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Table 1 Chromosomal genes differentially expressed in response to anaerobic conditionsa

From: Deep sequencing-based analysis of the anaerobic stimulon in Neisseria gonorrhoeae

Gene

ORF ID

Rep 1b

Rep 2

Definitionc

Regulond

Small molecule biosynthesis

hda

NGO0187

4.1

4.1

Histone deacetylase-like protein/acetoin utilization protein

 

pdxH

NGO0658

4.3

5.5

Pyridoxamine 5-phosphate oxidase

MtrR

mobA

NGO0754

3.5

4.6

Molybdopterin-guanine dinucleotide biosynthesis protein

NsrR

leu1

NGO0848

6.6

4.5

2-isopropylmalate synthase

 

folA

NGO1694

3.8

2.8

Dihydrofolate reductase

RpoH

Transport and binding proteins

fHBP

NGO0033

3.5

4.2

Factor H binding protein

 

hecA

NGO0706

3.2

4.9

Filamentous hemagglutinin

 

bfrA

NGO0794

14.1

9.9

Bacterioferritin A

 

bfrB

NGO0795

9.7

10.1

Bacterioferritin B

MtrR

pil

NGO1177

3.5

3.5

Neisseria-specific type IV pilin-related protein

 
 

NGO1440

4.4

2.8

ABC-type amino acid transporter, periplasmic protein

 

lecA

NGO1981

5.0

3.9

Adhesin protein

Lrp

Energy metabolism/Oxidation-Reduction

cybP

NGO0805

3.2

2.8

Nickel-dependent hydrogenase, b-type cytochrome subunit

 

npd

NGO1024

9.6

7.9

2-Nitropropane dioxygenase-like

MtrR

aniA

NGO1276

28.4

28.0

Nitrite reductase

NsrR, FNR

eftD

NGO1396

5.2

5.1

Electron transfer flavoprotein-ubiquinone oxidoreductase

 

Macromolecular biosynthesis

rl34

NGO2182

3.0

3. 1

50S ribosomal protein L34

 

Regulation

     

farR

NGO0058

4.0

3.7

MarR family transcriptional regulator

Lrp, MtrR

nmlR

NGO0602

7.2

7.6

Transcriptional regulator nmlR

NmlR, FNR

xre

NGO0797

3.2

3.4

XRE family transcriptional regulator

 

marR

NGO1244

5.4

15.2

MarR-family transcriptional regulator

RpoH, MtrR

nosR a

NGO1401/1402

9.4

9.5

Regulator of nitrous oxide reductase pseudogenes

FNR

lexA

NGO1427

4.2

5.3

LexA-family repressor

LexA

arsR

NGO1562

6.1

2.2

ArsR-family transcriptional regulator

 

Cell Structure

ompA

NGO1559

3.7

3.4

Outer membrane protein

 

lpcA

NGO1986

4.2

6.1

Phosphoheptose isomerase

 

Adaptation and stress response

grx3

NGO0114

3.3

6.6

Glutaredoxin 3

Fur

recN

NGO0318

4.7

5.5

Repair protein RecN

Fur, LexA

htpX

NGO0399

11.8

8.6

Heat shock protein, Peptidase family M48

Lrp

dnrN

NGO0653

8.9

12.3

Iron-sulfur cluster repair protein

NsrR, FNR

 

NGO0757

2.6

4.1

Putative periplasmic Cpx-family sensor kinase involved in P pilus formation

 

hslR

NGO0822

2.7

5.0

Heat shock protein HSP-15

 
 

NGO1022

3.8

3.4

DEDDh family exonuclease

 

clpB

NGO1046

4.9

9.4

Endopeptidase Clp ATP-binding chain B (HSP- F84.1)

RpoH, MtrR

recX

NGO1053

3.6

2.8

RecX-family regulator of RecA function

 

tehB

NGO1161

2.6

4.0

Tellurite resistance protein

 

hsp33

NGO1189

6.1

5.2

Heat shock protein HSP-33 chaperonin

MtrR

 

NGO1245

4.0

8.5

ABC-type multidrug transport system, ATPase/permease

 

hit

NGO1273

2.3

5.5

Protein Kinase C Interacting protein belonging to the ubiquitous HIT family of hydrolases that act on alpha-phosphates of ribonucleotides

 

nudH

NGO1334

3.3

3.3

Nudix hydrolase, dinucleoside polyphosphate hydrolase

 

grpE

NGO1422

3.6

2.7

Heat shock protein (HSP-70 cofactor; nucleotide exchange factor)

RpoH, MtrR

erpA

NGO1426

2.8

2.6

Putative iron-sulfur cluster insertion protein

RpoH, Lrp

dnaK

NGO1429

2.7

3.4

Heat shock protein, chaperone

RpoH

 

NGO1566

3.4

3.1

Nudix hydrolase, catalyzing the hydrolysis of nucleoside diphosphates

 

ntrA

NGO1702

3.5

20.1

Nitroreductase-like family containing uncharacterized proteins similar to nitroreductase

 

ccp

NGO1769

5.6

12.1

Cytochrome c peroxidase

 

yhhF

NGO1860

3.7

4.1

Probable DNA methylase

 

dnaJ

NGO1901

2.8

5.1

Heat shock protein HSP-40

RpoH

Hypothetical or Unassigned

 

NGO0010

5.1

7.2

Neisseria-specific protein, uncharacterized

 
 

NGO0011

3.2

3.0

Conserved hypothetical protein

 
 

NGO0119

5.4

5.1

Neisseria-specific protein, uncharacterized; possible ribonuclease

 
 

NGO0165

3.2

5.9

Neisseria-specific protein, uncharacterized

 
 

NGO0569

3.8

2.1

Conserved hypothetical protein (possible transcriptional regulator)

 
 

NGO0570

3.5

3.4

Possible DNA-binding CreA protein

RpoH

 

NGO0618

3.3

2.7

Neisseria-specific protein, uncharacterized

 
 

DUF331

4.1

7.8

Uncharacterized protein family DUF331; the function of this family is unknown

 
 

NGO0802

3.7

4.0

Hypothetical protein (possible Neisseria-specific protein)

 
 

NGO0854

3.6

8.4

Hypothetical protein

 
 

NGO0895

6.4

4.6

Neisseria-specific protein, uncharacterized

 
 

NGO0896

4.1

5.0

Hypothetical protein

 
 

NGO0995

3.1

3.3

Neisseria-specific protein, uncharacterized

 
 

NGO1033

4.3

6.8

Probable transglycosylase

 
 

NGO1037

4.4

5.2

Hypothetical protein

 
 

NGO1191

3.5

2.7

Neisseria-specific protein, uncharacterized

 
 

NGO1277

6.6

7.0

Conserved hypothetical protein (NirV) FGE- sulfatase super family.

 
 

NGO1428

14.3

8.4

Neisseria-specific protein, uncharacterized

LexA

 

NGO1517

4.8

4.8

Neisseria-specific protein, uncharacterized

NsrR

 

NGO1793

6.4

4.3

Conserved hypothetical protein (probable integral membrane protein)

 
 

NGO1987

3.1

4.4

Uncharacterized protein family UPF0102; the function of this family is unknown

 
 

NGO2023

2.4

7.3

Conserved hypothetical protein

 

Small RNA fnrS c

 

24.9

17.8

Probable small regulatory RNA

FNR

Gene

ORF ID

Rep 1

Rep 2

Definition

Regulon

Ngo Φ 1 phage

 

NGO0463

9.2

5.9

Putative phage associated protein

 
 

NGO0464

12.3

9.0

Putative phage associated protein

 
 

NGO0465

15.4

7.3

Putative phage associated protein

 
 

NGO0467

23.6

29.8

Putative phage associated protein

 
 

NGO0472

94.6

19.7

Putative phage associated protein

FNR

dnaB

NGO0485

6.1

4.2

Replicative DNA helicase

 
 

NGO0488

4.2

10.0

Putative phage associated protein

 
 

NGO0489

10.2

16.9

Phage Holliday junction resolvase (RusA-like) protein

 
 

NGO0491

14.2

5.1

Putative phage associated protein

 
 

NGO0492

8.7

6.6

Putative phage associated protein

 
 

NGO0494

10.0

10.9

Putative phage associated protein

 
 

NGO0495

9.6

7.6

Putative phage associated protein

 
 

NGO0496

16.1

12.9

Putative phage associated protein

 
 

NGO0497

24.1

17.0

Putative phage associated protein

 
 

NGO0498

18.0

9.5

Putative phage associated protein

 
 

NGO0499

17.4

12.9

Putative phage associated protein

 
 

NGO0500

17.6

6.6

Putative phage associated protein

 
 

NGO0501

27.4

9.1

Putative phage associated protein

 
 

NGO0502

47.2

6.8

Putative phage associated protein

 
 

NGO0503

6.0

4.8

Putative phage associated protein

 
 

NGO0504

14.4

5.2

Putative phage associated protein

 
 

NGO0506

15.9

11.3

Putative phage associated protein

 
 

NGO0507

22.3

12.1

Putative phage associated protein

 
 

NGO0508

15.6

11.1

Putative phage associated protein

 
 

NGO0509

3.5

3.6

Putative phage associated protein

 
 

NGO0510

7.1

5.6

Putative phage associated protein

 
 

NGO0512

9.4

13.2

Putative phage associated protein

 
 

NGO0513

4.9

5.2

Putative phage associated protein

 
 

NGO0514

9.8

6.2

Putative phage associated protein

 
 

NGO0522

9.4

5.6

Putative phage associated protein

 

Ngo Φ2 phage

 

NGO1100

4.1

5.0

Putative phage associated protein

 
 

NGO1120

75.5

16.0

Putative phage associated protein

 
 

NGO1131

19.4

16.8

Putative phage associated protein

 
 

NGO1132

11.3

16.2

Putative phage associated protein

 

Ngo Φ3 phage

 

NGO1614

8.2

11.0

Putative phage associated protein

 
 

NGO1615

10.3

7.2

Conserved hypothetical protein (type I restriction enzyme related)

FNR

 

NGO1624

34.0

16.0

Putative phage associated protein

 
 

NGO1627

6.6

4.4

Conserved hypothetical protein (probable phage origin)

 
 

NGO1628

7.6

4.9

Putative phage associated protein

 
 

NGO1633

26.9

137.3

Putative phage associated protein

 
 

NGO1634

27.4

18.8

Putative phage associated protein

 
 

NGO1635

58.1

5.4

Putative phage associated protein

 
 

NGO1636

26.4

10.0

Putative phage associated protein

 
 

NGO1637

16.6

5.5

Putative phage associated protein

 
 

NGO1640

22.4

10.6

Putative phage associated protein

 

Ngo Φ5 phage

 

NGO0731

5.1

7.3

Putative phage associated protein

 
 

NGO0732

3.3

2.2

Putative phage associated protein

 

Gene

ID

Rep 1

Rep 2

Definition

Regulon

Small molecule biosynthesis

cysK

NGO0340

-2.8

-6.7

Cysteine synthase

FNR

hesB

NGO0632

-3.8

-4.0

Iron-sulfur cluster biosynthesis

 

iscU

NGO0633

-4.8

-5.3

Iron-sulfur cluster assembly scaffold protein

 

iscS

NGO0636

-4.8

-5.6

Cysteine desulferase

 

hisD

NGO1240

-3.3

-3.2

Histidinol dehydrogenase

 

pgsA

NGO1247

-3.8

-7.1

CDP-alcohol phosphatidyltransferase

 

asd

NGO1997

-3.3

-5.0

Aspartate-semialdehyde dehydrogenase

 

Transport and binding proteins

gluP

NGO0142

-3.1

-4.3

Glucose/galactose transporter

 

nhaC

NGO0143

-2.8

-3.3

Na+/H+ antiporter (NhaC)

 

amtB

NGO0198

-3.7

-5.3

Ammonium Transporter Family

 

fbp

NGO0217

-4.8

-5.6

ABC-type iron transporter, periplasmic binding protein

Fur, Lrp

oxiA

NGO0372

-6.7

-20.0

Bacterial extracellular solute-binding protein

FarR

 

NGO0373

-3.7

-11.1

ABC-type arginine transport system, permease component

FarR

glnQ

NGO0374

-2.9

-11.1

ABC-type amino acid transporter, ATP-binding protein

FarR, FNR

citT

NGO0377

-5.6

-9.1

Di- and tri-carboxylate transporters (inorganic ion transport)

 

cysA

NGO0445

-5.6

-9.1

ABC-type sulfate transporter, ATP-binding protein

Lrp

sbp

NGO0877

-4.8

-25.0

ABC-related sulfate-binding protein

 
 

NGO1290

-3.8

-3.3

Putative sodium/alanine symport protein

 

hemO

NGO1318

-7.1

-12.5

Heme oxygenase/iron starvation protein

Fur

lldP

NGO1361

-9.1

-8.3

L-lactate permease (partial only)

 

exbD

NGO1377

-3.4

-3.6

Membrane bound biopolymer transport protein ExbD/TolR

 

exbB

NGO1378

-3.1

-5.0

Transport protein

 

lctP

NGO1449

-4.0

-14.3

L-lactate permease

 

potF

NGO1494

-7.7

-20.0

ABC-type spermidine/putrescine transporter, solute binding protein

MtrR

putP

NGO1552

-5.6

-11.1

Sodium/proline symport protein

 

ompU

NGO1688

-2.6

-3.7

Putative iron uptake protein

FNR

yaaJ

NGO1787

-3.3

-4.3

Sodium/alanine symport protein

 
 

NGO1807

-2.7

-3.8

Amino-acid symport protein

 

gltS

NGO1890

-3.1

-5.0

Sodium/glutamate symport protein

MtrR

 

NGO1954

-3.6

-6.3

Di- and tri-peptide permease, PRT2

 

sstT

NGO1957

-4.5

-11.1

Sodium/serine symport protein

 

glnM

NGO2011

-6.7

-12.5

ABC-type amino acid transport system, permease component

MtrR, FarR

glnP

NGO2012

-10.0

-10.0

ABC-type amino acid transport system, permease component

FarR

glnQ

NGO2013

-6.3

-11.1

ABC-type amino acid transporter, ATP-binding protein

MtrR, FarR

apaA

NGO2014

-6.3

-16.7

Bacterial extracellular solute-binding proteins, family 3

MtrR, FarR

 

NGO2016

-3.6

-3.3

Predicted permease

 
 

NGO2096

-6.3

-12.5

SNF family sodium-dependent transporter

 

Energy metabolism/Oxidation-Reduction

 

NGO0108

-4.0

-5.9

NADPH-dependent FMN reductase

Fur, Lrp

lldD

NGO0639

-7.1

-11.1

L-lactate dehydrogenase

 

eda

NGO0713

-3.0

-5.6

KHG-KDPG bifunctional aldolase

 

rpeC

NGO0758

-4.8

-3.8

Ribulose-phosphate 3-epimerase

 

fdx

NGO0825

-5.3

-5.3

Ferredoxin

 

cisY

NGO0918

-3.6

-3.8

Type II citrate synthase

Lrp

sdhB

NGO0920

-2.9

-4.2

Succinate dehydrogenase, iron-sulfur protein

Lrp

sdhA

NGO0921

-3.7

-3.4

Succinate dehydrogenase, flavoprotein subunit

Lrp

sdhD

NGO0922

-2.9

-3.4

Succinate dehydrogenase, membrane anchor protein

 

sdhC

NGO0923

-1.8

-4.2

Succinate dehydrogenase, cytochrome b556 chain

 

fumC

NG01029

-2.9

-6.3

Fumarate hydratase

Fur, MtrR

gpmA

NGO1258

-4.0

-5.6

Phosphoglyceromutase

Lrp

nqrA

NGO1413

-4.0

-7.7

Na(+)-translocating NADH-quinone reductase subunit A

 

nqrB

NGO1414

-5.0

-8.3

Na(+)-translocating NADH-quinone reductase subunit B

 

nqrC

NGO1415

-4.2

-8.3

Na(+)-translocating NADH-quinone reductase subunit C

 

nqrD

NGO1416

-3.8

-16.7

Na(+)-translocating NADH-quinone reductase subunit D

 

nqrE

NGO1417

-4.3

-12.5

Na(+)-translocating NADH-quinone reductase subunit E

 

nqrF

NGO1418

-3.7

-9.1

Na(+)-translocating NADH-quinone reductase subunit F

MtrR

dadA

NGO1808

-3.6

-5.3

D-amino acid dehydrogenase small subunit

 

mqo

NGO1980

-3.7

-5.0

Malate:quinone oxidoreductase

 

Macromolecular biosynthesis

greB

NGO0262

-3.7

-5.3

Transcription elongation factor

 

parC

NGO1259

-3.8

-2.9

DNA topoisomerase IV subunit A

 
 

NGO1261

-6.3

-7.1

S-adenosylmethionine-dependent methyltransferase

 

rplP

NGO1831.1

-3.2

-6.3

50S ribosomal protein L16

Lrp

rpsC

NGO1832

-3.2

-7.7

30S ribosomal protein S3

Lrp

rplV

NGO1833

-2.9

-10.0

50S ribosomal protein L22

 

rpsS

NGO1834

-2.8

-12.5

30S ribosomal protein S19

 

rplD

NGO1837

-2.2

-7.1

50S ribosomal protein L4

 

rspJ

NGO1841

-2.7

-7.1

30S ribosomal protein S10

Lrp

rpoC

NGO1850

-3.3

-5.0

DNA-directed RNA polymerase subunit beta'

 

rpoB

NGO1851

-2.1

-4.5

DNA-directed RNA polymerase subunit beta

 

Cell Structure

nspA

NGO0233

-3.1

-3.7

Outer membrane protein (Probable Opa protein)

 

GNA2132

NGO1958

-5.3

-8.3

Predicted lipoprotein GNA2132

 

lgtG

NGO2072

-7.7

-6.3

Probable lipooligosaccharide glycosyl transferase G

 

Adaptation and stress response

cspA

NGO0410

-3.8

-3.3

Cold shock protein

 

trxB

NGO0580

-2.6

-4.8

Thioredoxin reductase

NmlR

trx1

NGO0652

-5.3

-6.3

Thioredoxin I

Fur

cstA

NGO1064

-3.8

-12.5

Putative carbon starvation protein

 

mtrF

NGO1368

-7.7

-25.0

Antibiotic resistance efflux pump component

MtrR, FarR

sspB

NGO2131

-4.5

-3.6

Protease specificity-enhancing factor

 

Hypothetical or unassigned

 

NGO0554

-4.5

-5.0

Hypothetical protein

Fur

 

NGO0635

-4.8

-3.6

Hypothetical protein

 
 

NGO1065

-4.8

-7.7

Hypothetical protein

 
 

NGO2097

-3.7

-3.1

Conserved hypothetical protein

 

Small RNA

nrrF e

 

-4.8

-7.7

Fur-repressed small regulatory RNA

Fur

  1. a Gonococci grown in an anaerobe chamber on plates containing 5 mM nitrite.
  2. b The fold change for each replicate was calculated by comparing RPKM values of anaerobically grown gonococci to RPKM values of aerobically grown gonococci. A positive value represents an induction of gene expression anaerobically, and a negative value represents a repression of gene expression anaerobically
  3. c Protein definitions are derived from the annotated FA1090 genome (NCBI), and/or the NCBI conserved domain database [33].
  4. d (Fur) Genes that have been shown to be directly regulated by Fur in Sebastian et al., (2002) [95] and/or Jackson et al., (2010) [75]. (RpoH) Genes reported to be upregulated during RpoH overexpression in Gunesekere et al., (2006) [23]. (LexA) Genes reported to be in the LexA regulon by Schook et al., (2010) [50]. (Lrp) Genes found to be differentially expressed in a N. meningitidis Δlrp mutant (NMB0573, closest gonococcal homolog is NGO1407, NCBI) by microarray analysis in Ren et al., (2007) [46]. (MtrR) Genes found to be differentially expressed in a gonococcal ΔmtrR mutant by microarray analysis in FolsterΔ et al., (2009) [56]. (FarR) Genes reported to be in the FarR regulon by Friedrich et al., (2007) [54]. (NmlR) Genes reported to be in the NmlR regulon by Kidd et al., (2005) [47]. (FNR) Genes found to be differentially expressed microaerobically in a Δfnr mutant with and without nitrite by microarray analysis in Whitehead et al., (2007) [7]. (NsrR) Genes reported to be in the NsrR regulon by Isabella et al., (2007) [3] and Isabella, (2010) [19].
  5. e Fur-repressed small regulatory RNA described by Ducey et al., (2009) [96].