Ecological adaptation of the Persian Gulf polychaete in a polluted area: proteomics concerning dominant defensive biomarkers


Marine species are negatively affected by wastewater. Based on our field observation along the Persian Gulf coastal areas, a widespread colony of polychaete worms, Galeolaria sp. lived in an area polluted with municipal wastewater. Accordingly, we hypothesized that a probable ecological adaption to bacterial pollutants has occurred. To test this hypothesis, protein profiling of coelomic fluid in the polychaetes collected from polluted and non-polluted areas was compared by RP-HPLC and 2DE, followed by MALDI-TOF analyses. The identical spots were selected as biomarkers, and the function of those proteins was determined by searching in databases in order to annotate their homologs using bioinformatics analyses by BLASTP, InterPro, PROSITE, Panther, and CDD servers. Twenty six and 17 HPLC fractions were extracted from the samples of polluted and non-polluted areas, respectively. Bacterial load in the water of polluted area was 2.8-fold higher than non-polluted area. The protein content of the samples of polluted area (3.65 µg/µL) was significantly greater than the samples of non-polluted (2.50 µg/µL) ones. MDS analysis of the HPLC profiles discriminated molecular pattern of polluted and non-polluted samples. Quantitative analysis of 2-DE results showed 65 and 23 spots in the polluted and non-polluted areas, respectively. Homology analyses of the peptide fragments derived from three biomarkers in the samples from polluted area, respectively, showed similarity with keratin, cyanelle 30S ribosomal protein, and peptidyl-prolyl isomerase, suggesting a reaction against bacterial pollution. The dominant biomarkers confirmed that probably a conditional adaptation has been happened in the polychaetes lived in the polluted area.

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Peptidyl-prolyl cis–trans isomerase


  1. Ayaz AM, Choi S (2014) Gram-negative marine bacteria: structural features of lipopolysaccharides and their relevance for economically important diseases. Mari Drugs 12:2485–2514

    Article  Google Scholar 

  2. Barth S, Edlich F, Berchner-Pfannschmidt U, Gneuss S, Jahreis G, Hasgall PA, Fandrey J, Wenger RH, Camenisch G (2007) The peptidyl prolyl cis/trans isomerase FKBP38 determines hypoxia-inducible transcription factor prolyl-4-hydroxylase PHD2 protein stability. Mol Cell Biol 27:3758–3768

    CAS  Article  Google Scholar 

  3. Bijlsma R, Loeschcke V (2005) Environmental stress, adaptation and evolution: an overview. J Evol Biol 18:744–749

    CAS  Article  Google Scholar 

  4. Dales RP, Dixon LJR (1980) Responses of polychaete annelids to bacterial infection. Comp Biochem Physiol 67:391–396

    Article  Google Scholar 

  5. Dew B (1959) Serpulidae (polychaeta) from Australia. Rec Aust Museum 25:19–56

    Article  Google Scholar 

  6. Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 2:476–478

    Article  Google Scholar 

  7. Fuchs E, Marchuk D (1983) Type I and type II keratins have evolved from lower eukaryotes to form the epidermal intermediate filaments in mammalian skin. Proc Natl Acad Sci USA 80:5857–5861

    CAS  Article  Google Scholar 

  8. Geyer PK, Meyuhas O, Perry RP, Johnson LF (1982) Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol Cell Biol 2:685–693

    CAS  Article  Google Scholar 

  9. Halt MN, Kupriyanova EK, Cooper SJB, Rouse GW (2009) Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida, Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology. Invertebr Syst 2:583–593

    Google Scholar 

  10. Jang CY, Lee JY, Kim J (2004) RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 560:81–85

    CAS  Article  Google Scholar 

  11. Liu S, Wang X, Sun F, Zhang J, Feng J, Liu H, Rajendran KV, Sun L, Zhang Y, Jiang Y, Peatman E, Kaltenboeck L, Kucuktas H, Liu Z (2013) RNA-seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol Genomics 45:462–476

    CAS  Article  Google Scholar 

  12. López-Maury L, Marguerat S, Bähler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9:583–593

    Article  Google Scholar 

  13. Mazumder B, Sampath P, Seshadri V, Maitra RK, DiCorleto PE, Pl Fox (2003) Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115:187–198

    CAS  Article  Google Scholar 

  14. Mohammadi Bardbari A, Arabestani MR, Karami M, Keramat F, Aghazadeh H, Alikhani MY, Pooshang-Bagheri K (2018) Highly synergistic activity of melittin with imipenem and colistin in biofilm inhibition against multidrug-resistant strong biofilm producer strains of Acinetobacter baumannii. Eur J Clin Microbiol Infect Dis 37:443–454

    Article  Google Scholar 

  15. Moll R, Divo M, Langbein L (2008) The human keratins: biology and pathology Histochem. Cell Biol 129:705–733

    CAS  Google Scholar 

  16. Munro PM, Gauthier MJ, Breittmayer VA, Bongiovanni J (1989) Influence of osmoregulation processes on starvation survival of Escherichia coli in seawater. Appl Environ Microbiol 55:2017–2024

    CAS  Article  Google Scholar 

  17. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

    Google Scholar 

  18. Otero-González AJ, Magalhães BS, Garcia-Villarino M, López-Abarrategui C, Sousa DA, Dias SC, Franco OL (2010) Antimicrobial peptides from marine invertebrates as a new frontier for microbial infection control. FASEB J 24:1320–1334

    Article  Google Scholar 

  19. Pixley RA, Espinola RG, Ghebrehiwet B, Joseph K, Kao A, Bdeir K, Cines DB, Colman RW (2011) Interaction of high-molecular-weight kininogen with endothelial cell binding proteins suPAR, gC1qR and cytokeratin 1 determined by surface plasmon resonance (BiaCore). Thromb Haemost 105:1053–1059

    CAS  Article  Google Scholar 

  20. Reverter M, Perez T, Ereskovsky AV, Banaigs B (2016) Secondary metabolome variability and inducible chemical defenses in the Mediterranean sponge Aplysina cavernicola. J Chem Ecol 42:60–70

    CAS  Article  Google Scholar 

  21. Rosenfeld J, Capdevielle J, Guillemot JC, Ferrara P (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal Biochem 203(1):173–179

    CAS  Article  Google Scholar 

  22. Straughan D (1967) Marine Serpulidae (Annelida: Polychaeta) of eastern Queensland and New South Wales. Aust J Zool 15:201–216

    Article  Google Scholar 

  23. Wool IG (1996) Extraribosomal functions of ribosomal proteins. Trends Biochem Sci 21:164–165

    CAS  Article  Google Scholar 

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The authors wish to thank all who assisted in conducting this work.

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N.R.S performed all experiments and also contributed to analyzing and writing the manuscript. R.M.N supervised the project and contributed to the experimental design, analyses, and revision of the manuscript. D.S and P.G.M served as advisor. K.P.B supervised the project and contributed to experimental design, analyses, writing, revision, and redaction of the manuscript.

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Correspondence to R. Mousavi-Nadushan.

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Editorial responsibility: J Aravind.

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Roohi-Shalmaee, N., Mousavi-Nadushan, R., Mostafavi, P.G. et al. Ecological adaptation of the Persian Gulf polychaete in a polluted area: proteomics concerning dominant defensive biomarkers. Int. J. Environ. Sci. Technol. 17, 1937–1946 (2020).

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  • Polychaete
  • Ecological adaptation
  • Pollution
  • Proteomics
  • Dominant defensive biomarkers