Article Figures & Data
Figures
- 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.
Genome sizes of marine picocyanobacteria compared to a representative selection of other cyanobacteria.
- 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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
- TABLE 1.
Summary of the different Prochlorococcus and Synechococcus genomes sequenced to date
Genus and strain RCC no.a Subcluster or ecotypeb Clade no.c Genome size (Mb) No. of protein-coding genes GC (%) Status and accession no.d Reference Synechococcus CC9311 1086 5.1B I 2.61 2,892 52 [C]:CP000435 214 CC9605 753 5.1A II 2.51 2,645 59 [C]:CP000110 56 WH8102 539 5.1A III 2.43 2,519 59 [C]:BX548020 212 CC9902 5.1A IV 2.23 2,358 54 [C]:CP000097 56 BL107 515 5.1A IV 2.28 2,553 54 [WGS]:AATZ00000000 56 WH7803 752 5.1B V 2.37 2,586 60 [C]:CT971583 56 WH7805 1085 5.1B VI 2.62 2,934 57 [WGS]:AAOK00000000 56 RS9917 556 5.1B VIII 2.58 2,820 65 [WGS]:AANP00000000 56 RS9916 555 5.1B IX 2.66 3,009 60 [WGS]:AAUA00000000 56 WH5701 1084 5.2 2.86 3,129 66 [WGS]:AANO00000000 56 RCC307 307 5.3 2.22 2,583 61 [C]:CT978603 56 Prochlorococcus MED4 151 HL HLI 1.66 1,716 31 [C]:BX548174 239 MIT9515 HL HLI 1.70 1,908 31 [C]:CP000552 136 MIT9301 HL HLII 1.64 1,907 31 [C]:CP000576 136 AS9601 HL HLII 1.67 1,926 31 [C]:CP000551 136 MIT9215 HL HLII 1.74 1,989 31 [C]:CP000825 136 MIT9312 HL HLII 1.71 1,962 31 [C]:CP000111 136 NATL1A LL LLI 1.86 2,201 35 [C]:CP000553 136 NATL2A 314 LL LLI 1.84 2,158 35 [C]:CP000095 136 SS120 154 LL LLII 1.75 1,884 36 [C]:AE017126 57 MIT9211 LL LLIII 1.69 1,855 38 [C]:CP000878 136 MIT9303 LL LLIV 2.68 3,022 50 [C]:CP000554 136 MIT9313 407 LL LLIV 2.41 2,275 51 [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 clade Ecological conditions of largest relative abundance References Synechococcus (5.1)a I Coastal and/or temperate mesotrophic open ocean waters largely above 30°N and below 30°S 34, 340, 341 II Offshore, continent shelf, oligotrophic tropical or subtropical waters between 30°N and 30°S 2, 83-85, 294, 340, 341 III Ultraoligotrophic open-ocean waters 84, 85, 341 IV Coastal and/or temperate mesotrophic open ocean waters largely above 30°N and below 30°S 34, 340, 341 V/VI/VIIb Relatively 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 1897 Cu/Zn SOD, cluster 1853 Mn SOD, cluster 7995 Ni SOD, cluster 1843 Fe SOD, cluster 1824 1-Cys Prx, cluster 2925 2-Cys Prx, cluster 167 Type II Prx, cluster 3802 PrxQ, clusters 38, 812, 8024 Gpx, cluster 308 TxlA, cluster 471 GrxCc, cluster 445 Rub/HoxR, clusters 269, 3931 RbrA, cluster 1682 TrxA (m type), cluster 8028 TrxB (x type), cluster 47 Putative TrX, clusters 1171, 1233 FTR system NTR system, clusters 1301, 1904 DpsA, cluster 1889 FtrC, cluster 1648 FtrV, 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 • • − − • • • • 2 2 • • • − • • • • • • • 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 1330 phrB, cluster 1584 Photolyase-related protein, cluster 1460 MTFH domain, cluster 1541 FAD domain, cluster 1540 FAD domain, cluster 3563 PD 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 1610 ggpP (stpA), cluster 1282 ggtA, cluster 8069 ggtB, cluster 1455 ggtC, cluster 1454 ggtD, cluster 1453 proV, cluster 8061 proW, cluster 1943 proX, cluster 1944 gpgP, cluster 1370 gpgS, cluster 1368 gbmt1, cluster 1941 gbmt2, cluster 1942 spsA, cluster 368 spp, cluster 2483 betP, 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 468 amt, cluster 244 amtb, cluster 8701 glnA, cluster 103 glnAb, cluster 2090, 2505, 6741, or 8855 glnB, cluster 186 glnBb, cluster 2023 pipX, cluster 1044 glsFc, cluster 134 glsFb, cluster 9009 gdhA, cluster 1539 or 3700 ured, clusters 1358-1364 speA, cluster 415 speB, cluster 392 or 2247 cynS, cluster 1552 carAB, cluster 783 or 962 dadA, cluster 377 nadB, cluster 196 thiO, 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) • • − • 4g 2 • • • • − • • 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 8015/1531 ptrA, cluster 1606 pstS,b cluster 23(1829) phoA/5′NDc (phoX) psip1,d cluster 2662 pitA, cluster 6877 phoU, cluster 5756 arsR, cluster 1532 arsC, cluster 1227 arsB, 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) • • 3 2 (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 1274 cueO, cluster 2933 or 3002 ctaA, cluster 65 pacS, cluster 9116 atx1b Cd/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 2464 futA,b cluster 68 futB, cluster 639 futC, cluster 8066 Ferritin /bacterio-ferritin, cluster 1204, 2936, or 7301 Crp1390, cluster 1390 dpsA, cluster 1889 Putative Fe-regulated hydroxylase, cluster 1755 PSI-associated pcb/isiA superfamily, cluster 173/9095 isiB, cluster 1833 fur, cluster 956 zur, cluster 397 fur-type, cluster 1492 smtA (Zn), cluster 2886 znuA, cluster 919 znuA-like, cluster 2462 smtB Synechococcus CC9311 (I) • • • • 5 • • • • • • • • 4 • • − CC9605 (II) − • • • • • − • • 2 • • • 3c • − − WH8102 (III) − • • • − − − − − − • • • • • • − CC9902 (IV) − • • • • • − • • • • • • − • − − BL107 (IV) − • • • • • − • • • • • • − • − − WH7803 (V) − • • • − − • − − − • • • • • − − WH7805 (VI) − 2 • • • • • • − − • • • − • − − RS9917 (VIII) ?d 2 • • 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 factorsa Type 3 alternative sigma factors Histidine kinases Response regulators CRP-type regulators Yfr2 to -5 ncRNAs Yfr1 ncRNAs Synechococcus CC9311 (I) 8 2 12 16 4 8 1 CC9605 (II) 6 1 7 12 5 4 1 WH8102 (III) 6 1 9 12 2 5 1c CC9902 (IV) 6 1 8 11 3 2 1 BL107 (IV) 6 1 7 11 4 2 1 WH7803 (V) 7 1 14 15 2 2 1 WH7805 (VI) 7 1 13 17 4 2 1 RS9917 (VIII) 7 1 15 18 5 2 1 RS9916 (IX) 7 1 12 14 4 2 1 WH5701 (5.2) 7 2 11 10 4 1 1 RCC307 (5.3) 8 0 10 16 2 2 1 Synechocystis sp. strain PCC6803 5 4 47b 42 4 3c 1c Prochlorococcus MED4 (HLI) 5 0 6 6 3 4c 1c MIT9312 (HLII) 5 0 6 6 2 2 1 NATL2A (LLI) 5 0 6 6 3 4 1 SS120 (LLII) 5 0 5 6 3 1c 0 MIT9211 (LLIII) 5 0 5 6 2 1 0 MIT9313 (LLIV) 7 1 7 10 4 2c 1c
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.
- 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).
