Identification of transporter proteins for PQQ-secretion pathways by transcriptomics and proteomics analysis in <i>Gluconobacter oxydans</i> WSH-003

doi:10.1007/s11705-016-1580-4

Front. Chem. Sci. Eng.

2017, Vol. 11

Issue (1) : 72-88 https://doi.org/10.1007/s11705-016-1580-4

RESEARCH ARTICLE

Identification of transporter proteins for PQQ-secretion pathways by transcriptomics and proteomics analysis in Gluconobacter oxydans WSH-003

Hui Wan¹,Yu Xia¹,Jianghua Li^1,²,Zhen Kang^1,²,Jingwen Zhou^1,²(

)

¹. School of Biotechnology and Key Laboratory of Industrial Biotechnology, Ministry of Education, Jiangnan University, Wuxi 214122, China
². Synergetic Innovation of Center of Food Safety and Nutrition, Jiangnan University, Wuxi 214122, China

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Abstract

Pyrroloquinoline quinone (PQQ) plays a significant role as a redox cofactor in combination with dehydrogenases in bacteria. These dehydrogenases play key roles in the oxidation of important substrates for the biotechnology industry, such as vitamin C production. While biosynthesis of PQQ genes has been widely studied, PQQ-transport mechanisms remain unclear. Herein, we used both two-dimensional fluorescence-difference gel electrophoresis tandem mass spectrometry and RNA sequencing to investigate the effects of pqqB overexpression in an industrial strain of Gluconobacter oxydans WSH-003. We have identified 73 differentially expressed proteins and 99 differentially expressed genes, a majority of which are related to oxidation-reduction and transport processes by gene ontology analysis. We also described several putative candidate effectors that responded to increased PQQ levels resulting from pqqB overexpression. Furthermore, quantitative PCR was used to verify five putative PQQ-transport genes among different PQQ producing strains, and the results showed that ompW, B932_1930 and B932_2186 were upregulated in all conditions. Then the three genes were over-expressed in G. oxydans WSH-003 and PQQ production were detected. The results showed that extracellular PQQ of B932_1930 (a transporter) and B932_2186 (an ABC transporter permease) overexpression strains were enhanced by 1.77-fold and 1.67-fold, respectively. The results suggest that the proteins encoded by PqqB, B932_1930 and B932_2186 might enhance the PQQ secretion process.

Keywords 2D-DIGE pqqB pyrroloquinoline quinone RNA-Seq Vitamin C

Corresponding Author(s): Jingwen Zhou

Just Accepted Date: 13 July 2016 Online First Date: 18 September 2016 Issue Date: 17 March 2017

Cite this article:

Hui Wan,Yu Xia,Jianghua Li, et al. Identification of transporter proteins for PQQ-secretion pathways by transcriptomics and proteomics analysis in Gluconobacter oxydans WSH-003[J]. Front. Chem. Sci. Eng., 2017, 11(1): 72-88.

URL:

https://academic.hep.com.cn/fcse/EN/10.1007/s11705-016-1580-4
https://academic.hep.com.cn/fcse/EN/Y2017/V11/I1/72

Fig.1 The operon encoding PQQ biosynthesis in G. oxydans. Genes encoding PQQ biosynthesis are composed of pqqA/B/C/D/E in G. oxydans. PqqA provides the amino acids glutamate and tyrosine for constructing the PQQ backbone. PqqB may indirectly transport PQQ and plays a role as an oxygenase in the course of converting peptide PqqA to PQQ. The PqqC protein plays a crucial role in the final step of PQQ synthesis. PqqD is a novel peptide chaperone that interacts with PqqE, which is an S-adenosyl-L-methionine (SAM) superfamily protein proposed to catalyze C?C bond formation between glutamate and tyrosine

Tab.1 Primers used in overexpression of genes

Tab.2 Primers used for qPCR

Fig.2 Comparison of intracellular and extracellular PQQs among different G. oxydans recombinant strains. After cells reached the stationary phase (48 h), intracellular and extracellular PQQ levels were determined. WT: wild type strain; ET: pBBR1MCS-2-tufB strain; TB: pBBR1MCS-2-tufB-pqqB strain; TA: pBBR1MCS-2-tufB-pqqA strain; TP: pGUC-k0203-GS-k0095-pqqABCDE strain; TW: pBBR1MCS-2-tufB-ompW strain; T1930: pBBR1MCS-2-tufB-B932_1930 strain; T2186: pBBR1MCS-2-tufB-B932_2186 strain

Tab.3 Alignment statistics of total RNA-Seq results

Fig.3 FPKM distributions in the G. oxydans ET and TB strains based on RNA-Seq analysis. The scatterplots were generated by cummeRbund v2.0 and R v3.0 following analysis of RNA-Seq data. After cells reached the exponential phase (12 h), total RNA was extracted and correlations between transcript expression levels detected by MiSeq. FPKM values of moderately expressed genes ranged from 100 to 500, with the average at ~300. ET: pBBR1MCS-2-tufB strain; TB: pBBR1MCS-2-tufB-pqqB strain

Fig.4 Comparative proteomics analysis between G. oxydans ET and TB strains using 2D-DIGE-MS. (a) 2D-DIGE overlay map of membrane proteins; (b) 2D-DIGE overlay map of intracellular proteins; (c) Distribution map of differentially expressed membrane proteins; (d) Distribution map of differentially expressed intracellular proteins. 2D-DIGE images were labeled with Cy2 (blue for all samples), Cy3 (green, ET), and Cy5 (red, TB). A total of 73 differentially expressed proteins were identified by MALDI-TOF- MS/MS analysis

Fig.5 Categorization of GO terms based on differentially expressed genes and proteins. Differentially expressed genes and proteins were classified into three GO categories: cellular component, molecular function, and biological process. The Y-axis indicates the different GO terms, and the X-axis indicates the number of genes or proteins in a category. Grey: differentially expressed genes determined by RNA-Seq analysis; Black: differentially expressed proteins determined by 2D-DIGE analysis

Fig.6 Categorization of biological process terms based on differentially expressed genes and proteins. All differentially expressed genes and proteins were first mapped to GO terms in the database (http://www.geneontology.org/). From all gene and protein data, 79.6% were annotated and classified with GO terms by filtering node scores<5. The top five terms were: cellular nitrogen compound metabolic process, small molecule metabolic process, oxidation-reduction process, and translation, transmembrane transport

Fig.7 Transcription levels of genes-of-interest based on qPCR. The X-axis indicates the genes-of-interest, and the Y-axis indicates the fold change between G. oxydans ET and TB strains. ET strain was used for the control. Error bars represent deviation in results from experiments performed in triplicate. Expression of 16S RNA was used as an internal control

Fig.8 Transcription levels of putative PQQ-transport genes based on qPCR. The X-axis indicates the five putative PQQ-transport genes, while the Y-axis indicates the fold change between G. oxydans ET, TB, TA and TP strains. ET strain was used as the control. Error bars represent deviation in results from experiments performed in triplicate. Expression of 16S rRNA was used as an internal control. ET: pBBR1MCS-2-tufB strain; TB: pBBR1MCS-2-tufB-pqqB strain; TA: pBBR1MCS-2-tufB-pqqA strain; TP: pGUC-k0203-GS-k0095-pqqABCDE strain

Fig.9 SDS-PAGE analysis of putative PQQ-transport proteins overexpression. All the mass of overexpression proteins were the same as the theory value. Lane M: mass of standard protein; lane 1: global proteins of pBBR1MCS-2-tufB (ET) strain; lane 2: global proteins of pBBR1MCS-2-tufB-B932_2186 (T2186) strain; lane 3: global proteins of pBBR1MCS-2-tufB-B932_1930 (T1930) strain; lane 4: global proteins of pBBR1MCS-2-tufB-ompW (TW) strain

Gene ID	Protein definition	Gene name	Fold change TB/ET		p-value
Gene ID	Protein definition	Gene name	RNA-Seq	2D-DIGE	p-value
	Metabolic process
B932_0165	Exodeoxyribonuclease III		0.45		0.00015
B932_0188	2-isopropylmalate synthase		1.86		0.0086
B932_0238	DapD	dapD		2.93	0.0016
B932_0280	Acetyl-CoA carboxylase carboxyltransferase subunit alpha	accA		0.46	0.0027
B932_0287	Carbonic anhydrase 1	cynT		2.45	0.0058
B932_0325	6-phosphogluconate dehydrogenase-like protein		2.04		0.00115
B932_0326	Bifunctional transaldolase/phosphoglucose isomerase		2.11		0.00525
B932_0327	Transketolase	tktA		0.35	0.0038
B932_0356	Peptidyl-prolyl cis-trans isomerase precursor	ppiC		0.5	0.00033
B932_0357	Glutamate N-acetyltransferase / amino-acid N-acetyltransferase	argJ		1.84	0.00048
B932_0447	PLP dependent protein	yggS	1.72		0.0155
B932_0456	Polynucleotide phosphorylase	pnp		0.53	0.0011
B932_0522	GlpX	glpX		0.18	0.0082
B932_0624	Lipid A biosynthesis acyltransferase		0.64		0.0495
B932_0718	Thioredoxin		1.64		0.03165
B932_0982	Pyrroline-5-carboxylate reductase	proC		1.63	0.00015
B932_0988	Lipopolysaccharide modification acyltransferase		0.66		0.04825
B932_1020	Glutamine synthetase	glnA		1.75	0.00042
B932_1090	Glucose-1-phosphate thymidylyltransferase	rfbA		0.43	0.00055
B932_1110	Phosphatase			2.36	0.00055
B932_1236	Phosphoadenosine phosphosulfate reductase		1.99		0.02345
B932_1314	Fructose-1,6-bisphosphate aldolase	aldO		1.8	0.0069
B932_1399	Radical SAM protein		0.59		0.0399
B932_1406	Fructose-bisphosphate aldolase	fbaA		0.52	0.018
B932_1409	Nitrogen fixing thioredoxin-like protein NifU	nifU		0.32	0.00017
B932_1590	Phosphoglycerate kinase	pgk		6.42	0.00014
B932_1622	Acetyltransferase domain protein		0.52		0.00805
B932_1626	Acn5 family acetyltransferase		0.6		0.0417
B932_1705	Adenylosuccinate synthetase	purA		0.23	0.00018
B932_2067	Carbamoyl phosphate synthase small subunit		1.7		0.01385
B932_2122	ATP-dependent protease peptidase subunit		2.13		0.00015
B932_2143	Dimethylallyltransferase	ispA		0.27	0.0009
B932_2481	UTP-glucose-1-phosphate uridylyltransferase	galU		0.53	0.00036
B932_2542	Alpha-amino acid ester hydrolase			0.63	0.0083
B932_2586	Lytic transglycosylase		0.52		0.00185
B932_2711	Indole-3-glycerol phosphate synthase	trpC		0.38	0.00038
B932_3232	Methionine aminopeptidase		0.64		0.03705
B932_3480	3-oxoacyl-ACP reductase	fabG		0.38	0.00024

	Oxidation-reduction process
B932_1311	ACP phosphodiesterase	acpD		0.51	0.0049
B932_2072	NAD-dependent alcohol dehydrogenase	adh	2.56		5.0E-05
B932_2071	Alcohol dehydrogenase	adhP	1.5		0.04995
B932_0068	Cytochrome o ubiquinol oxidase subunit I	cyoB	1.68		0.04455
B932_0067	Cytochrome o ubiquinol oxidase subunit III	cyoC	1.61		0.04395
B932_1063	Putative cytochrome c-553		2.14		0.00075
B932_1302	Electron transfer flavoprotein subunit alpha	etfA		17.37	0.0088
B932_1062	NADP-dependent sorbitol dehydrogenase	exaA		0.34	0.0049
B932_0993	Putative NAD-dependent aldehyde dehydrogenase	gabD		1.55	0.00082
B932_1321	Quinoprotein glucose dehydrogenase	gcd		0.12	0.0041
B932_1312	Flavohemoprotein	hmp	0.62		0.02435
B932_1684	L-sorbose reductase	mtlK		0.52	0.00049
B932_2075	NAD(P) transhydrogenase subunit alpha	pntA		1.71	0.0016
B932_1092	dTDP-4-dehydrorhamnose reductase	rfbD		0.45	0.0064
B932_0665	L-sorbosone dehydrogenase, NAD(P) dependent	sld	1.64		0.0207
B932_3025	Large subunit of sorbitol dehydrogenase	sldA	1.99		0.0142
B932_3024	Small subunit of sorbitol dehydrogenase	sldB	1.69	2.35	0.0223
B932_0875	NAD-dependent xylitol dehydrogenase	xdh	1.8		0.04175
B932_1308	Xylitol dehydrogenase	xdh	1.66	2.09	0.0147
B932_0372	Bacterioferritin comigratory protein		0.48		0.00345
B932_1338	Putative antibiotic biosynthesis monooxygenase			0.59	0.00031
B932_1552	Oxidoreductase			0.26	0.004
B932_2352	Putative Zn-dependent oxidoreductase		1.97		0.0084

	Transport
B932_0284	Outer membrane protein	ompA		1.42	0.0094
B932_0205	Iron complex outermembrane receptor protein		1.77		0.00805
B932_0274	Outer membrane protein		0.63		0.0276
B932_0755	Membrane protein		1.92		0.0366
B932_0768	Ferrous iron transport protein A (FeoA)	feoA	1.7		0.03825
B932_0797	ATP synthase F0F1 subunit beta	atpD		2.13	0.0038
B932_0799	ATP synthase F0F1 subunit alpha	atpA		1.73	0.001
B932_0800	ATP synthase subunit delta	atpH		0.12	0.0057
B932_0804	Protein translocase subunit SecE	secE	1.75		0.008
B932_0839	Energy transducer		1.57		0.0315
B932_0965	GTP-binding protein YchF	ychF		0.32	0.0023
B932_1170	PqqB protein	pqqB	16.85	4.4	5.0E-05
B932_1188	Outer membrane protein OmpW	ompW		1.8	0.0014
B932_1815	Nickel ABC transporter substrate-binding protein	cbiK	0.49		0.0172
B932_1930	Transporter		2.01		0.0087
B932_1932	Molybdenum-pterin-binding protein	mop	2.13		0.0252
B932_1943	Outer membrane protein		0.44		0.00075
B932_1944	Outer membrane protein		0.62		0.04455
B932_2186	ABC transporter permease		2.12		0.0452
B932_2253	Sodium/proton antiporter nhaA	nhaA	0.48		0.00055
B932_2423	ABC transporter ATP-binding protein	sufC		0.42	0.011
B932_2846	Periplasmic sorbitol binding protein		1.6		0.02695
B932_3091	Outer membrane protein		0.62		0.02435
B932_3210	D-methionine ABC transporter permease metI	metI	0.57		0.02105

	Translation and refolding
B932_1993	50S ribosomal protein L7/L12	rplL		1.64	0.0063
B932_2022	50S ribosomal protein L15	rplO		0.32	0.00011
B932_0245	50S ribosomal protein L34P	rpmH	1.58		0.03065
B932_0636	30S ribosomal protein S1	rpsA		0.58	0.0027
B932_2447	30S ribosomal protein S2	rpsB		4.35	0.00097
B932_2020	30S ribosomal protein S5	rpsE		0.34	0.00074
B932_2007	30S ribosomal protein S19	rpsS	1.53		0.04425
B932_2397	RpsU	rpsU	1.71		0.02405
B932_1721	ATP-dependent Clp protease, ATP-binding subunit ClpB	clpB		0.48	0.00041
B932_2435	ATP-dependent Clp protease proteolytic subunit	clpP		1.51	0.0059
B932_0649	ATP-dependent Clp protease adaptor protein ClpS	clpS	1.83		0.00615
B932_2158	Elongation factor P	efp		2.45	0.0081
B932_2415	Elongation factor G	efg		2.44	0.002
B932_0080	Molecular chaperone GroES	groES	1.88		0.0028
B932_0079	Molecular chaperone GroEL	groEL	1.77	1.76	0.0198
B932_1318	Molecular chaperone DnaK	dnaK		0.26	0.0072
B932_2574	Molecular chaperone IbpA	ibpA	1.56		0.03285
B932_2000	Elongation factor Tu	tufM		36.59	0.035
B932_2466	Transcriptional regulator cold shock protein	cspA		1.75	0.00022
B932_1358	Translation initiation factor IF-3	infC		8.86	0.00035
B932_2183	Translation repressor		0.58		0.0328
B932_2222	Translation repressor		2.24		0.0033

	Transcription and signal transduction
B932_0462	Transcription termination factor NusA	nusA		0.59	0.045
B932_1032	MarR family transcriptional regulator		0.64		0.03695
B932_1731	Plasmid maintenance system antidote protein, XRE family		1.79		0.02025
B932_1810	RNA polymerase sigma factor, sigma-70 family protein		3.16		0.00945
B932_1389	Serine protease			2.43	0.0001
B932_2351	Transcriptional regulator		2.14		0.0038
B932_3161	Transposase		1.63		0.0276
B932_3162	Transposase		1.65		0.01615
B932_0672	Transposase		1.66		0.03855
B932_1744	Transposase		1.72		0.0093

	Response to stress
B932_3533	Osmotically inducible protein OsmC	osmC		0.42	0.00044
B932_0307	Linocin M18 bacteriocin protein			3.75	0.00025
B932_0530	Damage-inducible protein		0.53		0.00425
B932_2602	Damage-inducible protein		0.52		0.00315

	Motility
B932_0422	Selw selh selenoprotein		1.67		0.01395
B932_1211	Flagellar basal body rod protein FlgG	flgG		5.19	0.0064
B932_1143	Flagellar hook-associated protein 1 FlgK	flgK		2.75	0.00055
B932_0694	Bacteriophage tail fiber partial		2.21		0.0266

	Unfiled
B932_3010	Dinucleotide-binding enzyme			2.36	0.0018
B932_1634	Ribonuclease h		0.41		5.0E-05
B932_2418	Carboxypeptidase-like protein			0.58	0.0017
B932_0630	Zinc protease	pqqL		0.45	0.0072
B932_0472?	Tricorn protease-like protein	tri		0.46	0.0019
B932_2220	Single peptide protein		0.51		0.00385
B932_3007	Peptidase partial		0.55		0.0135
B932_1771	Helix-turn-helix domain-containing protein		1.92		0.0254

	Hypothetical protein
B932_0014	Hypothetical protein		2.68		0.0234
B932_0185	Hypothetical protein		0.56		0.0202
B932_0029	Hypothetical protein		0.49	0.3	0.0016
B932_0084	Hypothetical protein		0.48		0.0014
B932_0099	Hypothetical protein		0.48		0.0014
B932_0166	Hypothetical protein		1.7		0.0008
B932_0190	Hypothetical protein		0.57		0.001
B932_0208	Hypothetical protein		0.3		0.018
B932_0373	Hypothetical protein		0.49		0.000095
B932_0463	Hypothetical protein			0.16	0.00016
B932_0542	Hypothetical protein		0.64		0.03
B932_0554	Hypothetical protein		0.45		0.00015
B932_0678	Hypothetical protein		0.6		0.01465
B932_0679	Hypothetical protein		0.57		0.0089
B932_0685	Hypothetical protein		0.58		0.008
B932_0801	Hypothetical protein		0.53		0.00265
B932_0834	Hypothetical protein			0.55	0.0283
B932_1053	Hypothetical protein			0.64	0.04095
B932_1053	Hypothetical protein		0.57		0.0094
B932_1056	Hypothetical protein		0.6		0.01595
B932_1139	Hypothetical protein		1.53		0.0496
B932_1216	Hypothetical protein			1.92	0.02
B932_1288	Hypothetical protein		1.64		0.02015
B932_1712	Hypothetical protein			3.1	0.0152
B932_2348	Hypothetical protein		1.77		0.0118
B932_2350	Hypothetical protein		2.36		5.0E-05
B932_2362	Hypothetical protein		3.31		0.0113
B932_2483	Hypothetical protein		2.38		0.03095
B932_2563	Hypothetical protein		2.15		0.0045
B932_2935	Hypothetical protein		2.78		0.0119
B932_3243	Hypothetical protein		1.56		0.034
B932_3344	Hypothetical protein		2.67		0.01475
B932_3475	Hypothetical protein		5.18		0.0384
B932_3482	Hypothetical protein		1.52		0.0438

Tab.1 Table A The biological process categories of DEGs and DEPs

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