Skip to main content

Advertisement

Log in

Comparative proteomics reveal the impact of OmcA/MtrC deletion on Shewanella oneidensis MR-1 in response to hexavalent chromium exposure

  • Genomics, transcriptomics, proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Hexavalent chromium [Cr(VI)] is a priority pollutant causing serious environmental issues. Microbial reduction provides an alternative strategy for Cr(VI) remediation. The dissimilatory metal-reducing bacterium, Shewanella oneidensis MR-1, was employed to study Cr(VI) reduction and toxicity in this work. To understand the effect of membrane cytochromes on Cr(VI) response, a comparative protein profile analysis from S. oneidensis MR-1 wild type and its mutant of deleting OmcA and MtrC (△omcA/mtrC) was conducted using two-dimensional electrophoresis (2-DE) technology. The 2-DE patterns were compared, and the proteins with abundant changes of up to twofold in the Cr(VI) treatment were detected. Using mass spectrometry, 38 and 45 differentially abundant proteins were identified in the wild type and the mutant, respectively. Among them, 25 proteins were shared by the two strains. The biological functions of these identified proteins were analyzed. Results showed that Cr(VI) exposure decreased the abundance of proteins involved in transcription, translation, pyruvate metabolism, energy production, and function of cellular membrane in both strains. There were also significant differences in protein expressions between the two strains under Cr(VI) treatment. Our results suggest that OmcA/MtrC deletion might result in the Cr(VI) toxicity to outer membrane and decrease assimilation of lactate, vitamin B12, and cystine. When carbohydrate metabolism was inhibited by Cr(VI), leucine and sulfur metabolism may act as the important compensatory mechanisms in the mutant. Furthermore, the mutant may regulate electron transfer in the inner membrane and periplasm to compensate for the deletion of OmcA and MtrC in Cr(VI) reduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alekshun MN, Levy SB (1997) Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob Agents Chemother 41:2067–2075

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aubert S, Alban C, Bligny R, Douce R (1996) Induction of β-methylcrotonyl-coenzyme A carboxylase in higher plant cells during carbohydrate starvation: evidence for a role of MCCase in leucine catabolism. FEBS Lett 383:175–180

    Article  CAS  PubMed  Google Scholar 

  • Barabote RD, Saier MH Jr (2005) Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69:608–634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Belchik SM, Kennedy DW, Dohnalkova AC, Wang YM, Sevinc PC, Wu H, Lin YH, Lu HP, Fredrickson JK, Shi L (2011) Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77:4035–4041

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bencheikh-Latmani R, Williams SM, Haucke L, Criddle CS, Wu LY, Zhou JZ, Tebo BM (2005) Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) and U(VI) reduction. Appl Environ Microbiol 71:7453–7460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Binder S, Knill T, Schuster J (2007) Branched-chain amino acid metabolism in higher plants. Physiol Plant 129:68–78

    Article  CAS  Google Scholar 

  • Bjellqvist B, Ek K, Righetti PG, Gianazza E, Gorg A, Westermeier R, Postel W (1982) Isoelectric focusing in immobilized pH gradients: principle, methodology and some applications. J Biochem Biophys Methods 6:317–339

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brown SD, Thompson MR, VerBerkmoes NC, Chourey K, Shah M, Zhou JZ, Hettich RL, Thompson DK (2006) Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol Cell Proteomics 5:1054–1071

    Article  CAS  PubMed  Google Scholar 

  • Bulut H, Moniot S, Licht A, Scheffel F, Gathmann S, Saenger W, Schneider E (2012) Crystal structures of two solute receptors for L-cystine and L-cysteine, respectively, of the human pathogen Neisseria gonorrhoeae. J Mol Biol 415:560–572

    Article  CAS  PubMed  Google Scholar 

  • Cantoni O, Brandi G, Albano A, Cattabeni F (1995) Action of cystine in the cytotoxic response of Escherichia coli cells exposed to hydrogen peroxide. Free Radic Res 22:275–283

    Article  CAS  PubMed  Google Scholar 

  • Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics 5:2497–2507

    Article  CAS  PubMed  Google Scholar 

  • Chourey K, Thompson MR, Morrell-Falvey J, VerBerkmoes NC, Brown SD, Shah M, Zhou JZ, Doktycz M, Hettich RL, Thompson DK (2006) Global molecular and morphological effects of 24-hour chromium(VI) exposure on Shewanella oneidensis MR-1. Appl Environ Microbiol 72:6331–6344

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarke TA, Edwards MJ, Gates AJ, Hall A, White GF, Bradley J, Reardon CL, Shi L, Beliaev AS, Marshall MJ, Wang ZM, Watmough NJ, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci U S A 108:9384–9389

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cook AM, Denger K (2002) Dissimilation of the C2 sulfonates. Arch Microbiol 179:1–6

    Article  CAS  PubMed  Google Scholar 

  • Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008

    CAS  Google Scholar 

  • Dhal B, Thatoi HN, Das NN, Pandey BD (2013) Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: a review. J Hazard Mater 250:272–291

    Article  PubMed  Google Scholar 

  • Dong JM, Taylor JS, Latour DJ, Iuchi S, Lin ECC (1993) Three overlapping lct genes involved in L-lactate utilization by Escherichia coli. J Bacteriol 175:6671–6678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fischer E, Gunter K, Braun V (1989) Involvement of ExbB and TonB in transport across the outer membrane of Escherichia coli: phenotypic complementation of exb mutants by overexpressed tonB and physical stabilization of TonB by ExbB. J Bacteriol 171:5127–5134

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ge SM, Zhou MH, Dong XJ, Lu Y, Ge SC (2013) Distinct and effective biotransformation of hexavalent chromium by a novel isolate under aerobic growth followed by facultative anaerobic incubation. Appl Microbiol Biotechnol 97:2131–2137

    Article  CAS  PubMed  Google Scholar 

  • Gnanamani A, Kavitha V, Radhakrishnan N, Rajakumar GS, Sekaran G, Mandal AB (2010) Microbial products (biosurfactant and extracellular chromate reductase) of marine microorganism are the potential agents reduce the oxidative stress induced by toxic heavy metals. Colloids Surf B 79:334–339

    Article  CAS  Google Scholar 

  • Gonzalez R, Murarka A, Dharmadi Y, Yazdani SS (2008) A new model for the anaerobic fermentation of glycerol in enteric bacteria: trunk and auxiliary pathways in Escherichia coli. Metab Eng 10:234–245

    Article  CAS  PubMed  Google Scholar 

  • Hayashi M, Nakayama Y, Unemoto T (2001) Recent progress in the Na+-translocating NADH-quinone reductase from the marine Vibrio alginolyticus. BBA-Bioenergetics 1505:37–44

    Article  CAS  PubMed  Google Scholar 

  • Herrmann G, Jayamani E, Mai G, Buckel W (2008) Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190:784–791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horcajo P, de Pedro MA, Cava F (2012) Peptidoglycan plasticity in bacteria: stress-induced peptidoglycan editing by noncanonical D-amino acids. Microb Drug Resist 18:306–313

    Article  CAS  PubMed  Google Scholar 

  • Imanaka H, Yamatsu A, Fukui T, Atomi H, Imanaka T (2006) Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis. Mol Microbiol 61:898–909

    Article  CAS  PubMed  Google Scholar 

  • Leonhartsberger S, Korsa I, Bock A (2002) The molecular biology of formate metabolism in enterobacteria. J Mol Microbiol Biotechnol 4:269–276

    CAS  PubMed  Google Scholar 

  • Liu HW, Thorson JS (1994) Pathways and mechanisms in the biogenesis of novel deoxysugars by bacteria. Annu Rev Microbiol 48:223–256

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lovering AL, de Castro LH, Lim D, Strynadka NCJ (2007) Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis. Science 315:1402–1405

    Article  CAS  PubMed  Google Scholar 

  • Martin RG, Rosner JL (2001) The AraC transcriptional activators. Curr Opin Microbiol 4:132–137

    Article  CAS  PubMed  Google Scholar 

  • McCoy AJ, Maurelli AT (2006) Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends Microbiol 14:70–77

    Article  CAS  PubMed  Google Scholar 

  • Narayani M, Shetty KV (2013) Chromium-resistant bacteria and their environmental condition for hexavalent chromium removal: a review. Crit Rev Environ Sci Technol 43:955–1009

    Article  CAS  Google Scholar 

  • Neumann M, Mittelstädt G, Iobbi-Nivol C, Saggu M, Lendzian F, Hildebrandt P, Leimkühler S (2009) A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli. FEBS J 276:2762–2774

    Article  CAS  PubMed  Google Scholar 

  • Nikaido H (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382–388

    Article  CAS  PubMed  Google Scholar 

  • Postle K, Larsen RA (2007) TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20:453–465

    Article  CAS  PubMed  Google Scholar 

  • Ram S, Vajpayee P, Shanker R (2008) Rapid culture-independent quantitative detection of enterotoxigenic Escherichia coli in surface waters by real-time PCR with molecular beacon. Environ Sci Technol 42:4577–4582

    Article  CAS  PubMed  Google Scholar 

  • Rawls KS, Martin JH, Maupin-Furlow JA (2011) Activity and transcriptional regulation of bacterial protein-like glycerol-3-phosphate dehydrogenase of the haloarchaea in Haloferax volcanii. J Bacteriol 193:4469–4476

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Robinson C, Matos CFRO, Beck D, Ren C, Lawrence J, Vasisht N, Mendel S (2011) Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. BBA-Biomembranes 1808:876–884

    Article  CAS  PubMed  Google Scholar 

  • Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278:41148–41159

    Article  CAS  PubMed  Google Scholar 

  • Rouviere PE, Gross CA (1996) SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Gene Dev 10:3170–3182

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM, Fredrickson JK (2012) Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1. Front Microbiol 3:50

    PubMed Central  PubMed  Google Scholar 

  • Thompson MR, VerBerkmoes NC, Chourey K, Shah M, Thompson DK, Hettich RL (2007) Dosage-dependent proteome response of Shewanella oneidensis MR-1 to acute chromate challenge. J Proteome Res 6:1745–1757

    Article  CAS  PubMed  Google Scholar 

  • Thompson DK, Chourey K, Wickham GS, Thieman SB, VerBerkmoes NC, Zhang B, McCarthy AT, Rudisill MA, Shah M, Hettich RL (2010) Proteomics reveals a core molecular response of Pseudomonas putida F1 to acute chromate challenge. BMC Genomics 11:311

    Article  PubMed Central  PubMed  Google Scholar 

  • Urone PF (1955) Stability of colorimetric reagent for chromium, s-diphenylcarbazide, in various solvents. Anal Chem 27:1354–1355

    Article  CAS  Google Scholar 

  • Wang YT, Shen H (1995) Bacterial reduction of hexavalent chromium. J Ind Microbiol 14:159–163

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Xu MY, Sun GP (2010) Comparative analysis of membranous proteomics of Shewanella decolorationis S12 grown with azo compound or Fe(III) citrate as sole terminal electron acceptor. Appl Microbiol Biotechnol 86:1513–1523

    Article  CAS  PubMed  Google Scholar 

  • Wang CY, Shen RF, Wang C, Wang W (2013a) Root protein profile changes induced by Al exposure in two rice cultivars differing in Al tolerance. J Proteome 78:281–293

    Article  CAS  Google Scholar 

  • Wang YM, Sevinc PC, Belchik SM, Fredrickson J, Shi L, Lu HP (2013b) Single-cell imaging and spectroscopic analyses of Cr(VI) reduction on the surface of bacterial cells. Langmuir 29:950–956

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu R, Cui L, Chen L, Wang C, Cao C, Sheng G, Yu H, Zhao F (2013) Effects of bio-Au nanoparticles on electrochemical activity of Shewanella oneidensis wild type and △omcA/mtrC Mutant. Sci Rep 3:3307

    PubMed Central  PubMed  Google Scholar 

  • Yang XF, Kang CM, Brody MS, Price CW (1996) Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Gene Dev 10:2265–2275

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported financially by the National Natural Science Foundation of China (21322703, 21177122), China Postdoctoral Science Foundations (2012M520411), and Science and Technology Innovation and Collaboration Team Project of the Chinese Academy of Sciences.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Feng Zhao.

Additional information

Chao Wang and Juan Chen contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 491 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Chen, J., Hu, WJ. et al. Comparative proteomics reveal the impact of OmcA/MtrC deletion on Shewanella oneidensis MR-1 in response to hexavalent chromium exposure. Appl Microbiol Biotechnol 98, 9735–9747 (2014). https://doi.org/10.1007/s00253-014-6143-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6143-3

Keywords

Navigation