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INFECTION AND IMMUNITY, June 2005, p. 3764–3772
0019-9567/05/$08.00⫹0 doi:10.1128/IAI.73.6.3764–3772.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Vol. 73, No. 6

Effect of Anaerobiosis and Nitrate on Gene Expression in
Pseudomonas aeruginosa
M. J. Filiatrault, V. E. Wagner, D. Bushnell, C. G. Haidaris, B. H. Iglewski,*
and L. Passador†
Department of Microbiology and Immunology, University of Rochester School of Medicine and
Dentistry, Rochester, New York 14642
Received 15 October 2004/Returned for modification 24 November 2004/Accepted 2 February 2005

DNA microarrays were used to examine the transcriptional response of Pseudomonas aeruginosa to anaerobiosis and nitrate. In response to anaerobic growth, 691 transcripts were differentially expressed. Comparisons of P. aeruginosa grown aerobically in the presence or the absence of nitrate showed differential expression
of greater than 900 transcripts.
Pseudomonas aeruginosa is capable of anaerobic growth by
anaerobic respiration with nitrate, nitrite, or nitrous oxide as
the terminal electron acceptor (8, 9) or by generating ATP
from arginine catabolism (16, 26). Biofilms display hypoxic
gradients, and biofilm formation is enhanced under oxygen
limitation (7, 28, 31). P. aeruginosa grows as a biofilm in the
anoxic environment of the lower airway mucus plugs in cystic
fibrosis patients (7, 28).
Except with genes involved in denitrification (1, 29) and
several other genes (12, 14, 15, 20), little is known about anaerobic gene expression in P. aeruginosa. The present study
used microarrays to identify genes differentially expressed by P.
aeruginosa in response to anaerobiosis and nitrate.
Differential gene expression in response to anaerobic
growth. Growth curves for P. aeruginosa PAO1 cultured aerobically or anaerobically were generated to establish the RNA
sampling points (27) (supplemental Fig. A at http://www.urmc
.rochester.edu/smd/mbi/bhi/). Total RNA from three independent P. aeruginosa PAO1 aerobic or anaerobic cultures
was isolated and processed as previously described (27). RNA
integrity was assessed by reverse transcriptase PCR (RT-PCR)
using primers specific for pilA, and purity was confirmed by
PCR. Processing of RNA, microarray data generation, analysis, and validation by quantitative RT-PCR were performed
as previously described (27) (supplemental Table C at http:
//www.urmc.rochester.edu/smd/mbi/bhi/). All RT-PCR data
were normalized using PA4232, as the expression does not
change under the conditions examined (our data and reference
27).
The expression of total transcripts (72% to 80%) was
comparable to that seen in other P. aeruginosa microarray
studies (19, 27). A total of 691 transcriptional changes, representing approximately 12% of the genome, resulted in
statistically significantly different levels of expression in re-

sponse to anaerobic growth, with 245 transcripts up-regulated
and 446 transcripts down-regulated (supplemental Table A at
http://www.urmc.rochester.edu/smd/mbi/bhi/). Those transcripts
(n ⫽ 153) demonstrating a threefold or higher change are listed
in Table 1 and grouped into functional categories (supplemental
Fig. B at http://www.urmc.rochester.edu/smd/mbi/bhi/).
We found numerous genes with expression patterns consistent with anaerobic growth and previous reports, such as the
repression of napBAD, napF (17, 32), hcnAC (20), flgB, flgE,
flgI, flgL, fliC, fliD, fleS, fleR, fliE, fliF, fliM, flhA, and flhF (10)
and increased expression of hemF (22) (supplemental Table A
at http://www.urmc.rochester.edu/smd/mbi/bhi/).
Many genes involved in quorum sensing (lasR, lasA, lasB,
rhlR, rhlI, rhlA, and mvfR) were repressed under oxygen limitation. Consistent with reduced mvfR expression, transcripts
involved in the biosynthesis of the Pseudomonas quinolone
signal (pqsB and pqsE) and anthranilate synthase components
I and II (phnAB) (4) were decreased.
Genes involved in cytochrome c maturation, ccmB, ccmC,
ccmE, and ccmF, were up-regulated under anaerobic conditions, which is consistent with observations of Escherichia coli
(24). Additionally, transcript levels for PA5491 (a probable
cytochrome) were increased, suggesting that this previously
uncharacterized cytochrome may play a role in anaerobic respiration. Transcript levels for several other putative cytochromes (PA0918, PA1555, PA1556, PA2266, PA2482,
PA3331, PA4571, and PA4619) were repressed, suggesting that
they may not be required for anaerobic respiration.
Our data implicated many novel genes in anaerobic growth.
There were 284 transcripts classified as genes encoding hypothetical proteins differentially expressed under anaerobic conditions. Several genes which play a role in virulence (PA0930)
(21) or biofilm formation (PA2128, PA2129, and PA2130) (25)
were induced during anaerobic growth.
Differential gene expression in response to nitrate. In contrast to previous studies (32), no significant changes were observed (Table 1) for most of the genes involved in denitrification (nar, nir, nos, and nor), suggesting that nitrate may induce
their expression. This is supported by the capacity of P. aeruginosa for aerobic denitrification (5) and aerobic Nir activity
when nitrate is available (1, 13). Many denitrification genes are

* Corresponding author. Mailing address: University of Rochester
School of Medicine and Dentistry, Department of Microbiology and Immunology, 601 Elmwood Avenue, Box 672, Rochester, NY 14642. Phone:
(585) 275-3402. Fax: (585) 473-9573. E-mail: bigl@mail.rochester.edu.
† Present address: Thomson Physicians World, 150 Meadowlands
Parkway, Secaucus, NJ 07094.
3764

VOL. 73, 2005

NOTES

3765

TABLE 1. Differentially expressed transcripts between cultures grown aerobically with nitrate and cultures grown anaerobically with nitratea
Transcript

Gene

Fold changeb

Growth
phasec

PA0024
PA0025
PA0049
PA0149
PA0179
PA0200
PA0430
PA0433
PA0447
PA0471
PA0472
PA0586
PA0587
PA0747
PA0792
PA0802
PA0836
PA0918
PA0930
PA0997
PA0998
PA0999
PA1000
PA1002
PA1045
PA1052
PA1076
PA1140
PA1173
PA1174
PA1175
PA1176
PA1179
PA1180
PA1195
PA1282
PA1323
PA1324
PA1331
PA1418
PA1419
PA1420
PA1421
PA1429
PA1516
PA1517
PA1518
PA1523
PA1546
PA1556
PA1561
PA1673
PA1789
PA1806
PA1882
PA1883
PA1939
PA2012
PA2013
PA2014
PA2015
PA2016
PA2024
PA2026
PA2073
PA2110
PA2112
PA2113

hemF
aroE

4.5
3.5
⫺5.1
4.1
⫺4.3
⫺5.5
3.4
6.5
⫺5.2
9.7
4.1
⫺4.6
⫺4.9
⫺3.8
⫺3.1
5.3
⫺3.1
⫺3.6
3.9
⫺4.3/⫺18
⫺11.1/⫺43.7
⫺21
⫺10.8
⫺9.6
3
⫺3.5
⫺3.8
⫺3.2
⫺4.1
⫺3.2
⫺3.8
⫺3.8
⫺3.4
⫺4.8
⫺6.1
⫺6.1
⫺3.8
⫺3
3.3
⫺8.4
⫺14.2
⫺15.5
⫺15
⫺3
⫺3.3
⫺4.3
⫺4.1
⫺4.4
⫺4
⫺3.2
⫺4.5
⫺5.3
⫺3.9
⫺3.3
⫺3
⫺3
⫺3.7
⫺6.5
⫺4.8
⫺4.9
⫺6.8
⫺9.4
⫺4.7
⫺3.2
⫺6.6
⫺7.4
⫺4
⫺3.5/⫺3.9

ES
ES
ES
ML
ML
ML
ES
ML
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
B
B
ES
ML
ES
ML
ML
ML
ML
ML
ML
ML
ML
ES
ES
ML
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ES
ES
ML
ML
ML
ML
ML
ML
ES
ML
ES
ML
B

metF
gcdH

prpD

pqsB
pqsC
pqsD
pqsE
phnB

napB
napA
napD
napF
phoP
phoQ

gbuA

xdhB
hemN
aer
fabI

Protein descriptiond

Coproporphyrinogen III oxidase, aerobic
Shikimate dehydrogenase
Hypothetical protein
Probable sigma-70 factor, ECF subfamily
Probable two-component response regulator
Hypothetical protein
5,10-Methylenetetrahydrofolate reductase
Hypothetical protein
Glutaryl-CoA dehydrogenase
Probable transmembrane sensor
Probable sigma-70 factor, ECF subfamily
Hypothetical protein
Hypothetical protein
Probable aldehyde dehydrogenase
Propionate catabolic protein PrpD
Hypothetical protein
Probable acetate kinase
Cytochrome b561
Two-component sensor
Beta keto acyl-acyl carrier protein synthase
Beta keto acyl-acyl carrier protein synthase
3-Oxoacyl (acyl carrier protein) synthase III
Quinolone signal reponse signal
Anthranilate synthase component II
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Cytochrome c-type protein NapB precursor
Periplasmic nitrate reductase protein NapA
NapD protein of periplasmic nitrate reductase
Ferredoxin protein NapF
Two-component response regulator PhoP
Two-component sensor PhoQ
Hypothetical protein
Probable MFS transporter
Hypothetical protein
Hypothetical protein
Hypothetical protein
Probable sodium-solute symport protein
Probable transporter
Hypothetical protein
Guanidinobutyrase
Probable cation-transporting P-type ATPase
Hypothetical protein
Hypothetical protein
Hypothetical protein
Xanthine dehydrogenase
Oxygen-independent coproporphyrinogen III oxidase
Probable cytochrome c oxidase subunit
Aerotaxis receptor Aer
Hypothetical protein
Hypothetical protein
NADH-dependent enoyl-ACP reductase
Probable transporter
Probable NADH-ubiquinone plastoquinone oxidoreductase
Hypothetical protein
Probable acyl-CoA carboxylase alpha chain
Probable enoyl-CoA hydratase isomerase
Probable acyl-CoA carboxyltransferase beta chain
Probable acyl-CoA dehydrogenase
Probable transcriptional regulator
Probable ring-cleaving dioxygenase
Hypothetical protein
Probable transporter (membrane subunit)
Hypothetical protein
Hypothetical protein
Probable porin
Continued on following page

3766

INFECT. IMMUN.

NOTES
TABLE 1—Continued

Transcript

PA2114
PA2119
PA2128
PA2129
PA2130
PA2193
PA2259
PA2261
PA2264
PA2265
PA2302
PA2303
PA2366
PA2423
PA2478
PA2552
PA2553
PA2554
PA2555
PA2557
PA2572
PA2573
PA2753
PA2754
PA2759
PA2780
PA2790
PA3181
PA3329
PA3330
PA3333
PA3334
PA3337
PA3418
PA3425
PA3458
PA3465
PA3520
PA3531
PA3552
PA3553
PA3688
PA3724
PA3790
PA3866
PA3876
PA3877
PA3914
PA3915
PA3916
PA3917
PA3918
PA3919
PA4063
PA4064
PA4070
PA4129
PA4134
PA4211
PA4309
PA4354
PA4371
PA4504
PA4571
PA4577
PA4602
PA4619
PA4739

Gene

cupA1
cupA2
cupA3
hcnA
ptxS

fabH2
rfaD
idh

bfrB

lasB
oprC
narK2
narK1
moeA1
moaB1
moaE
moaD
moaC

phzBI
pctA

glyA3

Fold changeb

Growth
phasec

⫺4.5/⫺4.4
⫺5.7
4.2
9.5
3.6
⫺3.1
⫺4.8
⫺9.4
⫺3.2
⫺3.4
⫺3.8
⫺3.2
⫺3.9
⫺3.3
8.4
⫺5.1
⫺7.6
⫺7.1
⫺7.9
⫺4.3
⫺3
⫺3.6
⫺9
⫺5
⫺3.1
⫺3.5
⫺3.3
⫺3.2
⫺7.2
⫺4.7
⫺3.8
⫺3.6
⫺12.2
⫺4.2
⫺3.2
⫺6.3
⫺5.4
⫺3.9/⫺11.2
⫺8
⫺11.5
⫺14.8
⫺3
⫺5.7
10.2
3
⫺5.9
⫺7.3
⫺8.8
⫺3.9/⫺7.8
⫺3.4/⫺5.3
⫺5.7
⫺3.4/⫺6
⫺4.8
⫺3
⫺3.1
⫺5.2
⫺4.9
⫺6.7
⫺3.5
⫺4.3
3.1
8.8
⫺3.5
⫺6.4
⫺6
3
⫺3.1
⫺3.8

B
ML
ES
ML
ML
ES
ML
ML
ML
ML
ES
ES
ES
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ES
ES
ES
ML
ML
ES
ML
ML
B
ML
ES
ES
ML
ES
ML
ES
ML
ML
ES
B
B
ES
B
ML
ES
ES
ML
ES
ES
ES
ML
ES
ML
ML
ML
ML
ES
ML
ES

Protein descriptiond

Probable MFS transporter
Alcohol dehydrogenase (Zn dependent)
Fimbrial subunit CupA1
Chaperone CupA2
Usher protein CupA3
Hydrogen cyanide synthase HcnA
Transcriptional regulator PtxS
Probable 2-ketogluconate kinase
Conserved hypothetical protein
Gluconate dehydrogenase
Probable nonribosomal peptide synthetase
Hypothetical protein
Hypothetical protein
Hypothetical protein
Probable thiol-disulfide interchange protein
Probable acyl-CoA dehydrogenase
Probable acyl-CoA thiolase
Probable short-chain dehydrogenase
Probable AMP-binding enzyme
Probable AMP-binding enzyme
Probable two-component response regulator
Probable chemotaxis transducer
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
2-Keto-3-deoxy-6-phosphogluconate aldolase
Hypothetical protein
Probable short chain dehydrogenase
3-Oxoacyl (acyl carrier protein) synthase III
Probable acyl carrier protein
ADP-L-glycero-D-manno-heptose 6-epimerase
Leucine dehydrogenase
Hypothetical protein
Probable transcriptional regulator
Hypothetical protein
Hypothetical protein
Bacterioferritin
Hypothetical protein
Probable glycosyl transferase
Hypothetical protein
Elastase LasB
Outer membrane protein OprC
Pyocin protein
Nitrite extrusion protein 2
Nitrite extrusion protein 1
Molybdenum cofactor biosynthetic protein A1
Molybdopterin biosynthetic protein B1
Molybdopterin converting factor, large subunit
Molybdopterin converting factor, small subunit
Molybdopterin biosynthetic protein C
Hypothetical protein
Hypothetical protein
Probable ATP-binding component of ABC transporter
Probable transcriptional regulator
Hypothetical protein
Hypothetical protein
Probable phenazine biosynthesis protein
Chemotactic transducer PctA
Hypothetical protein
Hypothetical protein
Probable permease of ABC transporter
Probable cytochrome c
Hypothetical protein
Serine hydroxymethyltransferase
Probable c-type cytochrome
Hypothetical protein
Continued on following page

VOL. 73, 2005

NOTES

3767

TABLE 1—Continued
Transcript

PA4852
PA4878
PA5027
PA5170
PA5171
PA5172
PA5208
PA5216
PA5217
PA5496
PA5497
PA5504
PA5506
PA5507
PA5508
PA5510
PA5570

Gene

arcD
arcA
arcB

rpmH

Fold changeb

Growth
phasec

Protein descriptiond

3.1
⫺4.3
⫺5
⫺17.1
⫺6.6
⫺5.7
⫺3.2
3.8
5.2
3.2
3.5
3.1
⫺3.9
⫺4.1
⫺3
⫺3.4
3.3

ML
ES
ML
ML
ML
ML
ML
ML
ML
ES
ES
ML
ML
ML
ML
ML
ML

Hypothetical protein
Probable transcriptional regulator
Hypothetical protein
Arginine-ornithine antiporter
Arginine deiminase
Ornithine carbamoyltransferase, catabolic
Conserved hypothetical protein
Probable permease of ABC iron transporter
Probable binding protein component of ABC iron transporter
Hypothetical protein
Hypothetical protein
Probable permease of ABC transporter
Hypothetical protein
Hypothetical protein
Probable glutamine synthetase
Probable transporter
50S ribosomal protein L34

a

Only transcripts identified as anaerobically regulated that demonstrated a change of equal to or greater than threefold are reported. A list of all transcripts identified
as being anaerobically regulated exhibiting a statistically significant change (P ⱕ 0.05) is available online (http://www.urmc.rochester.edu/smd/mbi/bhi/). Genes are
identified by transcript number, gene name, and protein description (http://www.pseudomonas.com).
b
The change (n-fold) was calculated by comparing PAO1 grown aerobically with nitrate present (baseline) to PAO1 grown anaerobically with nitrate present
(experimental). A positive change represents an induction caused by the lack of oxygen, and a negative change represents repression caused by the lack of oxygen. When
two values are given, the first is for the ML phase and the second is for the ES phase.
c
Growth stage(s) during which statistically significantly differential transcript expression was observed. ML, midexponential phase; ES, early stationary phase; B, both
midexponential and early stationary phases.
d
Protein descriptions are from the Pseudomonas Genome Project website (www.pseudomonas.com). ECF, extracytoplasmic function; CoA, coenzyme A; MSF, major
facilitator superfamily; ABC, ATP-binding cassette.

influenced by the presence of an N-oxide (2). To investigate
this, microarray analysis using RNA from cultures grown aerobically in the presence or the absence of nitrate was performed. Nearly 18% of the genome (919 transcripts; 415 transcripts induced and 504 repressed) exhibited differential
expression in response to nitrate (supplemental Table B at
http://www.urmc.rochester.edu/smd/mbi/bhi/). The 266 genes
demonstrating a threefold or greater change are listed in Table
2. Functional categories are shown in supplemental Fig. C at
http://www.urmc.rochester.edu/smd/mbi/bhi/.
The transcription of narI was up-regulated by the presence
of nitrate, while narG, narH, and narJ were not found to
be statistically differentially expressed. napB, napA, napD,
nosRDFYL, and nirS exhibited increased expression in the
presence of nitrate. Other genes encoding proteins either
implicated (PA0513, PA0514, PA0516, PA0518, and PA0521)
or known to be involved (nirL, nirM, nirN, and nirF) in the
processing of respiratory system components were up-regulated in response to nitrate. Our results indicate that nitrate
alone is sufficient to induce the expression of many enzymes
involved in denitrification regardless of the presence or absence of oxygen and explain the apparent lack of differential
expression of some of these genes in our anaerobic experiments.
The expression of a number of genes involved in the production of virulence factors of P. aeruginosa were influenced by
the addition of nitrate. For example, while mexAB and rhlAB
expression were repressed by nitrate, mexF was up-regulated.
Transcription of a recently described chemotaxis cluster
(PA0174-0179) found to be required for optimal chemotaxis
(6) and aerotaxis (11) was induced by the nitrate. The R-type
pyocins (PA0614 to PA0646) (18) were induced by nitrate. We

also observed differential expression of 306 transcripts which
currently do not have defined functions. Importantly, a couple
of transcripts (PA0459 and PA5167) have been previously
found to be required for lung infection (21).
Consistent with previous reports for Escherichia coli (23),
Shewanella oneidensis, and Bacillus subtilis (3, 30), we found
that P. aeruginosa significantly changes its transcriptional profile in the absence of oxygen or in the presence of nitrate. It
should be noted that our results are biased towards using
nitrate as the terminal electron acceptor, and using other nitric
oxides or arginine may affect other genes.
Our results provide a global view of oxygen-regulated gene
expression in P. aeruginosa and illustrate the complex regulation of anaerobic metabolism in this organism. Changes in
genes encoding virulence factors and quorum-sensing components implicate altered pathogenic pathways during anaerobic
growth. Our identification of a substantial number of genes
encoding proteins of unknown function should contribute to
further annotation of the genome and provide impetus for
further research on the role of these genes in P. aeruginosa
physiology and metabolism.
We thank A. Brooks, K. Miller, L. Ascroft, and K. Wahowski at
the Microarray Core Facility in The Functional Genomics Center at
the University of Rochester for technical support and assistance
with the quantitative RT-PCR and Cystic Fibrosis Foundation
Therapeutics, Inc., for subsidizing the P. aeruginosa Affymetrix
GeneChip arrays.
This work was supported by grants IGLEWS00V0 and IGLEWS03FG0 to B.H.I., L.P., and C.G.H. from Cystic Fibrosis Foundation
Therapeutics and grant R37AI33713 to B.H.I from the NIH. M.J.F is
supported by an NIH fellowship (F32AI056825).

3768

INFECT. IMMUN.

NOTES

TABLE 2. Differentially expressed transcripts between cultures grown aerobically without nitrate and cultures grown aerobically with nitratea
Transcript

PA0045
PA0046
PA0047
PA0129
PA0130
PA0131
PA0132
PA0160
PA0164
PA0174
PA0175
PA0176
PA0177
PA0178
PA0179
PA0200
PA0386
PA0447
PA0459
PA0494
PA0509
PA0510
PA0512
PA0513
PA0514
PA0516
PA0518
PA0519
PA0521
PA0526
PA0586
PA0587
PA0614
PA0623
PA0624
PA0627
PA0628
PA0632
PA0633
PA0639
PA0742
PA0743
PA0744
PA0746
PA0747
PA0782
PA0792
PA0793
PA0795
PA0887
PA0889
PA0910
PA0985
PA1070
PA1071
PA1072
PA1073
PA1173
PA1174
PA1175
PA1249
PA1282
PA1317
PA1318
PA1319
PA1320
PA1337
PA1338

Gene
name

gabP

gcdH
nirN

nirL
nirF
nirM
nirS

putA
prpD
prpC
acsA
aotQ
braG
braF
braE
braD
napB
napA
napD
aprA
cyoA
cyoB
cyoC
cyoD
ansB
ggt

Fold changeb

Growth
phasec

⫺3.5
⫺3.4/⫺5.4
⫺3.1/⫺3.8
4.3
4.2
3.9
3.5
⫺3.8
⫺4.8
3.2
4.8
3.7
3.8
3
3.5
8.7
⫺3.2
3.4
4
3.2
11.8
17.5
13.9
16
16.1
16.3
4.9
9.3
23.6
8.1
4.1
4.5
3.3
3.5
4.1
4.6
4.5
4.3
4
3.8
3.6
3.3
3.7
5.5
5.5
⫺5.1
3.9
4
4.3
3.8
⫺3.2
3.4
7.6
4.1
3.7
3.4
3
6
3.8
3.3
6.7
6.3
⫺3.7
⫺3.1
⫺3
⫺4.8
4.8
3.4

ES
B
B
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ES
ES
ML
ML
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ML
ML
ML
ML
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ML
ML
ML
ML
ML
ML

Protein descriptiond

Hypothetical protein
Hypothetical protein
Hypothetical protein
Gamma-aminobutyrate permease
Probable aldehyde dehydrogenase
Hypothetical protein
Beta-alanine–pyruvate transaminase
Hypothetical protein
Probable gamma-glutamyltranspeptidase
Conserved hypothetical protein
Probable chemotaxis protein methyltransferase
Probable chemotaxis transducer
Probable purine-binding chemotaxis protein
Probable two-component sensor
Probable two-component response regulator
Hypothetical protein
Probable oxidase
Glutaryl-CoA dehydrogenase
Probable ClpA/B protease ATP-binding subunit
Probable acyl-CoA carboxylase subunit
Probable c-type cytochrome
Probable uroporphyrin-III C-methyltransferase
Conserved hypothetical protein
Probable transcriptional regulator
Heme d1 biosynthesis protein NirL
Heme d1 biosynthesis protein NirF
Cytochrome c551 precursor
Nitrite reductase precursor
Probable cytochrome c oxidase subunit
Hypothetical protein
Conserved hypothetical protein
Conserved hypothetical protein
Hypothetical protein
Probable bacteriophage protein
Hypothetical protein
Conserved hypothetical protein
Conserved hypothetical protein
Hypothetical protein
Hypothetical protein
Conserved hypothetical protein
Hypothetical protein
Probable 3-hydroxyisobutyrate dehydrogenase
Probable enoyl-CoA hydratase/isomerase
Probable acyl-CoA dehydrogenase
Probable aldehyde dehydrogenase
Proline dehydrogenase PutA
Propionate catabolic protein PrpD
Hypothetical protein
Citrate synthase 2
Acetyl-CoA synthetase
Arginine/ornithine transport protein AotQ
Hypothetical protein
Probable colicin-like toxin
Branched-chain amino acid transport protein BraG
Branched-chain amino acid transport protein BraF
Branched-chain amino acid transport protein BraE
Branched-chain amino acid transport protein BraD
Cytochrome c-type protein NapB precursor
Periplasmic nitrate reductase protein NapA
NapD protein of periplasmic nitrate reductase
Alkaline metalloproteinase precursor
Probable MFS transporter
Cytochrome o ubiquinol oxidase subunit II
Cytochrome o ubiquinol oxidase subunit I
Cytochrome o ubiquinol oxidase subunit III
Cytochrome o ubiquinol oxidase subunit IV
Glutaminase-asparaginase
Gamma-glutamyltranspeptidase precursor
Continued on following page

VOL. 73, 2005

NOTES

3769

TABLE 2—Continued
Transcript

PA1418
PA1419
PA1420
PA1421
PA1428
PA1559
PA1566
PA1596
PA1657
PA1660
PA1661
PA1662
PA1663
PA1664
PA1665
PA1666
PA1667
PA1668
PA1669
PA1761
PA1762
PA1790
PA1847
PA1855
PA1856
PA1883
PA1888
PA1902
PA1903
PA1904
PA1971
PA1985
PA1986
PA1987
PA1988
PA1989
PA1990
PA1999
PA2003
PA2011
PA2012
PA2013
PA2014
PA2024
PA2052
PA2066
PA2067
PA2068
PA2069
PA2110
PA2112
PA2114
PA2194
PA2250
PA2266
PA2300
PA2306
PA2327
PA2329
PA2330
PA2331
PA2358
PA2370
PA2404
PA2405
PA2406
PA2408
PA2442

Gene
name

gbuA

htpG

phzD2
phzE2
phzF2
braZ
pqqA
pqqB
pqqC
pqqD
pqqE
bdhA

cynS

hcnB
lpdV
chiC

gcvT2

Fold changeb

Growth
phasec

7.5
10.9
6
5.6
⫺7.4
⫺3.6
⫺5.9
⫺3.2
⫺5
⫺4.8
⫺3.4
⫺3.3
⫺3.3
⫺4
⫺4.4
⫺3
⫺4.8
⫺3.2
⫺4.7
3.2
3.7
⫺4.8
4.3
12.7
29/4.1
3
3.9
⫺13.5
⫺12.3
⫺12.9
⫺3.3
3.6
3
4
5
3.3
5.6
8.2
3.1
9.1
9.1
5.2
4.4
3.7
3.2
⫺4.4
⫺3.9
⫺7.5
⫺7.7
7.9
4.1
3.1
⫺3.3
3.7
⫺3
⫺6.1
⫺3.1
⫺4
⫺4.1
⫺5.2/⫺3.6
⫺6.7/⫺3.2
⫺3.7
4.8
⫺3.5
⫺6.2/⫺5
⫺3
⫺3.2
3.2

ML
ML
ML
ML
ES
ML
ES
ML
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ML
ES
ES
ML
B
ES
ML
ES
ES
ES
ES
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ML
ES
ES
ES
ES
ES
ML
ES
ES
ES
ES
ES
ES
ES
ML
B
B
ML
ML
ES
B
ES
ML
ES

Protein descriptiond

Probable sodium-solute symport protein
Probable transporter
Hypothetical protein
Guanidinobutyrase
Conserved hypothetical protein
Hypothetical protein
Conserved hypothetical protein
Heat shock protein HtpG
Conserved hypothetical protein
Hypothetical protein
Hypothetical protein
Probable ClpA/B-type protease
Probable transcriptional regulator
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Conserved hypothetical protein
Hypothetical protein
Probable cytochrome oxidase subunit
Probable NADH-ubiquinone/plastoquinone oxidoreductase
Hypothetical protein
Phenazine biosynthesis protein PhzD
Phenazine biosynthesis protein PhzE
Probable phenazine biosynthesis protein
Branched chain amino acid transporter BraZ
Pyrroloquinoline quinone biosynthesis protein A
Pyrroloquinoline quinone biosynthesis protein B
Pyrroloquinoline quinone biosynthesis protein C
Pyrroloquinoline quinone biosynthesis protein D
Pyrroloquinoline quinone biosynthesis protein E
Probable peptidase
Probable CoA transferase, subunit A
3-Hydroxybutyrate dehydrogenase
Hydroxymethylglutaryl-CoA lyase
Probable acyl-CoA carboxylase alpha chain
Probable enoyl-CoA hydratase/isomerase
Probable acyl-CoA carboxyltransferase beta chain
Probable ring-cleaving dioxygenase
Cyanate lyase
Hypothetical protein
Probable hydrolase
Probable MFS transporter
Probable carbamoyl transferase
Hypothetical protein
Conserved hypothetical protein
Probable MFS transporter
Hydrogen cyanide synthase HcnB
Lipoamide dehydrogenase-Val
Probable cytochrome c precursor
Chitinase
Conserved hypothetical protein
Probable permease of ABC transporter
Probable ATP-binding component of ABC transporter
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Hypothetical protein
Probable ATP-binding component of ABC transporter
Glycine cleavage system protein T2
Continued on following page

3770

INFECT. IMMUN.

NOTES
TABLE 2—Continued

Transcript

PA2443
PA2444
PA2445
PA2446
PA2460
PA2483
PA2552
PA2553
PA2554
PA2555
PA2570
PA2573
PA2593
PA2629
PA2663
PA2691
PA2763
PA2798
PA2968
PA2969
PA3019
PA3188
PA3221
PA3222
PA3232
PA3234
PA3235
PA3294
PA3327
PA3328
PA3329
PA3330
PA3331
PA3333
PA3334
PA3335
PA3336
PA3391
PA3393
PA3394
PA3395
PA3396
PA3416
PA3418
PA3430
PA3431
PA3432
PA3478
PA3479
PA3486
PA3487
PA3530
PA3552
PA3569
PA3570
PA3605
PA3655
PA3700
PA3723
PA3741
PA3742
PA3811
PA3813
PA3872
PA3876
PA3880
PA3881
PA3901

Gene
name

Fold changeb

Growth
phasec

sdaA
glyA2
gcvP2
gcvH2

6
6.8
3.1
3.1
⫺3.3
3
8.9
10.9
6.7
3.9
⫺5.1
3.1
⫺5.2
⫺3.6
41.4
3
⫺6.5
⫺3.2
⫺3.2
⫺3.3
⫺3.2
3.4
8.1
7
3.2
5
3.5
⫺4
⫺3.9
⫺7.9
⫺9.6
⫺10.9
⫺8.4
⫺9.1
⫺8.4
⫺11.5
⫺12.5
35.5
31.3
33.4
36
21.6
3.9
3.3
⫺3
⫺8.8
⫺10.1
⫺6.5
⫺6.5
⫺12
⫺3.2
4.1
6.5
3.9
4.8
⫺5.3
⫺3.1
⫺3.6
4.2
⫺4.7
⫺3.7
3.2
3.6
37
3.4
7.6
3.1
⫺5.7

ML
ML
ML
ML
ES
ES
ML
ML
ML
ML
ES
ML
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ES
ES
ML
ML
ML
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ML
ML
ML
ML
ES
ES
ES
ES
ES
ES
ML
ML
ES
ML
ES
ML
ES
ML
ES
ES
ES
ML
ES
ES
ML

palL
purB

fabD
plsX
csaA

fabH2

nosR
nosD
nosF
nosY
nosL
ldh

rhlB
rhlA
pldA
mmsB
mmsA
tsf
lysS
rplS
hscB
iscU
narI
narK2
fecA

Protein descriptiond
L-Serine

dehydratase
Serine hydroxymethyltransferase
Glycine cleavage system protein P2
Glycine cleavage system protein H2
Hypothetical protein
Conserved hypothetical protein
Probable acyl-CoA dehydrogenase
Probable acyl-CoA thiolase
Probable short-chain dehydrogenase
Probable AMP-binding enzyme
PA-I galactophilic lectin
Probable chemotaxis transducer
Hypothetical protein
Adenylosuccinate lyase
Hypothetical protein
Conserved hypothetical protein
Hypothetical protein
Probable two-component response regulator
Malonyl-CoA-(acyl carrier protein) transacylase
Fatty acid biosynthesis protein PlsX
Probable ATP-binding component of ABC transporter
Probable permease of ABC sugar transporter
CsaA protein
Hypothetical protein
Probable nuclease
Probable sodium-solute symporter
Conserved hypothetical protein
Hypothetical protein
Probable nonribosomal peptide synthetase
Probable FAD-dependent monooxygenase
Hypothetical protein
Probable short-chain dehydrogenase
Cytochrome P450
3-Oxoacyl (acyl carrier protein) synthase III
Probable acyl carrier protein
Hypothetical protein
Probable MFS transporter
Regulatory protein NosR
NosD protein
NosF protein
NosY protein
NosL protein
Probable pyruvate dehydrogenase E1 component, beta chain
Leucine dehydrogenase
Probable aldolase
Conserved hypothetical protein
Hypothetical protein
Rhamnosyltransferase chain B
Rhamnosyltransferase chain A
Conserved hypothetical protein
Phospholipase D
Conserved hypothetical protein
Conserved hypothetical protein
3-Hydroxyisobutyrate dehydrogenase
Methylmalonate-semialdehyde dehydrogenase
Hypothetical protein
Elongation factor Ts
Lysyl-tRNA synthetase
Probable FMN oxidoreductase
Hypothetical protein
50S ribosomal protein L19
Heat shock protein HscB
Probable iron-binding protein IscU
Respiratory nitrate reductase gamma chain
Nitrite extrusion protein 2
Conserved hypothetical protein
Hypothetical protein
Fe(III) dicitrate transport protein FecA
Continued on following page

VOL. 73, 2005

NOTES

3771

TABLE 2—Continued
Transcript

PA3905
PA3907
PA3912
PA3913
PA3914
PA3915
PA3916
PA3917
PA3918
PA3979
PA4055
PA4063
PA4142
PA4170
PA4210
PA4211
PA4217
PA4235
PA4292
PA4432
PA4479
PA4497
PA4512
PA4610
PA4620
PA4665
PA4670
PA4672
PA4743
PA4762
PA4853
PA4916
PA4917
PA4918
PA4919
PA4920
PA4921
PA5023
PA5048
PA5117
PA5118
PA5139
PA5167
PA5168
PA5169
PA5275
PA5296
PA5304
PA5372
PA5415
PA5436
PA5446
PA5448
PA5460
PA5496
PA5553
PA5554
PA5556
PA5557
ig326671
ig4326394
ig4713098

Gene
name

moeAI
moaBI
moaE
moaD
moaC
ribC

phzAI
phzBI
phzS
bfrA
rpsI
mreD
lpxO1
prfA
prs
rbfA
grpE
fis

pncB1
nadE

typA
thiI

rep
dadA
betA
glyAI
wbpY
atpC
atpD
atpA
atpH

Fold changeb

Growth
phasec

Protein descriptiond

⫺4.1
⫺3.8
3.3
3.6/14.8
7.3/⫺62.7
6.3/⫺15.6
5.8
6.7
6.3
⫺3.1
⫺4.1
4.1
⫺4.1
5.8
⫺11.9
⫺14.8
⫺13.1
3.4
⫺4.5
⫺4
⫺3.1
3.8
⫺3.1
4.2
⫺3
⫺3.5
⫺3.9
⫺5
⫺3.2
⫺3.1
⫺3.4
⫺9.8
⫺6.7
⫺7.2
⫺6.2
⫺4.4
⫺3.9
4.3
⫺4.2
⫺5
⫺3.5
⫺5
3
4.3
3.6
3.8
⫺3.1
⫺4.3
4.2
4.3
⫺3.4
⫺7.2
3.2
⫺3.2
3.1
⫺3
⫺3.1
⫺3.4
⫺3
2.9/3.5
3.2
⫺5.3

ES
ES
ML
B
B
B
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ES
ES
ES
ES
ES
ES
ES
ML
ES
ML
ML
ML
ML
ML
ML
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ML
ML
ES
ML
ML
ML
ES
ML
ML
ML
ML
B
ES
ES

Hypothetical protein
Hypothetical protein
Conserved hypothetical protein
Probable protease
Molybdenum cofactor biosynthetic protein A1
Molybdopterin biosynthetic protein B1
Molybdopterin-converting factor, large subunit
Molybdopterin-converting factor, small subunit
Molybdopterin biosynthetic protein C
Hypothetical protein
Riboflavin synthase alpha chain
Hypothetical protein
Probable secretion protein
Hypothetical protein
Probable phenazine biosynthesis protein
Probable phenazine biosynthesis protein
Flavin-containing monooxygenase
Bacterioferritin
Probable phosphate transporter
30S ribosomal protein S9
Rod shape-determining protein MreD
Probable binding protein component of ABC transporter
Lipopolysaccharide biosynthetic protein
Hypothetical protein
Hypothetical protein
Peptide chain release factor 1
Ribose-phosphate pyrophosphokinase
Peptidyl-tRNA hydrolase
Ribosome-binding factor A
Heat shock protein GrpE
DNA-binding protein Fis
Hypothetical protein
Hypothetical protein
Hypothetical protein
Nicotinate phosphoribosyltransferase
NH3-dependent NAD synthetase
Hypothetical protein
Conserved hypothetical protein
Probable nuclease
Regulatory protein TypA
Thiazole biosynthesis protein Thil
Hypothetical protein
Probable C4-dicarboxylate-binding protein
Probable dicarboxylate transporter
Probable C4-dicarboxylate transporter
Conserved hypothetical protein
ATP-dependent DNA helicase Rep
D-Amino acid dehydrogenase, small subunit
Choline dehydrogenase
Serine hydroxymethyltransferase
Probable biotin carboxylase subunit of a transcarboxylase
Hypothetical protein
Glycosyltransferase WbpY
Hypothetical protein
Hypothetical protein
ATP synthase epsilon chain
ATP synthase beta chain
ATP synthase alpha chain
ATP synthase delta chain
Intergenic region between PA0458 and PA0459, 326671–327284, plus strand
Intergenic region between PA3969 and PA3970, 4326394–4327696, plus strand
Intergenic region between PA4280 and PA4281, 4713098–4713795, plus strand

a
Only transcripts identified as nitrate regulated that demonstrated a change of equal to or greater than threefold are reported. A list of all transcripts identified as
being nitrate regulated exhibiting a statistically significant change (P ⱕ 0.05) is available online (http://www.urmc.rochester.edu/smd/mbi/bhi/). Genes are identified by
transcript number, gene name, and protein description (http//www.pseudomonas.com).
b
The change (n-fold) was calculated by comparing PAO1 grown aerobically lacking nitrate (baseline) to PAO1 grown aerobically with nitrate (experimental). A
positive change represents induction caused by the presence of nitrate, and a negative change represents repression caused by the presence of nitrate. When two values
are given, the first is for the ML phase and the second is for the ES phase.
c
Growth stage(s) during which statistically significantly differential transcript expression was observed. ML, midexponential phase; ES, early stationary phase; B, both
midexponential and early stationary phases.
d
Protein descriptions are from the Pseudomonas Genome Project website (www.pseudomonas.com). CoA, coenzyme A; FAD, flavin adenine dinucleotide; MSF,
major facilitator superfamily; ABC, ATP-binding cassette; FMN, flavin mononucleotide.

3772

NOTES

INFECT. IMMUN.
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