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PHYSIOLOGY AND METABOLISM

Phosphorus Deprivation Responses and Phosphonate Utilization in a Thermophilic Synechococcus sp. from Microbial Mats

Melissa M. Adams, María R. Gómez-García, Arthur R. Grossman, Devaki Bhaya
Melissa M. Adams
1Carnegie Institution for Science, Department of Plant Biology, Stanford University, Stanford, California 94305
2 Department of Biology, Stanford University, Stanford, California 94305
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María R. Gómez-García
1Carnegie Institution for Science, Department of Plant Biology, Stanford University, Stanford, California 94305
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Arthur R. Grossman
1Carnegie Institution for Science, Department of Plant Biology, Stanford University, Stanford, California 94305
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Devaki Bhaya
1Carnegie Institution for Science, Department of Plant Biology, Stanford University, Stanford, California 94305
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  • For correspondence: dbhaya@stanford.edu
DOI: 10.1128/JB.01011-08
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  • FIG. 1.
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    FIG. 1.

    Genomic organization of phn genes and comparison of the regions flanking the phn gene clusters in OS-B′ and OS-A. (A) The top row of genes shows the main phn gene cluster of OS-B′, with the ABC phosphonate (Phn) transporter (phn C-1, phn D-1, and phn E-1) and the C-P lyase (phnG-phnM) genes. The bottom row shows the second (phnD, phn D-2, phn D-3 phn C-2, and phn E-3) and third (phnE-4, phnD-4, and phnC-3) phn clusters. See Table 2 for accession numbers. The Phn transporter genes include the ATPase component (phnC; red), the substrate binding protein (phnD; yellow), and the membrane permease component (phnE; green). A putative Pho box is located upstream of phnC-1, phnD, and phnC. Asterisks indicate genes that overlap with the next contiguous gene. (Inset) Logo representation of the profile of the top 10 ranked Pho boxes of OS-B′, as predicted by phylogenetic footprinting (40). The logo was generated by using the Weblogo server (http://weblogo.berkeley.edu/logo.cgi ). (B) Organization of flanking regions around the main phn gene cluster (gray arrows) in OS-B′ compared to the analogous region in OS-A. (C) Organization of flanking regions around the second phn cluster (phnD, phnD-2, phnD-3, phnC-2, phnE-2, and phnE-3) in OS-B′ compared to the analogous region in OS-A. (D) Organization of flanking regions around the third phn cluster (phnE-4, phnD-4, and phnC-3) in OS-B′ compared to the analogous region in OS-A. Gray arrows represent the phn genes, and solid colored arrows (but not black arrows) indicate syntenic sequences in OS-A relative to OS-B′, while the broken arrows indicate genes where there is a break in synteny between the two genomes. Black arrows in the OS-B′ genome represent genes not present in OS-A. The scale is indicated in panel B.

  • FIG. 2.
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    FIG. 2.

    Growth response, APase activity, and absorbance spectra of OS-B′ under various P conditions. (A) Late-logarithmic-phase cells grown in +P medium were transferred growth under four different conditions: (i) +P, (ii) −P, (iii) +P medium with 0.5 mM MePhn (+P+MePhn), and (iv) −P medium with 0.5 mM MePhn (−P+MePhn). Growth of all cultures was monitored for ∼192 h. Note the log scale on the y axis for cells per ml data. (B) APase activity and growth measurements were quantified in cell cultures once every 24 h. The APase activity was measured as μg of pNPP hydrolyzed per h per 1 × 106 cells. (C) Whole-cell absorption spectra of each culture between the wavelengths of 400 and 800 nm, normalized to the OD750, at 96 h after cell transfer. Results for growth and APase activity show the means and standard deviations (error bars) from measurements taken from biological triplicates.

  • FIG. 3.
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    FIG. 3.

    Quantification of relative Pho regulon transcript accumulation following Pi starvation. Specific Pho regulon transcripts, including those of the phn gene cluster, were measured over 24-h intervals under various P conditions. The top panel represents transcripts for genes encoding phosphatases, the middle panel is transcripts for genes associated with transport systems, and the bottom panel is transcripts for genes involved in Phn transport and metabolism. For each gene, relative transcript levels, presented as a ratio under −P and +P conditions, were determined at 24, 48, and 72 h following the transfer of cells to the new growth medium. In the presence of MePhn, relative transcript levels representing −P+MePhn compared to +P+MePhn are shown at 24 h, 48 h, and 72 h. The qPCR results show the means and standard deviations (error bars) for data from three technical replicates.

  • FIG. 4.
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    FIG. 4.

    Quantification of Pho regulon transcript accumulation after Pi addition to P-starved cultures. Pi was added back to the growth medium after 72 h of starvation, and transcript levels were measured (as described in Fig. 3) at 96 h (i.e., 24 h after adding Pi back). Relative transcript levels are shown that compare −P to +P after Pi addition and the control, i.e., −P compared to +P prior to Pi addition but with no Pi added back. The qPCR results show the means and standard deviations (error bars) for data from three technical replicates.

  • FIG. 5.
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    FIG. 5.

    Growth of cultures in MePhn. Growth responses of MePhn-acclimated (triangles) and nonacclimated (squares) OS-B′ cells to +P, −P, and −P+MePhn conditions. The graph shows the means and standard deviations (error bars) from measurements taken from biological triplicates. Starting cultures were initially grown to logarithmic phase in either +P or −P+MePhn medium for 20 days. Note the log scale on the y axis for cells per ml data.

Tables

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  • TABLE 1.

    Primers used to quantify putative Pho regulon transcripts of OS-B′a

    GeneLocus tagSize Forward primerReverse primer
    ntaa
    phoACYB_11981,349449TGGTGCAAACGGGATCCATCATTGAATCTCCTCATAGTCGCTGCGCTT
    phoDCYB_06841,727575GCCGCGGCGATATCGATTTCATTTCAACAAAGGAAGTCCGGCCAAACA
    phoXCYB_19882,048682ACGATGCCCGCTTTGAGTACATCTCTTGGCCACATACAAGGTGCCATT
    pstS-1CYB_10771,076358CACAGGTGACTTTCCCGAATATTCCACGTAGCCAATCGAG
    pstS-2CYB_19151,061353ATGCGAACCCTGCTTTCTGCTTTCGAGATTTGCACGGTTTGGGCTTGA
    phnC-1CYB_0159791263AAACAAGGTTGCCCTAAGGGAGGTTGGCCTTCATGGAGAGGAAGAGAA
    phnD-1CYB_0160896298GCTCCCATTGAAGCGTTCGTGAAATTGCCCTTGGCGTCTTCTAGAGTT
    phnC-2CYB_1467809269TGGCTCAATGGAATCGACCTCACTTAGCCCAACTGACCCGAAAGAACA
    phnICYB_0164696231TGCTGGATTTGGAAATGGATCGCCAGTGGCTCATCCAGTTGCTGAGAA
    phnJCYB_0165866288GTAGCATATGAAACCCAAGCATAGAACTCGAGAGGACCGCTCGTTT
    • ↵ a Included in the table are locus tags, the sizes of the gene in nucleotides (nt) and amino acids (aa), and both the forward and reverse primer sequences that were used.

  • TABLE 2.

    Putative Pho regulon genes of the OS-B′ genomea

    Name of gene(s)Locus tagPutative encoded proteinClosest homolog% AAID
    phoR CYB_0858Sensor histidine kinase Nostoc strain PCC 712041
    phoB CYB_2856Response regulator Gloeobacter violaceus PCC 742175
    phoA CYB_1198Alkaline phosphatase Chlorobium chlorochromatii CaD345
    phoX CYB_1988Alkaline phosphatase Hahella chejuensis KCTC 239654
    phoD CYB_0684Phosphodiesterase Bacillus subtilis 28
    surE-1 CYB_0884Acid phosphatase Thermosynechococcus elongatus BP-160
    surE-2 CYB_1427Acid phosphatase Lyngbya strain PCC 810651
    phoH CYB_2320PhoH family protein Thermosynechococcus elongatus BP-161
    npp CYB_02745′-Nucleotidase phosphatase Cyanothece strain PCC 742453
    nucH CYB_2765Putative secreted nuclease Roseiflexus castenholzii DSM 1394146
    ppx CYB_1493Exopolyphosphatase Anabaena variabilis ATCC 2941358
    ppk CYB_2082Polyphosphate kinase Cyanothece strain PCC 880162
    pstS-1, pstC-1, pstA-1, pstB-1 CYB_1077-74High-affinity ABC-type Pi transporter Cyanothece strain CCY 0110b 50, 51, 53, 70
    pstS-2, pstC-2, pstA-2, pstB-2 CYB_1915-12High-affinity ABC-type Pi transporter Cyanothece strain ATCC 51142b 45, 50, 70, 70
    phoU CYB_2526Regulatory protein Nostoc strain PCC 712061
    phnC-1 , phnD-1, phnE-1 CYB_0159-61Phn ABC-type transporter proteins Cyanothece strain PCC 8801b 44, 31, 45
    phnG-phnM CYB_0162-68C-P lyase Roseiflexus strain RS-1b 48, 32, 38, 59, 45, 41, 39
    phnD,c phnD-2, phnD-3, phnC-2, phnE-2, phnE-3 CYB_1464-69Phn ABC-type transporter proteins Dinoroseobacter shibae DFL 12b 69, 51, 53, 72, 54, 56
    phnE-4, phnD-4, phnC-3 CYB_0012-11, 09Phn ABC-type transporter proteins Cyanothece strain PCC 7424b 36, 27, 69
    ugpB, ugpA CYB_2477-78Glycerol-3-phosphate transporter Deinococcus geothermalis DMS 11300b 39, 46
    • ↵ a Gene names, locus tags, predicted products, and percent AAID to the closest bacterial homolog in all available sequenced organisms (excluding OS-A) are given. Genes associated with putative operons are grouped in the list. Genes shown in bold are preceded by a high-ranking predicted Pho box (44).

    • ↵ b For gene clusters, we show the percent AAID relative to the respective homologs from a single organism.

    • ↵ c PhnD had the highest AAID to the Sinorhizobium meliloti 1021 homolog.

  • TABLE 3.

    Effect of MePhn on transcript accumulationa

    GeneRelative transcript level (at 72 h)
    phoX 18
    phnJ 14
    pstS-2 11
    phnC-1 8
    phoA 8
    pstS-1 7
    phnC-2 5
    phnD-1 5
    phoD 4
    • ↵ a Comparison of relative transcript levels from cells grown under −P conditions relative to −P+MePhn conditions after 72 h of starvation. Transcripts were quantified for all investigated genes of the OS-B′ Pho regulon, as illustrated in Fig. 3 and 4.

Additional Files

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    Files in this Data Supplement:

    • Supplemental file 1 - Table S1, comparison of Pho regulon genes; Table S2, amino acid-level identity of Phn transporter components from the OS-B′ genome.
      MS Word document, 28K.
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Phosphorus Deprivation Responses and Phosphonate Utilization in a Thermophilic Synechococcus sp. from Microbial Mats
Melissa M. Adams, María R. Gómez-García, Arthur R. Grossman, Devaki Bhaya
Journal of Bacteriology Nov 2008, 190 (24) 8171-8184; DOI: 10.1128/JB.01011-08

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Phosphorus Deprivation Responses and Phosphonate Utilization in a Thermophilic Synechococcus sp. from Microbial Mats
Melissa M. Adams, María R. Gómez-García, Arthur R. Grossman, Devaki Bhaya
Journal of Bacteriology Nov 2008, 190 (24) 8171-8184; DOI: 10.1128/JB.01011-08
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KEYWORDS

Alkaline Phosphatase
Organophosphorus Compounds
Phosphorus
Synechococcus

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