluster 5.2 (WH5701), and subcluster 5.3 (RCC307, formerly subcluster 5.1 clade X) using oligonucleotide probes thus far precludes generalizations about the ecological distributions of these clades.

    • ↵ b Analyses of ecological distribution patterns for these lineages have largely used an oligonucleotide probe that detects these clades collectively.

  • TABLE 3.

    Distribution of genes involved in ROS protection and detoxification in marine picocyanobacterial genomes

    Genus and strain (clade)Presencea of:
    KatG, cluster 1897Cu/Zn SOD, cluster 1853Mn SOD, cluster 7995Ni SOD, cluster 1843Fe SOD, cluster 18241-Cys Prx, cluster 29252-Cys Prx, cluster 167Type II Prx, cluster 3802PrxQ, clusters 38, 812, 8024Gpx, cluster 308TxlA, cluster 471GrxCc, cluster 445Rub/HoxR, clusters 269, 3931RbrA, cluster 1682TrxA (m type), cluster 8028TrxB (x type), cluster 47Putative TrX, clusters 1171, 1233FTR systemNTR system, clusters 1301, 1904DpsA, cluster 1889
    FtrC, cluster 1648FtrV, cluster 1644
    Synechococcus
        CC9311 (I)−•−2b−−••3•••••••2••2d•
        CC9605 (II)••−•−−•−3•••••••2••2d−
        WH8102 (III)−−−•−−•−3•••••••2•••−
        CC9902 (IV)−•−•−−•−3•••••••2••2d−
        BL107 (IV)−•−•−−•−3•••••••2••2d−
        WH7803 (V)••−−•−•−3••••−••2••••
        WH7805 (VI)••−−•−•−3••••−••2••••
        RS9917 (VIII)•−•−•••−3••••••••••••
        RS9916 (IX)••−−•−•−3•••••••2••••
        WH5701 (5.2)•−•−•••−3•••••••2••••
        RCC307 (5.3)••−−•••−3•••••••2••••
    Synechocystis sp. strain PCC6803••−−••••22•••−•••••••
    Prochlorococcus
        MED4 (HLI)−−−•−−•−3••••−•−2−−2d−
        MIT9515 (HLI)−−−•−−•−3••2•−•−2−−2d−
        AS9601 (HLII)−−−•−−•−3••••−•−2−−2d−
        MIT9215 (HLII)−−−•−−•−3••••−•−2−−2d−
        MIT9301 (HLII)−−−•−−•−3••••−•−2−−2d−
        MIT9312 (HLII)−−−•−−•−3••••−•−2−−2d−
        NATL1A (LLI)−−−•−−•−4••••−•−2−−2d−
        NATL2A (LLI)−−−•−−•−4••••−•−2−−2d−
        SS120 (LLII)−−−•−−•−2•••2−•−2−−2d−
        MIT9211 (LLIII)−−−•−−•−3••••−•−2−−2d−
        MIT9303 (LLIV)−−−•−−••3••••••−2−−••
        MIT9313 (LLIV)−−−•−−••3••••••−2−−••
    • ↵ a The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ b While one of these sodN genes appears to be cyanobacterial, the other copy has an abnormal percent GC content compared with the rest of the genome and is likely the result of a horizontal gene transfer event (60).

    • ↵ c All marine picocyanobacteria also possess a protein containing a glutaredoxin domain and a PD1-like DNA-binding domain (cluster 178).

    • ↵ d One of these proteins is a large NTR (or NTRC), i.e., thioredoxin reductase fused to a thioredoxin domain as recently identified in Arabidospis thaliana (257).

  • TABLE 4.

    Phyletic pattern of photolyases and DNA glycosylases potentially involved in the repair of thymine dimers in marine picocyanobacteria

    Genus and strain (clade)Presencea of:
    phrA, cluster 1330phrB, cluster 1584Photolyase-related protein, cluster 1460MTFH domain, cluster 1541FAD domain, cluster 1540FAD domain, cluster 3563PD DNA glycosylase, cluster 2679
    Synechococcus (all strains)•••••−−
    Prochlorococcus
        MED4 (HLI)•−•−−•−
        MIT9515 (HLI)•••−−•−
        AS9601 (HLII)•••−−•−
        MIT9215 (HLII)•••−−•−
        MIT9301 (HLII)•••−−•−
        MIT9312 (HLII)•••−−•−
        NATL1A (LLI)•−•−−•−
        NATL2A (LLI)•−•−−•−
        SS120 (LLII)−−−−−−•
        MIT9211 (LLIII)−−−−−−•
        MIT9303 (LLIV)−−−−−−•
        MIT9313 (LLIV)−−−−−−•
    • ↵ a •, present in single copy; −, absent.

  • TABLE 5.

    Distribution of gene orthologs in marine picocyanobacteria encoding proteins potentially involved in compatible solute synthesisa and transport

    Genus and strain (clade)Presenceb of:Compatible solute accumulationc
    ggpS, cluster 1610ggpP (stpA), cluster 1282ggtA, cluster 8069ggtB, cluster 1455ggtC, cluster 1454ggtD, cluster 1453proV, cluster 8061proW, cluster 1943proX, cluster 1944gpgP, cluster 1370gpgS, cluster 1368gbmt1, cluster 1941gbmt2, cluster 1942spsA, cluster 368spp, cluster 2483betP, cluster 1663
    Synechococcus
        CC9311 (I)••••••−−−••−−•−•NI
        CC9605 (II)••••••−−−••−−•−•NI
        WH8102 (III)••••••••••••••−•GG, GB
        CC9902 (IV)••••••−−−••−−•−•NI
        BL107 (IV)••••••−−−••−−•−•NI
        WH7803 (V)••••••••••••••−•GG, Suc, GB
        WH7805 (VI)••••••••••••••−•NI
        RS9917 (VIII)••••••••••••••−•NI
        RS9916 (IX)••••••••••••••−•NI
        WH5701 (5.2)••••••−−−−−−−•2−NI
        RCC307 (5.3)••••••−−−••−−•••NI
    Prochlorococcus
        MED4 (HLI)−•−−−−−−−••−−•−−NI
        MIT9515 (HLI)−•−−−−−−−••−−•−•NI
        AS9601 (HLII)−•−−−−−−−••−−•−−NI
        MIT9215 (HLII)−•−−−−−−−••−−•−−NI
        MIT9301 (HLII)−•−−−−−−−••−−•−−NI
        MIT9312 (HLII)−•−−−−−−−••−−•−−Suc, GGA
        NATL1A (LLI)−•−−−−−••−−•−−NI
        NATL2A (LLI)−•−−−−−−−••−−•−−Suc, GGA
        SS120 (LLII)−•−−−−−−−••−−•−−Suc, GGA
        MIT9211 (LLIII)−•−−−−−−−••−−•−−NI
        MIT9303 (LLIV)−••••••••−−•••−−NI
        MIT9313 (LLIV)−••••••••−−•••−−Suc, GB
    • ↵ a No clear homolog of functionally characterized trehalose biosynthetic genes from other bacteria could be found in these marine picocyanobacterial genomes.

    • ↵ b The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ c The ability to accumulate specific compatible solutes was analyzed by gas-liquid chromatography in ethanol extracts from selected strains (Klähn and Hagemann, unpublished data). NI, not investigated. Suc, sucrose.

  • TABLE 6.

    Cross-genome comparison of N metabolism gene contents among Prochlorococcus and Synechococcus strains

    Genus and strain (clade)Presencea of:
    ntcA, cluster 468amt, cluster 244amtb, cluster 8701glnA, cluster 103glnAb, cluster 2090, 2505, 6741, or 8855glnB, cluster 186glnBb, cluster 2023pipX, cluster 1044glsFc, cluster 134glsFb, cluster 9009gdhA, cluster 1539 or 3700ured, clusters 1358-1364speA, cluster 415speB, cluster 392 or 2247cynS, cluster 1552carAB, cluster 783 or 962dadA, cluster 377nadB, cluster 196thiO, cluster 417
    Synechococcus
        CC9311 (I)•••e•2•−••−•••••••••
        CC9605 (II)••−•−•−••−•••2•••••
        WH8102 (III)••−•−•−••−•e••2•••••
        CC9902 (IV)••−•−•−••−•••••••••
        BL107 (IV)••−•−•−••−•••••••••
        WH7803 (V)••−•2•−••−•−•••••••
        WH7805 (VI)••−•2•−••−•••••••••
        RS9917 (VIII)••−•2•−••−•f••••••••
        RS9916 (IX)••−•−•−••−•••••••••
        WH5701 (5.2)••−•4g2••••−••2−••••
        RCC307(5.3)••−•−••••−•••2•••••
    Prochlorococcus
        MED4 (HLI)••−•−••••−−••••••••
        MIT9515 (HLI)••••−••••−•−••−••••
        AS9601 (HLII)••−•−••••−−•••−••••
        MIT9215 (HLII)••−•−••••−••••−••••
        MIT9301 (HLII)••−•−••••−−•••−••••
        MIT9312 (HLII)••−•−••••−−•••−••••
        NATL1A (LLI)••−•−••••−−••••••••
        NATL2A (LLI)••−•−••••−−••••••••
        SS120 (LLII)••−•−••••−−−••−••••
        MIT9211 (LLIII)••−•−••••−−−••−••••
        MIT9303 (LLIV)••−•−••••−••••−••••
        MIT9313 (LLIV)••−•−••••−••••−••••
    • ↵ a The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ b amt, glnA, glnB, and glsF homologs.

    • ↵ c Synonyms gltS, gltB.

    • ↵ d ureABCDEFG.

    • ↵ e Frameshifted ORF.

    • ↵ f There is also a potential second copy of gdh encoded by RS9917_05900 (cluster 4952).

    • ↵ g One of these is interrupted by a transposase.

  • TABLE 7.

    Distribution of P- and arsenate-related gene orthologs in marine picocyanobacteria

    Genus and strain (clade)Presencea of:
    phoB/R, cluster 8015/1531ptrA, cluster 1606pstS,b cluster 23(1829)phoA/5′NDc (phoX)psip1,d cluster 2662pitA, cluster 6877phoU, cluster 5756arsR, cluster 1532arsC, cluster 1227arsB, cluster 1815
    Synechococcus
        CC9311 (I)−−•−−−−−•−
        CC9605 (II)••2−−−−•••
        WH8102 (III)••4 (1)4 (1)•−−•••
        CC9902 (IV)−−•−−−−−•−
        BL107 (IV)?e/−•2−−−−−•−
        WH7803 (V)••3 (1)2 (1)−−−•••
        WH7805 (VI)••32 (1)f−−−•••
        RS9917 (VIII)••5 (2)(1)−−−••2
        RS9916 (IX)••2−−−−••−
        WH5701 (5.2)••3 (1g)2 (1)−•−••−
        RCC307 (5.3)••4 (1)(1)−−••−•
    Synechocystis sp. strain PCC6803•−3 (1)•−−••••
    Prochlorococcus
        MED4 (HLI)•••••−−•••
        MIT9515 (HLII)−−•−−−−•−
        AS9601 (HLII)−−•−−−−•−
        MIT9215 (HLII)−−•−−−−•−
        MIT9301 (HLII)•−2−−−•••
        MIT9312 (HLII)•−••−−−••−
        NATL1A (LLI)•••−−−•••
        NATL2A (LLI)••••−−−•••
        SS120 (LLII)−•2−−−−••−
        MIT9211 (LLIII)−−•−−−−−•−
        MIT9303 (LLIV)−/••3h−−−•••
        MIT9313 (LLIV)•/Δi−2−−−−••−
    • ↵ a The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ b In parentheses is the number of gene copies phylogenetically most closely related to sphX; a single copy of pstA (cluster 165), pstB (cluster 817), and pstC (cluster 818) is present in all marine picocyanobacterial genomes except in Synechococcus sp. strain WH7805, where two copies of pstA exist.

    • ↵ c 5′ND, 5′ nucleotidase. All marine picocyanobacterial genomes so far examined also contain a dedA-like alkaline phosphatase gene (cluster 302). The phoA/5′ND group encompasses clusters 2917, 3430, 5181, 5416, 5811, 6036, 6582, and 9093. Another predicted phosphatase encompasses part of cluster 1164 and is related to a gene from Vibrio cholerae AAR99475 (phoX), the number of copies of which are indicated within parentheses.

    • ↵ d psip1 encodes a P starvation-inducible polypeptide of unknown function.

    • ↵ e In BL107_12310 several conserved residues in PhoB are altered, potentially suggesting a change of function.

    • ↵ f A predicted alkaline phosphatase gene in Synechococcus sp. strain WH7805 contains a stop codon which introduces a frameshift, resulting in ORFs WH7805_08937 and WH7805_08942; physiological studies showed no obvious alkaline phosphatase activity in this strain (S. Mazard and D. J. Scanlan, unpublished data).

    • ↵ g Another copy of sphX in Synechococcus sp. strain WH5701 is interrupted by a transposase.

    • ↵ h One of the pstS copies is a truncated version upstream of phoR.

    • ↵ i The phoR gene of MIT9313 contains two frameshifts.

  • TABLE 8.

    Distribution of Cu-related gene orthologs in marine picocyanobacterial genomes

    Genus and strain (clade)Presencea of:
    petE, cluster 1274cueO, cluster 2933 or 3002ctaA, cluster 65pacS, cluster 9116atx1bCd/Co/Hg/Pb/Zn-translocating P-type ATPase, cluster 9115 or 9117
    Synechococcus
        CC9311 (I)•••−−−
        CC9605 (II)•−•−−•
        WH8102 (III)•−•−−−
        CC9902 (IV)•••−−−
        BL107 (IV)•−•−−−
        WH7803 (V)•• (2)•−−−
        WH7805 (VI)•−•−−−
        RS9917 (VIII)•−•−−•
        RS9916 (IX)•−•−−−
        WH5701 (5.2)•−••−•
        RCC307 (5.3)−••−−−
    Synechocystis sp. strain PCC6803•−••••
    Prochlorococcus
        MED4 (HLI)•−•−−−
        MIT9515 (HLI)•−•−−−
        AS9601 (HLII)•−•−−−
        MIT9215 (HLII)•−•−−−
        MIT9301 (HLII)•−•−−−
        MIT9312 (HLII)•−•−−−
        NATL1A (LLI)•−•−−−
        NATL2A (LLI)•−•−−−
        SS120 (LLII)•−•−−−
        MIT9211 (LLIII)•−•−−−
        MIT9303 (LLIV)•−•−−−
        MIT9313 (LLIV)•−•−−−
    • ↵ a The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ b Searches for Atx1 using BLASTP and TBLASTN gave TBLASTN E values in marine Synechococcus and Prochlorococcus strains of >0.4, so Atx1 is either absent or looks completely different from ssr2857 of Synechocystis sp. strain PCC6803.

  • TABLE 9.

    Distribution of Fe and Zn related gene orthologs in marine picocyanobacterial genomes

    Genus and strain (clade)Presencea of:
    feoB, cluster 2464futA,b cluster 68futB, cluster 639futC, cluster 8066Ferritin /bacterio-ferritin, cluster 1204, 2936, or 7301Crp1390, cluster 1390dpsA, cluster 1889Putative Fe-regulated hydroxylase, cluster 1755PSI-associated pcb/isiA superfamily, cluster 173/9095isiB, cluster 1833fur, cluster 956zur, cluster 397fur-type, cluster 1492smtA (Zn), cluster 2886znuA, cluster 919znuA-like, cluster 2462smtB
    Synechococcus
        CC9311 (I)••••5••••••••4••−
        CC9605 (II)−•••••−••2•••3c•−−
        WH8102 (III)−•••−−−−−−••••••−
        CC9902 (IV)−•••••−••••••−•−−
        BL107 (IV)−•••••−••••••−•−−
        WH7803 (V)−•••−−•−−−•••••−−
        WH7805 (VI)−2••••••−−•••−•−−
        RS9917 (VIII)?d2••2••−−−•••−••−
        RS9916 (IX)−2••••••−−•••−•−−
        WH5701 (5.2)••••3e•••−−•••2•−−
        RCC307 (5.3)−2•••e−•−−−•••−••−
    Synechocystis sp. strain PCC6803•2••2−•−• isiA••••−•−•
    Prochlorococcus
        MED4 (HLI)−•••••−−−•••−−•−−
        MIT9515 (HLI)−•••••−•• pcbB•••−−•−
        AS9601 (HLII)−•••••−•• pcbB•••−−•−
        MIT9215 (HLII)−•••••−•• pcbB•••−−•−
        MIT9301 (HLII)−•••••−•• pcbB•••−−•−
        MIT9312 (HLII)−•••••−•• pcbB•••−−•−−
        NATL1A (LLI)−•••••−•• pcbC•••−−•−
        NATL2A (LLI)−•••••−•• pcbC•••−−•−−
        SS120 (LLII)−•••••−•• pcbC•••−−•−−
        MIT9211 (LLIII)−•••••−•• pcbC•••−−•−−
        MIT9303 (LLIV)−•••2•••• pcbB••••−••
        MIT9313 (LLIV)−•••2•••• pcbB••••−•−−
    • ↵ a The presence of a single gene is indicated by a closed circle. Where multiple genes are present, the number is given. −, absent.

    • ↵ b It is not possible to determine a homolog of futA2 (slr0513), although there are two distinct groups.

    • ↵ c One copy is interrupted by a stop codon so may be a pseudogene.

    • ↵ d Synechococcus sp. strain RS9917 contains two ORFs that are N- and C-terminal halves of an FeoB transporter but which are interrupted by transposase elements.

    • ↵ e WH5701 and RCC307 contain a bacterioferritin most closely related to genes from heterotrophic bacteria.

  • TABLE 10.

    Cross-genome comparison of the number of regulatory genes

    Genus and strain (clade)No. of:
    Sig70-type sigma factorsaType 3 alternative sigma factorsHistidine kinasesResponse regulatorsCRP-type regulatorsYfr2 to -5 ncRNAsYfr1 ncRNAs
    Synechococcus
        CC9311 (I)821216481
        CC9605 (II)61712541
        WH8102 (III)61912251c
        CC9902 (IV)61811321
        BL107 (IV)61711421
        WH7803 (V)711415221
        WH7805 (VI)711317421
        RS9917 (VIII)711518521
        RS9916 (IX)711214421
        WH5701 (5.2)721110411
        RCC307 (5.3)801016221
    Synechocystis sp. strain PCC68035447b4243c1c
    Prochlorococcus
        MED4 (HLI)506634c1c
        MIT9312 (HLII)5066221
        NATL2A (LLI)5066341
        SS120 (LLII)505631c0
        MIT9211 (LLIII)5056210
        MIT9313 (LLIV)7171042c1c
    • ↵ a Sig70-type sigma factors include SigA and the complete set of type 2 factors present in these strains.

    • ↵ b The total includes 20 hybrid histidine kinases.

    • ↵ c Expression and transcript start sites were verified in experiments (10, 309).

Additional Files

  • Figures
  • Tables
  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 1 - Tables S1 (Distribution of gene orthologs in marine picocyanobacteria coding proteins potentially involved in 2-phosphoglycolate metabolism via the plant-like C2 cycle and the bacterium-like glycerate pathway), S2 (Distribution of gene orthologs in marine picocyanobacteria encoding transport proteins), S3 (Marine Synechococcus and Prochlorococcus �giant� ORFs), S4 (Cross-genome comparison of histidine kinase components of two-component systems among Prochlorococcus and Synechococcus strains), and S5 (Cross-genome comparison of response regulator components of two-component systems among Prochlorococcus and Synechococcus strains).
      Zipped MS Word document, 84K.
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Ecological Genomics of Marine Picocyanobacteria
D. J. Scanlan, M. Ostrowski, S. Mazard, A. Dufresne, L. Garczarek, W. R. Hess, A. F. Post, M. Hagemann, I. Paulsen, F. Partensky
Microbiology and Molecular Biology Reviews Jun 2009, 73 (2) 249-299; DOI: 10.1128/MMBR.00035-08

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Ecological Genomics of Marine Picocyanobacteria
D. J. Scanlan, M. Ostrowski, S. Mazard, A. Dufresne, L. Garczarek, W. R. Hess, A. F. Post, M. Hagemann, I. Paulsen, F. Partensky
Microbiology and Molecular Biology Reviews Jun 2009, 73 (2) 249-299; DOI: 10.1128/MMBR.00035-08
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  • Top
  • Article
    • SUMMARY
    • INTRODUCTION
    • GENOME STRUCTURE
    • ECOLOGICAL CONTEXT FOR INTERPRETING GENOMIC DATA
    • LIGHT
    • SALT
    • NUTRIENT ACQUISITION
    • GIANT PROTEINS: ROLES IN MOTILITY, IN PREDATOR AVOIDANCE, OR AS AN “ENVIRONMENTAL SHIELD”?
    • GENE REGULATION
    • CONCLUSIONS AND FUTURE DIRECTIONS
    • ACKNOWLEDGMENTS
    • REFERENCES
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KEYWORDS

Cyanobacteria
Ecosystem
Genome, Bacterial
Water Microbiology

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