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Environmental Microbiology

The Ferredoxin-Like Protein FerR Regulates PrbP Activity in Liberibacter asiaticus

Lei Pan, Danilo da Silva, Fernando A. Pagliai, Natalie A. Harrison, Claudio F. Gonzalez, Graciela L. Lorca
Maia Kivisaar, Editor
Lei Pan
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Danilo da Silva
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Fernando A. Pagliai
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Natalie A. Harrison
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Claudio F. Gonzalez
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Graciela L. Lorca
aMicrobiology and Cell Science Department, Genetics Institute, Institute of Food and Agricultural Science, University of Florida, Gainesville, Florida, USA
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Maia Kivisaar
University of Tartu
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DOI: 10.1128/AEM.02605-18
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  • FIG 1
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    FIG 1

    Synteny of ferRLas and prbPLas homologs is conserved in Alphaproteobacteria. (A) Graphic representation of the prbPLas genomic context in representative genomes from Alphaproteobacteria. Shown are prbPLas and its homologous genes in L. asiaticus (GenBank accession no. NC_012985.3), L. crescens (GenBank accession no. NC_019907.1), Sinorhizobium meliloti (GenBank accession no. NC_003047.1), and Bartonella bacilliformis (GenBank accession no. NC_008783.1). Genomes were visualized in the JGI IMG genome viewer. (B) Taxonomy tree of microbial species containing ferRLas and its homologs. FerRLas homologs were identified by Protein BLAST. The taxonomy order was based on the NCBI taxonomy database. The CBP group is a bacterial group that primarily consists of members of Bacteroidetes and Chlorobi as well as putative environmental isolates. The cooccurrence and/or synteny of ferRLas and prbPLas were examined using STRING, JGI IMG genome, and SEED viewers. The cooccurrence of ferRLas and prbPLas is represented as discontinued lines in the gene representation figures, while synteny is represented as continuous lines.

  • FIG 2
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    FIG 2

    PrbPLas and FerRLas interact in a bacterial two-hybrid system. β-Galactosidase activity was determined using E. coli JM109 as a reporter strain. The genetic constructs in the strains are as follows: 2HB01 carrying pB2HΔα and pB2HΔω, 2HB02 carrying pB2HΔα and pB2HΔω_ferRLas, 2HB03 carrying the pB2HΔα_prbPLas and pB2HΔω, and 2HB04 carrying pB2HΔα_prbPLas and the pB2HΔω_ferRLas. β-Galactosidase assays were performed at different stages during the exponential-growth phase (OD600, 0.3, 0.5, and 0.8). The growth curves of all the strains tested are shown in Fig. S2A. Enzymatic activities are shown as the average arbitrary units (AU) with the standard deviation (SD) from biological and technical triplicates. Statistical significance was determined as described in Materials and Methods. *, P < 0.05; **, P < 0.01; ***, P < 0.001; ****, P < 0.0001.

  • FIG 3
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    FIG 3

    FerRLas increases PrbPLas activity as a transcriptional activator. (A) In vitro transcription assays using increasing concentrations of FerRLas (0, 1, 2, and 4 μM) and/or 2.0 μM PrbPLas added to the RNA polymerase-containing reactions as indicated at the top. (B) ImageJ was utilized to quantify the amount of the PrplK transcript obtained in the in vitro transcription. The fold change was calculated by the band intensity normalized to the transcript level in the reactions performed in the absence of PrbPLas and FerRLas. The quantification was based on observations from at least three replicates. Statistical significance was determined as described in Materials and Methods. Different letters on top of the bars denote statistical significance of at least a P value of <0.05. (C) The effects of FerRLas on PrbPLas-DNA binding were evaluated using electrophoresis mobility shift assays. The reaction mixture contained 1.0 ng of the biotinylated Prplk probe and 2.5 μM PrbPLas or 1 to 5 μM FerRLas, as indicated at the top of each lane. The first lane has no protein added.

  • FIG 4
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    FIG 4

    FerRLas activity is not modulated by oxidizing/reducing conditions. (A) Electrophoresis mobility shift assay of PrbPLas and FerRLas with PrplK; the reaction mixture contained 1.0 ng of the biotinylated Prplk probe, 2.5 μM PrbPLas, 2.5 μM FerRLas, and increasing concentrations (0 to 500 μM) of DTT or diamide, as indicated at the top. The first lane has no protein added. (B) The effects of oxidizing and reducing agents were tested on FerRLas activity using in vitro transcription assays. PrbPLas and FerRLas (0 to 2.5 μM) were added to the reactions, as indicated at the top. Increasing concentrations of DTT or diamide were added at the indicated concentrations. All reactions contained the same amount of RNA polymerase (0.5 μM).

  • FIG 5
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    FIG 5

    In silico prediction of the PrbPLas-interacting interface in FerRLas. (A) Hydrophobicity analysis in the 3D model FerRLas-SD. The color gradient from red to white illustrates hydrophobic potential to neutral, while the black dashed line circle encloses the predicted hydrophobicity patch in FerRLas-SD. (B) Surface electrostatic potential analysis in FerRLas-SD. The color gradient from red to blue illustrates negative to positive surface charges, while the black dashed line circle encloses the predicted hydrophobicity patch in FerRLas-SD. (C) Cartoon representation of the FerRLas-SD model with stick representation of the amino acid residues that form the predicted hydrophobicity patch. (D) Hydrophobic amino acid residues in the predicted patch are shown in red.

  • FIG 6
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    FIG 6

    FerRLas:PrbPLas interactions are mediated by residues V20, V23, and C40 in FerRLas. (A) Mutations V20A, V23A, and C40A in FerRLas decrease interactions with PrbPLas in a bacterial two-hybrid system. β-Galactosidase activity was performed in E. coli JM109 (β-galactosidase deficient). The reporter strains used were 2HB04 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas, 2HB08 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas V20A, 2HB12 carrying pB2HΔα and pB2HΔω_ferRLas V23A, and 2HB16 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas C40A. β-Galactosidase assays were performed at different stages during the exponential-growth phase (OD600, 0.3, 0.5, and 0.8). The growth curves of all the strains tested are shown in Fig. S2B. The activities were normalized to the highest background strains of 2HB02 carrying pB2HΔα and pB2HΔω_ferRLas, 2HB07 carrying pB2HΔα and pB2HΔω_ferRLas V20A, 2HB11 carrying pB2HΔα and pB2HΔω_ferRLas V23A, and 2HB15 carrying pB2HΔα and pB2HΔω_ferRLas C40A and are shown as arbitrary units (AU). Statistical significance was determined as described in Materials and Methods. *, P < 0.05; **, P < 0.01. (B) The mutations in V20, V23, and C40 reduced FerRLas activity on PrbPLas. In vitro transcription assays were performed with PrbPLas, FerRLas WT, or the FerRLas V20A, V23A, and C40A mutants. Each protein was added at a concentration of 2.5 μM, as indicated at the top; all reactions contained the same amount of RNA polymerase (0.5 μM). The image has been cropped and rearranged for presentation. (C) ImageJ was utilized to quantify the amount of the PrplK transcripts obtained in the in vitro transcription assay. The activity fold change was calculated by the band intensity normalized to the transcript level in the reactions performed in the presence of PrbPLas and FerRLas. The quantification was based on observations from at least three replicates. Statistical significance was determined as described in Materials and Methods. *, P < 0.05; **, P < 0.01.

  • FIG 7
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    FIG 7

    Increase of osmolarity induces ferRLcr expression level in L. crescens. The expression levels of ferRLcr (B488_01730) and prbPLcr (B488_01720) were determined in L. crescens in the prescence or absence of increasing concentrations of sucrose (50 to 100 mM) by qRT-PCR. The relative expression value of each gene was normalized to the expression levels of gyrase subunit A gene (gyrA). In black, control (Ctrl) condition in BM7 medium; light gray, BM7 medium supplemented with 50 mM sucrose; dark gray, BM7 medium supplemented with 100 mM sucrose. L. crescens cells were collected when the OD600 was 0.3. The experiment was performed using 4 biological replicates. The black horizontal line indicates statistical significance between connecting data bars. Statistical significance was determined as described in Materials and Methods. *, P < 0.05.

  • FIG 8
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    FIG 8

    Proposed model of FerRLas modulation of PrbPLas activity. We propose that under insect symbiont living conditions, ferRLas and prbPLas expression is maintained at basal level. When L. asiaticus is exposed to osmotic pressure, i.e., there were high sucrose contents during entrance of this bacterium into the citrus phloem, LdtRLas activates mRNA expression of ferRLas. Consequently, elevated concentrations of FerRLas promote interactions between FerRLas and PrbPLas, which increase PrbPLas activity by stabilizing the promoter open complex formation of genes that are necessary for adaptation to the host environment. The figure does not represent accurate scale and molecular ratio.

Tables

  • Figures
  • Additional Files
  • TABLE 1

    Strains and plasmids used in this study

    Strain or plasmidGenotype or descriptionaReference or source
    Bacterial strains
        Escherichia coli
            DH5αF– Φ80lacZΔM15 Δ(lacZYA-argF)U169 recA1 endA1 hsdR17 (rK– mK+) phoA supE44 λ– thi-1 gyrA96 relA1Invitrogen
            K-12 JM109F′ traD36 proA+B+ lacIq Δ(lacZ)M15/Δ(lac proAB) glnV44 e14 gyrA96 recA1 relA1 endA1 thi hsdR17Promega
            2HB01JM109 carrying empty pB2HΔα and empty pB2HΔω (Ampr Cmr)This work
            2HB02JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas (Ampr Cmr)This work
            2HB03JM109 carrying pB2HΔα_prbPLas and empty pB2HΔω (Ampr Cmr)This work
            2HB04JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas (Ampr Cmr)This work
            2HB05JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas Y3A (Ampr Cmr)This work
            2HB06JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas Y3A (Ampr Cmr)This work
            2HB07JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas V20A (Ampr Cmr)This work
            2HB08JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas V20A (Ampr Cmr)This work
            2HB09JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas C21A (Ampr Cmr)This work
            2HB10JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas C21A (Ampr Cmr)This work
            2HB11JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas V23A (Ampr Cmr)This work
            2HB12JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas V23A (Ampr Cmr)This work
            2HB13JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas D24A (Ampr Cmr)This work
            2HB14JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas D24A (Ampr Cmr)This work
            2HB15JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas C40A (Ampr Cmr)This work
            2HB16JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas C40A (Ampr Cmr)This work
            2HB17JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas D42A (Ampr Cmr)This work
            2HB18JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas D42A (Ampr Cmr)This work
            2HB19JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas C43A (Ampr Cmr)This work
            2HB20JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas C43A (Ampr Cmr)This work
            2HB21JM109 carrying empty pB2HΔα and pB2HΔω_ferRLas V45A (Ampr Cmr)This work
            2HB22JM109 carrying pB2HΔα_prbPLas and pB2HΔω_ferRLas V45A (Ampr Cmr)This work
            BL21 (DE3)F– ompT hsdS(rB– mB–) gal dcm (DE3) pRARENovagen
            ArcticExpress (DE3) RILE. coli B F– ompT hsdS(rB– mB–) dcm+ gal λ (DE3) endA Hte [cpn10 cpn60] [argU ileY leuW] (Strr Tetr Gentr)Agilent
            EEPrbPBL21 (DE3) carrying p15TV-prbPLas (Ampr)21
            AEFerRArcticExpress (DE3) RIL carrying p15TV_ferRLas (Ampr)This work
            AEFerR V20AArcticExpress (DE3) RIL carrying p15TV_ferRLas V20A (Ampr)This work
            AEEFerR V23AArcticExpress (DE3) RIL carrying p15TV_ferRLas V23A (Ampr)This work
            AEEFerR C40AArcticExpress (DE3) RIL carrying p15TV_ferRLas C40A (Ampr)This work
            EERNAPDBL21 (DE3) carrying p15TV-rpoD, pACYCDuet-rpoB-rpoC, pRSFDuet-rpoZ-rpoA (Ampr Cmr Kanr)24
            ECPRPLKDH5α carrying pMiniT-PrplK (Ampr)24
        Liberibacter crescens BT-1Standard wild-type strain73
    Plasmids
        pB2HΔαpACYCDuet-1Ωtac with E. coli β-galactosidase fragment lacking sequence for amino acids 11–41 (Δα) cloned in the BamHI-NcoI site (Cmr)38
        pB2HΔωpETDuet-1ΔSphIΩtac with E. coli β-galactosidase fragment lacking sequence for amino acids 789–1023 (Δω) cloned in the BamHI-NcoI site (Ampr)38
        pB2HΔα_prbPLaspB2HΔα with prbP gene from L asiaticus cloned in the BamHI-SphI site (Cmr)21
        pB2HΔω_ferRLaspB2HΔω with ferR gene from L asiaticus cloned in the BamHI-SphI site (Ampr)This work
        pB2HΔω_ferRLas Y3ApB2HΔω_ferRLas with Y3A (Ampr)This work
        pB2HΔω_ferRLas V20ApB2HΔω_ferRLas with V20A (Ampr)This work
        pB2HΔω_ferRLas C21ApB2HΔω_ferRLas with C21A (Ampr)This work
        pB2HΔω_ferRLas V23ApB2HΔω_ferRLas with V23A (Ampr)This work
        pB2HΔω_ferRLas D24ApB2HΔω_ferRLas with D24A (Ampr)This work
        pB2HΔω_ferRLas C40ApB2HΔω_ferRLas with C40A (Ampr)This work
        pB2HΔω_ferRLas D42ApB2HΔω_ferRLas with D42A (Ampr)This work
        pB2HΔω_ferRLas C43ApB2HΔω_ferRLas with C43A (Ampr)This work
        pB2HΔω_ferRLas V45ApB2HΔω_ferRLas with V45A (Ampr)This work
        p15TV-LExpression vector for purification of proteins by nickel affinity chromatography (Ampr)Cheryl Arrowsmith, (Addgene plasmid # 26093)
        p15TV_ferRLasferR gene from L asiaticus cloned in the BseRI site of p15TV-L (Ampr)This work
        p15TV-ferRLas V20Ap15TV_ferRLas with V20A (Ampr)This work
        p15TV-ferRLas V23Ap15TV_ferRLas with V23A (Ampr)This work
        p15TV-ferRLas C40Ap15TV_ferRLas with C40A (Ampr)This work
    • ↵a Ampr, ampicillin resistance; Cmr, chloramphenicol resistance; Strr, streptomycin resistance; Tetr, tetracycline resistance; Gentr, gentamicin resistance; Kanr, kanamycin resistance.

  • TABLE 2

    Proteins identified by LC-MS/MS in the immunoprecipitation assaysa

    Locus tagDescriptionAb + PrbPLas + lysateAb + lysate
    Unique peptide countCoverage (%)Unique peptide countCoverage (%)
    CLIBASIA_01510PrbPLas112800
    B488_01730FerRLcr11300
    B488_08440RNA polymerase β-subunit5300
    B488_08430RNA polymerase β′-subunit141100
    B488_04340RNA polymerase α-subunit51800
    • ↵a Ab, antibody.

  • TABLE 3

    Primers used in this study

    Primer by useSequence (5′–3′)
    EMSA
        EMSA_CLIB_00130_Ext_FwCTGTTTTCTTCGAGGTTGGTG
        EMSA_CLIB_00130_Ext_RvCCGCATTAAACGCCTTACAA
        EMSA_CLIB_00130_FwCTGATGGTCCGTTTGCTTCT
        EMSA_CLIB_00130_Rv_BioTGCAGAACCCGACTCTATCTG
    Cloning, two-hybrid system, and site-directed mutagenesis
        CLIB_01505_Ext-FwAAAAATCCGTAGAAAGGCAGT
        CLIB_01505_Ext-RvTTGCGAATCTATTGATGTCAGG
        CLIB_01505_LIC-FwTTGTATTTCCAGGGCATGACATACGTCGTCACTGAAAA
        CLIB_01505_LIC-RvCAAGCTTCGTCATCATTATGTATTTTTTCCCCCAGGA
        CLIB_01505_SphI_FwCCGGCATGCATGACATACGTCGTCACTGAAAA
        CLIB_01505_BamHI_RvCCGGGATCCTTATGTATTTTTTCCCCCAGGA
        CLIB_01505_Y3A_FwATGCATGACAGCCGTCGTCACTG
        CLIB_01505_Y3A_RvGCATATGGATCGATCCTG
        CLIB_01505_V20A_FwCATACAGATTGCGTGGAAGCTTGTCCTGTCGATTGTTTT
        CLIB_01505_V20A_RvAAAACAATCGACAGGACAAGCTTCCACGCAATCTGTATG
        CLIB_01505_C21A_FwACAGATTGCGTGGAAGTTGCTCCTGTCGATTGTTTTTAC
        CLIB_01505_C21A_RvGTAAAAACAATCGACAGGAGCAACTTCCACGCAATCTGT
        CLIB_01505_V23A_FwTGCGTGGAAGTTTGTCCTGCCGATTGTTTTTACGAAGGA
        CLIB_01505_V23A_RvTCCTTCGTAAAAACAATCGGCAGGACAAACTTCCACGCA
        CLIB_01505_D24A_FwGTGGAAGTTTGTCCTGTCGCTTGTTTTTACGAAGGAGAA
        CLIB_01505_D24A_RvTTCTCCTTCGTAAAAACAAGCGACAGGACAAACTTCCAC
        CLIB_01505_C40A_FwGCAATCCATCCAGATGAGGCCATAGATTGTGGGGTATGC
        CLIB_01505_C40A_RvGCATACCCCACAATCTATGGCCTCATCTGGATGGATTGC
        CLIB_01505_D42A_FwCATCCAGATGAGTGCATAGCTTGTGGGGTATGCGAGCCC
        CLIB_01505_D42A_RvGGGCTCGCATACCCCACAAGCTATGCACTCATCTGGATG
        CLIB_01505_C43A_FwCCAGATGAGTGCATAGATGCTGGGGTATGCGAGCCCGAA
        CLIB_01505_C43A_RvTTCGGGCTCGCATACCCCAGCATCTATGCACTCATCTGG
        CLIB_01505_V45A_FwTGCATAGATTGTGGGGCATGCGAGCCCGAATGC
        CLIB_01505_V45A_RvGCATTCGGGCTCGCATGCCCCACAATCTATGCA
    Cotranscription assay
        CLIB_01505_RTPCR_FwGCATACAGATTGCGTGGAAGT
        CLIB_01505_RTPCR_RvCCCCACAATCTATGCACTCAT
        CLIB_01510_RTPCR_FwCTGCCCATGGAGTAGGAACTATTAC
        CLIB_01510_RTPCR_RvATCTTGTCCTTGTCAAATGCAATAA
    Sequencing
        T7TAATACGACTCACTATAGGG
        T7 termGCTAGTTATTGCTCAGCGG
        pB2H_Omega_FwCTCAAGCTTACTCCCCATCC
        pB2H_Omega_RvGGCGATTAAGTTGGGTAACG
        pB2H_Alpha_FwGACAATTAATCATCGGCTCGT
        pB2H_Alpha_RvGACAGTATCGGCCTCAGGAA

Additional Files

  • Figures
  • Tables
  • Supplemental material

    • Supplemental file 1 -

      Cotranscription assays (Fig. S1); growth curves (Fig. S2); EMSA (Fig. S3); quantification of EMSA results (Fig. S4); analysis of mutant interactions (Fig. S5).

      PDF, 929K

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The Ferredoxin-Like Protein FerR Regulates PrbP Activity in Liberibacter asiaticus
Lei Pan, Danilo da Silva, Fernando A. Pagliai, Natalie A. Harrison, Claudio F. Gonzalez, Graciela L. Lorca
Applied and Environmental Microbiology Feb 2019, 85 (4) e02605-18; DOI: 10.1128/AEM.02605-18

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The Ferredoxin-Like Protein FerR Regulates PrbP Activity in Liberibacter asiaticus
Lei Pan, Danilo da Silva, Fernando A. Pagliai, Natalie A. Harrison, Claudio F. Gonzalez, Graciela L. Lorca
Applied and Environmental Microbiology Feb 2019, 85 (4) e02605-18; DOI: 10.1128/AEM.02605-18
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    • ABSTRACT
    • INTRODUCTION
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    • MATERIALS AND METHODS
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KEYWORDS

Liberibacter asiaticus
PrbP
ferredoxin-like protein
transcriptional accessory protein

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