Skip to main content
SpringerLink
Log in

Temperature-induced changes in the proteome of Pseudomonas aeruginosa during petroleum hydrocarbon degradation

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Petroleum hydrocarbon contaminants, which are among the most serious pollutants in the petroleum industry, can be degraded sufficiently by Pseudomonas aeruginosa. However, temperature-induced stress will severely inhibit this biodegradation. In this study, the proteome of P. aeruginosa P6 at 25 °C, 43 °C and 37 °C was used to examine the impact of temperature on the molecular mechanism of biodegradation of petroleum hydrocarbon by P. aeruginosa P6. Differentially expressed proteins were identified by iTRAQ technology, and the functions of these proteins were identified by bioinformatic analysis. The impact of 25 °C and 43 °C on cellular processes has also been discussed. The results showed that the expression of proteins in chemotaxis toward petroleum hydrocarbons, terminal oxidation of aromatic rings in petroleum hydrocarbons and trans-membrane transport of fatty acids and nutriments were clearly inhibited under 25 °C condition. The expression of proteins in chemotaxis, emulsification, adhesion and terminal oxidation of petroleum hydrocarbons; catalysis of fatty alcohols and fatty aldehydes; trans-membrane transport of nutriments and β-oxidation were clearly inhibited under 43 °C condition.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Altermann E, Klaenhammer TR (2005) Pathway Voyager: pathway mapping using the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. BMC Genomics 6(1):60

    Article  PubMed  PubMed Central  Google Scholar 

  • Consortium UP (2015) UniProt: a hub for protein information. Nucleic Acids Res 43 (Database issue):204–212

  • Chang W, Klemm S, Beaulieu C, Hawari J, Whyte L, Ghoshal S (2011) Petroleum hydrocarbon biodegradation under seasonal freeze−thaw soil temperature regimes in contaminated soils from a sub-arctic site. Environ Sci Technol 45(3):1061–1066

    Article  CAS  PubMed  Google Scholar 

  • Casabona MG, Silverman JM, Sall KM et al (2013) An abc-transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in pseudomonas aeruginosa. Environ Microbiol 15(2):471–486

    Article  CAS  PubMed  Google Scholar 

  • Deeb RA, Alvarez CL (2015) Temperature effects and substrate interactions during the aerobic biotransformation of btex mixtures by toluene-enriched consortia and rhodococcus rhodochrous. Biotechnol Bioeng 62(5):526–536

    Article  Google Scholar 

  • Delille D, Coulon F, Pelletier E (2004) Effects of temperature warming during a bioremediation study of natural and nutrient-amended hydrocarbon-contaminated sub-antarctic soils. Cold Reg Sci Technol 40(1–2):0–70

  • Eriksson M, Ka JO, Mohn WW (2001) Effects of low temperature and freeze-thaw cycles on hydrocarbon biodegradation in arctic tundra soil. Applied Environl Microbiol 67(11):5107–5112

    Article  CAS  Google Scholar 

  • Frédéric C, Pelletier E, Lénaick G et al (2005) Effects of nutrient and temperature on degradation of petroleum hydrocarbons in contaminated sub-antarctic soil. Chemosphere 58(10):0–1448

  • Frédéric C, Mckew BA, Osborn AM et al (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9(1):177–186

    Article  Google Scholar 

  • Franceschini A, Szklarczyk D, Frankild S et al (2012) STRING V9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41(D1)

  • Haastert PJMV, Devreotes PN (2004) Chemotaxis: signalling the way forward. Nat Rev Mol Cell Bio 5(8):626

    Article  Google Scholar 

  • Hui S, Ghergurovich JM, Morscher RJ et al (2017) Glucose feeds the TCA cycle via circulating lactate. Nature 551(7678):115

    Article  PubMed  PubMed Central  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (pahs): a review. J Hazard Mater 169(1–3):1–15

    Article  CAS  PubMed  Google Scholar 

  • Hagelueken G, Schubert WD (2007) Crystal structure of the electron transfer complex rubredoxin-rubredoxin reductase of P. aeruginosa. P Natl Acad Sci USA 104:12276–12281

  • Houten SM, Violante S, Ventura FV et al (2016) The biochemistry and physiology of mitochondrial fatty acid β-oxidation and its genetic disorders. Annu Rev Physiol 78(1):23–44

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Guo L, Xie LQ et al (2014) Proteome profiling of mitotic clonal expansion during 3T3-L1 adipocyte differentiation using iTRAQ-2DLC-MS/MS. J Proteome Res 13:1307–1314

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Sun WB, Liang RB et al (2015) iTRAQ-based quantitative proteomic analysis of Pseudomonas aeruginosa SJTD-1: A global response to n-octadecane induced stress. J Proteomics 123:14–28

    Article  CAS  PubMed  Google Scholar 

  • Kohl M, Wiese S, Warscheid B (2011) Cytoscape: Software for Visualization and Analysis of Biological Networks. Methods Mol Biol 696:291–303

    Article  CAS  PubMed  Google Scholar 

  • Lindstrom JE, Braddock JF (2002) Biodegradation of petroleum hydrocarbons at low temperature in the presence of the dispersant corexit 9500. Mar Pollut Bull 44(8):739–747

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Das KC, Mcclendon RW (2003) The influence of temperature and moisture contents regimes on the aerobic microbial activity of a biosolids composting blend. Bioresource Technol 86(2):131–137

    Article  CAS  Google Scholar 

  • Mi H, Dong Q, Muruganujan A et al (2010) PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 38(Database issue):D204–D210

  • Ma Z, Marsolais F, Bernards MA et al (2016) Glyoxylate cycle and metabolism of organic acids in the scutellum of barley seeds during germination. Plant Sci 248:37–44

    Article  CAS  PubMed  Google Scholar 

  • Margesin R, Schinner F (2001) Bioremediation (natural attenuation and biostimulation) of diesel-oil-contaminated soil in an alpine glacier skiing area. Applied Environ Microbiol 67(7):3127–3133

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2007) Effect of temperature on oil degradation by a psychrotrophic yeast in liquid culture and in soil. FEMS Microbiol Ecol 24(3):243–249

    Article  Google Scholar 

  • Miller RM, Tomaras AP, Barker AP et al (2008) Pseudomonas aeruginosa twitching motility-mediated chemotaxis towards phospholipids and fatty acids: specificity and metabolic requirements. J Bacteriol 190:4038–4049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JD, Li XX, Qu CT (2019) A Global Proteomic Change in Petroleum Hydrocarbon-Degrading Pseudomonas aeruginosa in Response to High and Low Concentrations of Petroleum Hydrocarbons. Curr Microbiol 76(11):1270–1277

    Article  CAS  PubMed  Google Scholar 

  • NíChadhain SM, Norman RS, Pesce KV et al (2006) Microbial dioxygenase gene population shifts during polycyclic aromatic hydrocarbon bio-degradation. Appl Environ Microb 72(6):4078–4087

    Article  Google Scholar 

  • Ohkuma M, Zimmer T, Iida T et al (1998) Isozyme function of n-alkane-inducible cytochromes p450 in candida maltosa revealed by sequential gene disruption. J Biol Chem 273(7):3948–3953

    Article  CAS  PubMed  Google Scholar 

  • Pontes B, Ayala Y, Fonseca AC et al (2013) Membrane elastic properties and cell function. PLoS ONE 8(7):e67708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul D, Dineshkumar N, Nair S (2006) Proteomics of a plant growth-promoting rhizobacterium, Pseudomonas fluorescens MSP-393, subjected to salt shock. World J Microbiol Biotechnol 22:369–374

    Article  CAS  Google Scholar 

  • Posner M, Kiss AJ, Skiba J et al (2012) Functional validation of hydrophobic adaptation to physiological temperature in the small heat shock protein α a-crystallin. PLoS ONE 7(3):e34438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojo F (2010) Enzymes for aerobic degradation of alkanes. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg, 2010:781–797

  • Rojo F (2010) Genetic features and regulation of n-alkane metabolism. In: Timmis K (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, Heidelberg 2010:1141–1154

  • Simmons TJ, Frandsen KEH, Ciano L et al (2017) Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates. Nat Commun 8(1)

  • Smith PK, Krohn RI, Hermanson GT (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 163(1):76–85

    Article  Google Scholar 

  • Ali HR, Ismail DA, El-Gendy NS (2014) The Biotreatment of Oil-Polluted Seawater by Biosurfactant Producer Halotolerant Pseudomonas aeruginosa Asph2. Energ Source Part A 36(13):1429–1436

    Article  CAS  Google Scholar 

  • Shi Z, Wang B, Chihanga T et al (2014) Energy metabolism during anchorage-independence induction by osteopontin-c. PLoS ONE 9(8):e105675

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamber S, Ochs MM, Hancock RE (2006) Role of the novel OprD family of porins in nutrient uptake in Pseudomonas aeruginosa. J Bacteriol 188:45–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres LG, Rojas N, Bautista G et al (2005) Effect of temperature, and surfactant’s hlb and dose over the tph-diesel biodegradation process in aged soils. Process Biochem 40(10):3296–3302

    Article  CAS  Google Scholar 

  • Ulrich AC, Tappenden K, Armstrong J et al (2010) Effect of cold temperature on the rate of natural attenuation of benzene, toluene, ethylbenzene, and the three isomers of xylene (btex). Revue Canadienne De Géotechnique 47(5):516–527

    Article  CAS  Google Scholar 

  • Vaysse PJ, Prat L, Mangenot S et al (2009) Proteomic analysis of marinobacter hydrocarbonoclasticus, sp17 biofilm formation at the alkane-water interface reveals novel proteins and cellular processes involved in hexadecane assimilation. Res Microbiol 160(10):829–837

    Article  CAS  PubMed  Google Scholar 

  • Varjani SJ, Upasani VN (2016) Biodegradation of petroleum hydrocarbons by oleophilic strain of pseudomonas aeruginosa ncim 5514. Bioresource Technol 222:195–201

    Article  CAS  Google Scholar 

  • Wang Z (2010) Identification of outer membrane porin f protein of Yersinia enterocolitica recognized by antithyrotopin receptor antibodies in Graves’ disease and determination of its epitope using mass spectrometry and bioinformatics tools. J Clin Endocr Metab 95:4012

    Article  CAS  PubMed  Google Scholar 

  • Wang JD, Li XX, Qu CT (2017) Exploration of up-regulated key proteins in Pseudomonas aeruginosa for high-efficiency petroleum degradation by proteomic analysis. Curr Microbiol 74(10):1178–1184

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Shao Z (2013) Enzymes and genes involved in aerobic alkane degradation. Front Microbiol 4(4):116

    PubMed  PubMed Central  Google Scholar 

  • Wisniewski JR, Zougman A, Nagaraj N et al (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362

    Article  CAS  PubMed  Google Scholar 

  • Medic A, Ljesevic M, Inui H et al (2020) Efficient biodegradation of petroleum n-alkanes and polycyclic aromatic hydrocarbons by polyextremophilic Pseudomonas aeruginosa san ai with multidegradative capacity. RSC Adv 10(24):14060–14070

    Article  CAS  Google Scholar 

  • Zeng G, Zhang L, Dong H, Chen Y, Zhang J, Zhu Y, Yuan Y, Xie YK, Fang W (2017) Pathway and mechanism of nitrogen transformation during composting: functional enzymes and genes under different concentrations of pvp-agnps. Bioresour Technol 253(3):112–120

    PubMed  Google Scholar 

  • Zhang L, Zhang J, Zeng G, Dong H, Chen Y, Huang C, Zhu Y, Xu R, Cheng Y, Hou K, Cao W, Fang W (2018) Multivariate relationships between microbial communities and environmental variables during co-composting of sewage sludge and agricultural waste in the presence of pvp-agnps. Bioresource Technol 261:10–18

    Article  CAS  Google Scholar 

  • Pikovskii YI, Korotkov LA, Smirnova MA et al (2017) Laboratory analytical methods for the determination of the hydrocarbon status of soils (a review). Eurasian Soil Sci 50(10):1125–1137

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the National Major Science and Technology Projects of China (Program No. 2016ZX05040-003).

Author information

Authors and Affiliations

  1. College of Chemistry and Chemical Engineering, Xi’an Shiyou University, Xi’an, People’s Republic of China

    Jun-Di Wang, Cheng-Tun Qu & Shao-Fu Song

  2. School of Human Settlements and Civil Engineering, Xi’an Jiaotong University, Xi’an, People’s Republic of China

    Jun-Di Wang

  3. Shaanxi Key Laboratory of Environmental Pollution Control Technology and Reservoir Protection of Oilfield, Xi’an Shiyou University, Xi’an, 710065, People’s Republic of China

    Jun-Di Wang, Cheng-Tun Qu & Shao-Fu Song

  4. State Key Laboratory of Petroleum and Petrochemical Pollution Control and Treatment, Beijing, 102206, People’s Republic of China

    Jun-Di Wang, Cheng-Tun Qu & Shao-Fu Song

Authors
  1. Jun-Di Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Tun Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shao-Fu Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun-Di Wang.

Ethics declarations

Conflict of interes

The authors have declared no conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, JD., Qu, CT. & Song, SF. Temperature-induced changes in the proteome of Pseudomonas aeruginosa during petroleum hydrocarbon degradation. Arch Microbiol 203, 2463–2473 (2021). https://doi.org/10.1007/s00203-021-02211-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-021-02211-y

Keywords

Search

Navigation