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MOLECULAR BIOLOGY OF PATHOGENS

Staphylococcus aureus Serves as an Iron Source for Pseudomonas aeruginosa during In Vivo Coculture

Lauren M. Mashburn, Amy M. Jett, Darrin R. Akins, Marvin Whiteley
Lauren M. Mashburn
Department of PeriodonticsDepartment of Microbiology and Immunology, The University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
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Amy M. Jett
Department of Microbiology and Immunology, The University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
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Darrin R. Akins
Department of Microbiology and Immunology, The University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
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Marvin Whiteley
Department of PeriodonticsDepartment of Microbiology and Immunology, The University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
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  • For correspondence: marvin-whiteley@ouhsc.edu
DOI: 10.1128/JB.187.2.554-566.2005
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  • FIG. 1.
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    FIG. 1.

    Growth of P. aeruginosa in vitro in MOPS minimal medium with 20 mM glucose (▪) and in vivo in the DMC in the rat (▴). Representative growth curves are shown. Maximum doubling times were approximately 40 min in vitro and 50 min in vivo.

  • FIG. 2.
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    FIG. 2.

    Lysis of S. aureus is necessary for iron acquisition by P. aeruginosa during coculture. (A) A BHI petri plate was swabbed with a confluent lawn of S. aureus, and 5 μl of an overnight culture of wild-type P. aeruginosa PA14 and P. aeruginosa PA14-LM1 containing a Tn5 insertion in pqsA were spotted on the plate and incubated at 37°C for 24 h. A zone of clearing (indicating lysis of S. aureus) is visible around the wild-type P. aeruginosa colony. Similar lysis results were also observed in test tube coculture experiments (data not shown). Although not shown here, approximately 20% of the time P. aeruginosa PA14-LM1 produces a small zone of lysis in this assay. (B) Semiquantitative RT-PCR analysis of the low-iron-inducible gene pvdS and the constitutively expressed clpX gene (42). P. aeruginosa was grown in vitro in glucose minimal medium containing excess FeSO4 (3.5 μM) or in vivo as a monoculture or in coculture with S. aureus. P. aeruginosa PA14-LM1, which is unable to lyse S. aureus but possesses no observed growth defects under iron-limited conditions, was also grown in vivo in coculture with S. aureus.

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    FIG. 3.

    Growth yields of wild-type P. aeruginosa and P. aeruginosa PA14-LM1 grown in iron-limited MOPS minimal medium (see Materials and Methods) as a monoculture, with 10 μM FeSO4, in coculture with S. aureus, and with the addition of mechanically lysed S. aureus. Data are expressed as (the ratio of P. aeruginosa cell yield in the presence of the addition)/(monoculture cell yields with no addition) (numbers >1 indicate increased cell yield during growth with the indicated addition). For the two no-addition controls, the ratio was calculated by pair-wise comparisons of four individual replicates. S. aureus does not grow in this minimal medium due to amino acid auxotrophy. Less than 103 S. aureus cells were present in PA14-S. aureus coculture colonies at the time of sampling, while >109 remained in the PA14-LM1-S. aureus cocultures. Error bars represent the standard deviation for three to four experimental repeats.

Tables

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  • TABLE 1.

    Classes of in vivo-induced genes

    Functional classaNo. activatedbNo. repressedb
    Adaptation, protection102
    Amino acid biosynthesis and metabolism176
    Biosynthesis of cofactors73
    Carbon compound catabolism32
    Cell wall-LPS10
    Central intermediary metabolism41
    Chaperones and heat shock protein20
    Energy metabolism256
    Membrane proteins20
    Motility and attachment10
    Nucleotide biosynthesis and metabolism10
    Protein-secretion-export apparatus40
    Putative enzymes152
    Related to phage, transposon, plasmid011
    Secreted factors20
    Transcriptional regulators292
    Translation, posttranslational modification, degradation10
    Transport of small molecules3218
    Two-component regulatory systems30
    Hypothetical proteins6519
    Unknown (conserved hypothetical)146
    • ↵a Functional classes are from the P. aeruginosa genome website (www.pseudomonas.com).

    • ↵b Genes that were activated or repressed in the DMC at least fivefold compared to cells grown in vitro in MOPS medium.

  • TABLE 2.

    P. aeruginosa genes differentially regulated during in vivo growth

    ORFaGeneHomology or functionaFold regulationb
    0149Probable sigma-70 factor7
    0171Hypothetical protein−8
    0200Hypothetical protein7
    0280cysASulfate transport protein−11
    0281cysWSulfate transport protein−17
    0282cysTSulfate transport protein−11
    0283sbpSulfate-binding protein precursor−15
    0284Hypothetical protein−17
    0440*Probable oxidoreductase7
    0466Hypothetical protein−7
    0509*nirNProbable c-type cytochrome7
    0510Probable uroporphyrin III c-methyltransferase13
    0511*nirJHeme d1 biosynthesis protein7
    0512Conserved hypothetical protein8
    0513Probable transcriptional regulator8
    0514*nirLHeme d1 biosynthesis protein11
    0515Probable transcriptional regulator9
    0516*nirFHeme d1 biosynthesis protein8
    0517*nirCProbable c-type cytochrome precursor11
    0518*nirMCytochrome c551 precursor12
    0519*nirSNitrate reductase precursor15
    0521Probable cytochrome c oxidase subunit6
    0523*norCNitric oxide reductase subunit C32
    0524*norBNitric oxide reductase subunit B68
    0525*Probable denitrification protein15
    0587Conserved hypothetical protein5
    0613Hypothetical protein−5
    0614Hypothetical protein−5
    0617Probable bacteriophage protein−10
    0621Conserved hypothetical protein−5
    0622Probable bacteriophage protein−8
    0627Conserved hypothetical protein−5
    0629Conserved hypothetical protein−7
    0631Hypothetical protein−6
    0632Hypothetical protein−7
    0633Hypothetical protein−8
    0635Hypothetical protein−11
    0636Hypothetical protein−8
    0639Conserved hypothetical protein−9
    0641Probable bacteriophage protein−19
    0674Hypothetical protein25
    0675Probable sigma-70 factor5
    0713Hypothetical protein26
    0714Hypothetical protein24
    0781Hypothetical protein18
    0782†putAProline dehydrogenase8
    0865†hpd4-Hydroxyphenylpyruvate dioxygenase5
    0872†phhAPhenylalanine-4-hydroxylase31
    0910Hypothetical protein−18
    0911Hypothetical protein−6
    0921Hypothetical protein−6
    0984Colicin immunity protein7
    1123Hypothetical protein5
    1178oprHOuter membrane protein H1 precursor−17
    1179phoPTwo-component response regulator−5
    1195Hypothetical protein6
    1196Probable transcriptional regulator5
    1382Probable type II secretion system protein12
    1414Hypothetical protein5
    1516Hypothetical protein5
    1537Probable short-chain dehydrogenase6
    1540Conserved hypothetical protein7
    1541Probable drug efflux transporter8
    1552Probable cytochrome c−12
    1553Probable cytochrome c oxidase subunit−13
    1554Probable cytochrome oxidase subunit−5
    1673Hypothetical protein5
    1742Probable amidotransferase7
    1746Hypothetical protein9
    1837Hypothetical protein−13
    1838cysISulfite reductase−10
    1871lasALasA protease precursor6
    1887Hypothetical protein11
    1888Hypothetical protein10
    1892Hypothetical protein−9
    1894Hypothetical protein−9
    1895Hypothetical protein−10
    1896Hypothetical protein−9
    1897Hypothetical protein−35
    1911Probable transmembrane sensor6
    1912Probable sigma-70 factor7
    1922Probable TonB-dependent receptor11
    1924Hypothetical protein9
    1925Hypothetical protein8
    1999†Probable CoA transferase, subunit A35
    2000†Probable CoA transferase, subunit B44
    2001atoBAcetyl-CoA acetyltransferase13
    2003bdhA3-Hydroxybutyrate dehydrogenase6
    2004Conserved hypothetical protein8
    2016Probable transcriptional regulator5
    2114Probable MFS transporter−7
    2202Probable amino acid permease−7
    2204Probable binding protein component of ABC transporter−10
    2223Hypothetical protein6
    2247†bkdA12-Oxoisovalerate dehydrogenase (alpha subunit)38
    2248†BkdA22-Oxoisovalerate dehydrogenase (beta subunit)14
    2249†bkdBBranched-chain alpha-keto acid dehydrogenase (lipoamide component)15
    2250†lpdVLipoamide dehydrogenase (−Val)9
    2466Probable TonB-dependent receptor5
    2534Probable transcriptional regulator5
    2567Hypothetical protein5
    2648nuoMNADH dehydrogenase I chain−5
    2686pfeRTwo-component response regulator6
    2687pfeSTwo-component sensor5
    2753Hypothetical protein7
    2807Hypothetical protein−19
    2825Probable transcriptional regulator5
    2826Probable glutathione peroxidase5
    2929Hypothetical protein5
    2931Probable transcriptional regulator19
    2932morBMorphinone reductase71
    2933Probable MFS transporter31
    2934Probable hydrolase16
    2945Conserved hypothetical protein−6
    3038Probable porin−6
    3118†leuB3-Isopropylmalate dehydrogenase−5
    3120†leuD3-Isopropylmalate dehydratase small subunit−6
    3121†leuC3-Isopropylmalate dehydratase large subunit−6
    3126ibpAHeat shock protein7
    3188Probable permease of ABC sugar transporter−382
    3189Probable permease of ABC sugar transporter−79
    3195gapAGlyceraldehyde-3-phosphate dehydrogenase−6
    3249Probable transcriptional regulator5
    3309Conserved hypothetical protein6
    3313Hypothetical protein−5
    3391*nosRRegulatory protein54
    3392*nosZNitrous oxide reductase precursor25
    3393*nosDNosD protein11
    3394*nosFNosF protein16
    3395*nosYNosY protein8
    3396*nosLNosL protein8
    3404Probable secretion protein7
    3405hasEMetalloprotease secretion protein32
    3406hasDTransport protein16
    3415Probable dihydrolipoamide acetyltransferase9
    3416Probable pyruvate dehydrogenase E1 component, beta chain36
    3417Probable pyruvate dehydrogenase E1 component, alpha subunit7
    3418†ldhLeucine dehydrogenase8
    3441Probable molybdopterin-binding protein−12
    3442Probable ATP-binding component of ABC transporter−21
    3443Probable permease of ABC transporter−43
    3444Conserved hypothetical protein−161
    3445Conserved hypothetical protein−62
    3446Conserved hypothetical protein−19
    3450Probable antioxidant protein−8
    3516Probable lyase−5
    3581glpFGlycerol uptake facilitator protein9
    3582glpKGlycerol kinase6
    3584glpDGlycerol-3-phosphate dehydrogenase44
    3598Conserved hypothetical protein7
    3600Conserved hypothetical protein139
    3601Conserved hypothetical protein83
    3719Hypothetical protein21
    3720Hypothetical protein30
    3721Probable transcriptional regulator5
    3837Probable permease of ABC transporter−5
    3862Hypothetical protein6
    3870moaA1Molybdopterin biosynthetic protein7
    3871Probable peptidyl-prolyl cis-trans isomerase7
    3872*narIRespiratory nitrate reductase gamma chain9
    3873*narJRespiratory nitrate reductase delta chain11
    3874*narHRespiratory nitrate reductase beta chain24
    3875*narGRespiratory nitrate reductase alpha chain19
    3876*narK2Nitrite extrusion protein 210
    3877*narK1Nitrite extrusion protein 16
    3914moeA1Molybdenum cofactor biosynthetic protein7
    3915moaB1Molybdopterin biosynthetic protein5
    3922Conserved hypothetical protein−6
    3931Conserved hypothetical protein−16
    3933Probable choline transporter10
    3935tauDTaurine dioxygenase−16
    3936Probable permease of ABC taurine transporter−35
    3937Probable ATP-binding component of ABC taurine transporter−25
    3938Probable periplasmic taurine-binding protein precursor−21
    4063Hypothetical protein15
    4064Probable ATP-binding component of ABC transporter7
    4065Hypothetical protein5
    4156Probable TonB-dependent receptor10
    4160fepDFerric enterobactin transport protein5
    4167Probable oxidoreductase13
    4168Probable TonB-dependent receptor17
    4181Hypothetical protein16
    4182Hypothetical protein10
    4197Probable two-component sensor10
    4288Probable transcriptional regulator8
    4333Probable fumarase−5
    4364Hypothetical protein113
    4365Probable transporter54
    4442†cysNATP sulfurylase GTP-binding subunit, APS kinase−22
    4443†cysDATP sulfurylase small subunit−10
    4577Hypothetical protein5
    4588†gdhAGlutamate dehydrogenase−6
    4610Hypothetical protein9
    4621Probable oxidoreductase5
    4657Hypothetical protein5
    4738Conserved hypothetical protein−6
    4739Conserved hypothetical protein−9
    4834Hypothetical protein18
    4835Hypothetical protein16
    4836Hypothetical protein32
    4837Probable outer membrane protein38
    4838Hypothetical protein7
    5024Conserved hypothetical protein−13
    5027Hypothetical protein5
    5088Hypothetical protein7
    5100†hutUUrocanase7
    5102Hypothetical protein−8
    5106Conserved hypothetical protein6
    5170†arcDArginine-ornithine antiporter11
    5171†arcAArginine deiminase9
    5172†arcBOrnithine carbamoyltransferase, catabolic10
    5173†arcCCarbamate kinase6
    5302†dadXCatabolic alanine racemase6
    5303Conserved hypothetical protein9
    5304†dadAd-Amino acid dehydrogenase, small subunit9
    5351Rubredoxin−5
    5372†betACholine dehydrogenase12
    5373†betBBetaine aldehyde dehydrogenase12
    5374betITranscriptional regulator11
    5427adhAAlcohol dehydrogenase6
    5446Hypothetical protein13
    5475Hypothetical protein5
    5481Hypothetical protein−7
    5482Hypothetical protein−8
    5499‡np20Transcriptional regulator6
    5500znuCZinc transport protein6
    5532Hypothetical protein8
    5534Hypothetical protein13
    5535Conserved hypothetical protein15
    5536Conserved hypothetical protein52
    5538amiAN-Acetylmuramoyl-l-alanine amidase28
    5539Hypothetical protein8
    5540Hypothetical protein17
    5541Probable dihydroorotase11
    • ↵a From the P. aeruginosa genome website, www.pseudomonas.com. Genes involved in anaerobic metabolism (*), transport and metabolism of amino acids (†), or identified previously using IVET (‡) are listed in bold.

    • ↵b Fold change in P. aeruginosa mRNA level when grown in vivo in the DMC compared to that in bacteria grown in glucose minimal medium in vitro. Positive numbers represent induction, and negative numbers indicate repression in the DMC. All genes listed were also >5- fold regulated when DMC-grown and succinate-grown P. aeruginosa cultures were compared.

  • TABLE 3.

    Expression of P. aeruginosa iron-regulated genes during monoculture and coculture growth in vivo

    ORFaGeneHomology or functionaFold regulationb
    In vivo vs in vitroCoculture vs monoculture
    0471Probable transmembrane sensor7−17
    0472Probable sigma-70 factor8−34
    0500bioBBiotin synthase−9NC
    0672Hypothetical protein44−44
    0707toxRTranscriptional regulator6−4
    1245Hypothetical protein5−3
    1300Probable sigma-70 factor35−37
    1301Probable transmembrane sensor13−12
    2033Hypothetical protein20−23
    2034Hypothetical protein20−16
    2384Hypothetical protein41−46
    2385Probable acylase34−30
    2386pvdAl-Ornithine N5-oxygenase85−74
    2389Conserved hypothetical protein9−9
    2390Probable ATP-binding/permease fusion ABC transporter7−8
    2391Probable outer membrane protein5−7
    2392Hypothetical protein18−12
    2393Probable dipeptidase precursor53−127
    2394Probable aminotransferase57−60
    2395Hypothetical protein13−38
    2396Hypothetical protein13−7
    2397pvdEPyoverdine biosynthesis protein44−25
    2398fpvAFerripyoverdine receptor30−86
    2399pvdDPyoverdine synthetase40−23
    2400Probable nonribosomal peptide synthetase94−28
    2401Probable nonribosomal peptide synthetase94−40
    2402Probable nonribosomal peptide synthetase46−28
    2403Hypothetical protein58−22
    2404Hypothetical protein43−39
    2405Hypothetical protein43−37
    2406Hypothetical protein24−21
    2407Probable adhesion protein14−18
    2408Probable ATP-binding component of ABC transporter38−11
    2411Probable thioesterase84−111
    2412Conserved hypothetical protein197−203
    2413Probable class III aminotransferase51−136
    2424Probable nonribosomal peptide synthetase112−53
    2425Probable thioesterase44−51
    2426pvdSSigma factor66−117
    2427Hypothetical protein14−8
    2451Hypothetical protein9−9
    2452Hypothetical protein73−110
    2467Probable transmembrane sensor5−8
    2468Probable sigma-70 factor6−13
    3407hasApHeme acquisition protein2,180−724
    3408hasRHeme acquisition protein74−74
    3409Probable transmembrane sensor9−7
    3410Probable sigma-70 factor14−18
    3530Conserved hypothetical protein9−39
    3899Probable sigma-70 factor17−26
    3900Probable transmembrane sensor7−11
    3901fecAFe(III) dicitrate transport protein9−10
    4158fepCFerric enterobactin transport protein13−13
    4218Probable transporter40−22
    4219Hypothetical protein109−66
    4220Hypothetical protein288−48
    4221fptAFe(III) pyochelin receptor precursor81−92
    4222Probable ATP-binding component of ABC transporter34−13
    4223Probable ATP-binding component of ABC transporter26−15
    4224Hypothetical protein58−34
    4225pchFPyochelin synthetase52−65
    4226pchEDihydroaeruginoic acid synthetase53−46
    4227pchRTranscriptional regulator21−76
    4228pchDPyochelin biosynthesis protein74−66
    4229pchCPyochelin biosynthesis protein99−163
    4230pchBSalicylate biosynthesis protein126−118
    4231pchASalicylate biosynthesis isochorismate synthetase122−89
    4359Conserved hypothetical protein5−10
    4467Hypothetical protein21−10
    4468sodMSuperoxide dismutase40−48
    4469Hypothetical protein48−53
    4470fumC1Fumarate hydratase60−106
    4471Hypothetical protein100−131
    4570Hypothetical protein37−25
    4708Hypothetical protein9−6
    4709Probable hemin degrading factor9−8
    4710Probable outer membrane hemin receptor19−30
    4895Probable transmembrane sensor12−13
    4896Probable sigma-70 factor14−25
    4973thiCThiamin biosynthesis protein−14NC
    5312Probable aldehyde dehydrogenase6NC
    5313Probable pyridoxal-dependent aminotransferase7NC
    • ↵a From the P. aeruginosa genome website, www.pseudomonas.com.

    • ↵b Regulation of P. aeruginosa iron-regulated genes (28) as determined by Affymetrix GeneChip analysis. Two conditions were compared: monoculture growth in vivo versus monoculture in vitro growth in glucose minimal medium with added FeSO4 (positive numbers represent induction in vivo); and in vivo coculture growth versus in vivo monoculture growth (positive numbers represent induction during coculture growth). NC, no change.

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Staphylococcus aureus Serves as an Iron Source for Pseudomonas aeruginosa during In Vivo Coculture
Lauren M. Mashburn, Amy M. Jett, Darrin R. Akins, Marvin Whiteley
Journal of Bacteriology Jan 2005, 187 (2) 554-566; DOI: 10.1128/JB.187.2.554-566.2005

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Staphylococcus aureus Serves as an Iron Source for Pseudomonas aeruginosa during In Vivo Coculture
Lauren M. Mashburn, Amy M. Jett, Darrin R. Akins, Marvin Whiteley
Journal of Bacteriology Jan 2005, 187 (2) 554-566; DOI: 10.1128/JB.187.2.554-566.2005
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