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Stress responses of Acinetobacter strain Y during phenol degradation

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Abstract

Quantification of gene expression of Acinetobacter strain Y under 1000 mg/l of phenol was investigated using qPCR and proteomic analyses. The results show that Acinetobacter strain Y utilized 100 % of phenol within 18 h of exposure. The results of qPCR and proteomic analyses demonstrate a sequential expression of phenol-degrading genes of Acinetobacter strain Y via the ortho-pathway followed by the β-ketoadipate pathway. Many stress-responsive proteins such as chaperones, chaperonins, porins and the enzymes involved in the signal transduction pathway were upregulated especially in the early stage. The stressed bacteria produced more ABC-type transporters, membrane receptors and efflux pumps to mitigate the impacts of phenol stress. The functions of TCA/glyoxylate cycle and oxidative phosphorylation processes were negatively affected. Many enzymes in the gluconeogenesis pathway were upregulated. This study demonstrates bacterial strategies of Acinetobacter strain Y via the energy saving mechanisms and the coordinated control between carbon (C)- and nitrogen (N)-limitations in coping with the stress by scavenging the reactive oxygen species.

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References

  • American Public Health Association (APHA) (1998) Standard methods for the examination of water and wastewater. 20th edn, In: Greenberg AE, Clesceri LS, Eaton AS (eds) American Public Health Association, American Water Works Association (AWWA), Water Environment Federation (WEF)

  • Andersen JL, He G-X, Kakarla P et al (2015) Multidrug efflux pumps from Enterobacteriaceae, Vibrio cholera and Staphylococcus aureus Bacterial Food Pathogens. Int J Environ Res Public Health 12:1487–1547. doi:10.3390/ijerph120201487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold T, Zeth K, Linke D (2009) Structure and function of colicin S4, a colicin with a duplicated receptor-binding domain. J Biol Chem 284:6403–6413. doi:10.1074/jbc.M808504200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardwell JC, Craig EA (1988) Ancient heat shock gene is dispensable. J Bacteriol 170:2977–2983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benndorf D, Loffhagen N, Babel W (2001) Protein synthesis patterns in Acinetobacter calcoaceticus induced by phenol and catechol show specificities of responses to chemostress. FEMS Microbiol Lett 200:247–252

    Article  CAS  PubMed  Google Scholar 

  • Bleichrodt FS, Fischer R, Gerischer UC (2010) The beta-ketoadipate pathway of Acinetobacter baylyi undergoes carbon catabolite repression, cross-regulation and vertical regulation, and is affected by Crc. Microbiology 156:1313–1322. doi:10.1099/mic.0.037424-0

    Article  CAS  PubMed  Google Scholar 

  • Brigelius-Flohé R, Flohé L (2011) Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 15:2335–2381

    Article  PubMed  PubMed Central  Google Scholar 

  • Britton RA (2009) Role of GTPases in bacterial ribosome assembly. Ann Rev Microbiol 63:155–176

    Article  CAS  Google Scholar 

  • Burmann BM, Schweimer K, Luo X, Wahl MC, Stitt BL, Gottesman ME, Rösch P (2010) A NusE:NusG complex links transcription and translation. Science 328:501–504. doi:10.1126/science.1184953

    Article  CAS  PubMed  Google Scholar 

  • Cipollone R, Ascenzi P, Frangipani E, Visca P (2006) Cyanide detoxification by recombinant bacterial rhodanese. Chemosphere 63:942–949

    Article  CAS  PubMed  Google Scholar 

  • Cipollone R, Ascenzi P, Tomao P, Imperi F, Visca P (2008) Enzymatic detoxification of cyanide: clues from Pseudomonas aeruginosa Rhodanese. J Mol Microbiol Biotechnol 15:199–211. doi:10.1159/000121331

    Article  CAS  PubMed  Google Scholar 

  • Cornelissen CN, Hollander A (2011) TonB-dependent transporters expressed by Neisseria gonorrhoeae. Front Microbiol 27:117. doi:10.3389/fmicb.2011.00117

    Google Scholar 

  • Craven SH, Ezezika OC, Momany C, Neidle EL (2008) LysR homologs in Acinetobacter: insights into a diverse and prevalent family of transcriptional regulators. In: Gerischer UC (ed) Acinetobacter Molecular Biology, 1st edn. Caister Academic Press, Norwich, pp 163–202

    Google Scholar 

  • Delhaye A, Collet A-F, Laloux G (2016) Fine-tuning of the Cpx envelope stress response is required for cell wall homeostasis in Escherichia coli. mBio 7(1):e00047-16

    PubMed  PubMed Central  Google Scholar 

  • Donovan GT, Norton JP, Bower JM, Mulvey MA (2013) Adenylate cyclase and the cyclic AMP receptor protein modulate stress resistance and virulence capacity of uropathogenic Escherichia coli. Infect Immun 81:249–258. doi:10.1128/IAI.00796-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernando DM, Kumar A (2013) Resistance-nodulation-division multidrug efflux pumps in gram-negative bacteria: role in virulence. Antibiotics 2:163–181. doi:10.3390/antibiotics2010163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fontenelle C, Blanco C, Arrieta M, Dufour V, Trautwetter A (2011) Resistance to organic hydroperoxides requires ohr and ohrR genes in Sinorhizobium meliloti. BMC Microbiol 11:100. doi:10.1186/1471-2180-11-100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng A, Lim CJ (2007) Proteome analysis of the adaptation of a phenol-degrading bacterium Acinetobacter sp. EDP3 to the variation of phenol loadings. Chin J Chem Eng 15(6):781–787

    Article  CAS  Google Scholar 

  • Giel JL, Nesbit AD, Mettert EL, Fleischhacker AS, Wanta BT, Kiley PJ (2013) Regulation of iron–sulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fe–2S]–IscR in Escherichia coli. Mol Microbiol 87:478–492

    Article  CAS  PubMed  Google Scholar 

  • Giuffrida MG, Pessione E, Mazzoli R, Dellavalle G, Barello C, Conti A, Giunta C (2001) Media containing aromatic compounds induce peculiar proteins in Acinetobacter radioresistens as revealed by proteome analysis. Electrophoresis 22:1705–1711

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Flecha B, Demple B (1995) Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270:13681–13687

    Article  CAS  PubMed  Google Scholar 

  • Grass G, Rensing C (2001) Genes involved in copper homeostasis in Escherichia coli. J Bacteriol 183:2145–2147. doi:10.1128/JB.183.6.2145-2147.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graumann J, Lilie H, Tang X, Tucker KA et al (2001) Activation of the redox-regulated molecular chaperone Hsp33—a two-step mechanism. Structure 9:377–387

    Article  CAS  PubMed  Google Scholar 

  • Haas CE, Rodionov DA, Kropat J, Malasarn D, Merchant SS, de Crécy-Lagard V (2009) A subset of the diverse COG0523 family of putative metal chaperones is linked to zinc homeostasis in all kingdoms of life. BMC Genom 10:470. doi:10.1186/1471-2164-10-470

    Article  Google Scholar 

  • Hantke K (1990) Dihydroxybenzoylserine—a siderophore for E. coli. FEMS Microbiol Lett 55:5–8

    CAS  PubMed  Google Scholar 

  • Heeb S, Valverde C, Gigot-Bonnefoy C, Haas D (2005) Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 243:251–258

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann A, Bukau B, Kramer G (2010) Structure and function of the molecular chaperone trigger factor. Biochimica et Biophysica Acta (BBA)—MolCell Res 1803:650–661

    Article  CAS  Google Scholar 

  • Hunter GJ, Hunter T (2013) GroESL protects superoxide dismutase (SOD)—deficient cells against oxidative stress and is a chaperone for SOD. Health 5:1719–1729. doi:10.4236/health.2013.510232 (Article ID: 38248)

    Article  CAS  Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418

    Article  CAS  PubMed  Google Scholar 

  • Kim E-A, Kim JY, Kim S-J, Park KR, Chung H-J, Leem S-H, Kim SI (2004) Proteomic analysis of Acinetobacter lwoffii K24 by 2-D gel electrophoresis and electrospray ionization quadrupole-time of flight mass spectrometry. J Microbiol Methods 57:337–349

    Article  CAS  PubMed  Google Scholar 

  • Kim C-M, Kim S-J, Shin S-H (2012) Cyclic AMP-receptor protein activates aerobactin receptor IutA expression in Vibrio vulnificus. J Microbiol 50:320–325. doi:10.1007/s12275-012-2056-y

    Article  CAS  PubMed  Google Scholar 

  • Kwon K-H, Yeom SH (2009) Optimal microbial adaptation routes for the rapid degradation of high concentration of phenol. Bioprocess Biosyst Eng 32(4):435–442

    Article  CAS  PubMed  Google Scholar 

  • Leblanc SK, Oates CW, Raivio TL (2011) Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. J Bacteriol 193:3367–3375. doi:10.1128/JB.01534-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin J, Sharma V, Milase R, Mbhense N (2015) Simultaneous enhancement of phenolic compound degradations by Acinetobacter strain V2 via a step-wise continuous acclimation process. J Basic Microbiol. doi:10.1002/jobm.201500263

    Google Scholar 

  • Llamas MA, Sparrius M, Kloet R, Jiménez CR, Vandenbroucke-Grauls C, Bitter W (2006) The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 188:1882–1891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loftus SR, Walker D, Maté MJ, Bonsor DA, James R, Moore GR, Kleanthous C (2006) Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. PNAS USA 103:12353–12358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo X, Hsiao HH, Bubunenko M, Weber G, Court DL, Gottesman ME, Urlaub H, Wahl MC (2008) Structural and functional analysis of the E. coli NusB-S10 transcription antitermination complex. Mol Cell 32:791–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magalhaes AC, Dunn H, Ferguson SSG (2012) Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. Br J Pharmacol 165:1717–1736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier T, Ferbitz L, Deuerling E, Ban N (2005) A cradle for new proteins: trigger factor at the ribosome. Curr Opin Struct Biol 15:204–212

    Article  CAS  PubMed  Google Scholar 

  • Matern Y, Barion B, Behrens-Kneip S (2010) PpiD is a player in the network of periplasmic chaperones in Escherichia coli. BMC Microbiol 10:251. doi:10.1186/1471-2180-10-251

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsuoka Y, Shimizu K (2015) Current status and future perspectives of kinetic modeling for the cell metabolism with incorporation of the metabolic regulation mechanism. Bioresour Bioprocess 2:4

    Article  Google Scholar 

  • Mazzoli R, Fattori P, Lamberti C, Giuffrida MG, Zapponi M, Giunta C, Pessione E (2011) High isoelectric point sub-proteome analysis of Acinetobacter radioresistens S13 reveals envelope stress responses induced by aromatic compounds. Mol BioSyst 7:598–607

    Article  CAS  PubMed  Google Scholar 

  • Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367

    Article  CAS  PubMed  Google Scholar 

  • Missiakas D, Raina S (1998) The extracytoplasmic function sigma factors: role and regulation. Mol Microbiol 28:1059–1066

    Article  CAS  PubMed  Google Scholar 

  • Mooney RA, Schweimer K, Rösch P, Gottesman M, Landick R (2009) Two Structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J Mol Biol 391:341–358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mujacic M, Bader MW, Baneyx F (2004) Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK–DnaJ–GrpE system in the management of protein misfolding under severe stress conditions. Mol Microbiol 51:849–859

    Article  CAS  PubMed  Google Scholar 

  • Murakami K, Fuse H, Takimura O, Inoue H, Yamaoka Y (2000) Cloning and characterization of the iutA gene which encodes ferric aerobactin receptor from marine Vibrio species. Microbios 101:137–146

    CAS  PubMed  Google Scholar 

  • Nakamoto H, Fujita K, Ohtaki A et al (2014) Physical interaction between bacterial heat shock protein 90 (Hsp90) and Hsp70 chaperones mediates their cooperative action to refold denatured proteins. JBC 289:6110–6119. doi:10.1074/jbc.M113.524801

    Article  CAS  Google Scholar 

  • Nešvera J, Rucká L, Pátek M (2015) Catabolism of phenol and its derivatives in bacteria: genes, their regulation, and use in the biodegradation of toxic pollutants. Adv Appl Microbiol 93:107–160. doi:10.1016/bs.aambs.2015.06.002

    Article  PubMed  Google Scholar 

  • Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1:1559–1582

    Article  CAS  PubMed  Google Scholar 

  • Ong CL, Ulett GC, Mabbett AN et al (2008) Identification of type 3 fimbriae in uropathogenic Escherichia coli reveals a role in biofilm formation. J Bacteriol 190:1054–1063

    Article  CAS  PubMed  Google Scholar 

  • Pawlik M-C, Hubert K, Joseph B, Claus H, Schoen C, Vogel U (2012) The zinc-responsive regulon of Neisseria meningitidis comprises 17 genes under control of a Zur element. J Bacteriol 194:6594–6603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez A, Poza M, Fernández A et al (2012) Involvement of the AcrAB-TolC efflux pump in the resistance, fitness, and virulence of Enterobacter cloacae. Antimicrob Agents Chemother 56:2084–2090

    Article  PubMed  PubMed Central  Google Scholar 

  • Pessione E, Divari S, Griva E, Cavaletto M, Rossi GL, Gilardi G, Giunta C (1999) Phenol hydroxylase from Acinetobacter radioresistens is a multicomponent enzyme. Purification and characterization of the reductase moiety. Eur J Biochem 265:549–555

    Article  CAS  PubMed  Google Scholar 

  • Putrinš M, Tover A, Tegova R, Saks Ü, Kivisaar M (2007) Study of factors which negatively affect expression of the phenol degradation operon pheBA in Pseudomonas putida. Microbiology 153:1860–1871

    Article  PubMed  Google Scholar 

  • Reeves SA, Parsonage D, Nelson KJ, Poole LB (2011) Kinetic and thermodynamic features reveal that Escherichia coli BCP is an unusually versatile peroxiredoxin. Biochemistry 50:8970–8981. doi:10.1021/bi200935d

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruangprasert A, Craven SH, Neidle EL, Momany C (2010) Full-length structures of BenM and two variants reveal different oligomerization schemes for LysR-type transcriptional regulators. J Mol Biol 404(4):568–586

    Article  CAS  PubMed  Google Scholar 

  • Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4:57–66

    Article  PubMed  Google Scholar 

  • Santos PM, Benndorf D, Sá-Correia I (2004) Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics. Proteomics 4(9):2640–2652

    Article  CAS  PubMed  Google Scholar 

  • Scott JM, Ju J, Mitchell T, Haldenwang WG (2000) The Bacillus subtilis GTP binding protein Obg and regulators of the ςB stress response transcription factor cofractionate with ribosomes. J Bacteriol 182:2771–2777. doi:10.1128/JB.182.10.2771-2777.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segura A, Ramos JL (2014) Toluene tolerance systems in Pseudomonas. In: Nojiri H, Tsuda M, Fukuda M, Kamagata Y (eds) Biodegradative Bacteria, vol 10. Springer, Japan, pp 227–248. doi:10.1007/978-4-431-54520-0_11

    Chapter  Google Scholar 

  • Shimizu K (2014) Regulation systems of bacteria such as E. coli in response to nutrient limitation and environmanental stresses. Metabolites 4:1–35

    Article  Google Scholar 

  • Versteeg S, Mogk A, Schumann W (1999) The Bacillus subtilis htpG gene is not involved in thermal stress management. Mol Gen Genet 261:582–588

    Article  CAS  PubMed  Google Scholar 

  • Vidakovics MLP, Paba J, Lamberti Y, Ricart CA, Valle de Sousa M, Rodriguez ME (2007) Profiling the Bordetella pertussis proteome during iron starvation. J Proteome Res 6:2518–2528. doi:10.1021/pr060681i

    Article  PubMed  Google Scholar 

  • Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177–1190

    Article  CAS  PubMed  Google Scholar 

  • Vita J, Marti S, Sanchez-Cespedes J (2007) Porins, efflux pumps and multidrug resistance in Acinetobacter baumannii. J Antimicrob Chemother 59:1210–1215

    Article  Google Scholar 

  • Warnecke T (2012) Loss of the DnaK-DnaJ-GrpE chaperone system among the Aquificales. Mol Biol Evol 29:3485–3495. doi:10.1093/molbev/mss152

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Peng Z, Zhan Y, Wang J, Yan Y, Chen M, Lu MW, Ping S, Zhang W, Zhao Z, Li S, Takeo M, Lin M (2011) Novel regulator MphX represses activation of phenol hydroxylase genes caused by a XylR/DmpRType regulator MphR in Acinetobacter calcoaceticus. PLoS ONE 6:e17350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan Y, Yu H, Yan Y, Ping S, Lu W, Zhang W, Chen M, Lin M (2009) Benzoate catabolite repression of the phenol degradation in Acinetobacter calcoaceticus PHEA-2. Curr Microbiol 59:368–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan Y, Yan Y, Zhang W, Chen M, Lu W, Ping S, Lin M (2012) Comparative analysis of the complete genome of an Acinetobacter calcoaceticus strain adapted to a phenol-polluted environment. Res Microbiol 163(1):36–43

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Wang Y, Lee OO, Tian R et al (2013) Adaptation of intertidal biofilm communities is driven by metal ion and oxidative stresses. Sci Rep 3:3180. doi:10.1038/srep03180

    PubMed  PubMed Central  Google Scholar 

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  1. Discipline of Microbiology, School of Life Sciences, University of KwaZulu-Natal (Westville), Private Bag X54001, Durban, South Africa

    Johnson Lin

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Communicated by Jorge Membrillo-Hernández.

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Lin, J. Stress responses of Acinetobacter strain Y during phenol degradation. Arch Microbiol 199, 365–375 (2017). https://doi.org/10.1007/s00203-016-1310-9

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