Skip to main content
Log in

Antibacterial effects of a polypeptide-enriched extract of Rana chensinensis via the regulation of energy metabolism

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The improper usage of antibiotics is known to cause widespread antibiotic resistance. In this study, the antibacterial effects of a polypeptide-enriched extract from the skin of the amphibian Rana chensinensis (RCP) were evaluated against the Gram-negative bacteria Escherichia coli and Pseudomonas aeruginosa, the Gram-positive bacterium Staphylococcus aureus and the fungus Candida albicans. The mechanisms underlying these effects were also studied, and the minimum inhibitory concentration of RCP was determined for each species. Analyses of the levels of adenosine triphosphates (ATPases), including Na+/K+-ATPase and Ca2+-ATPase, and scanning electron microscopy confirmed that RCP damaged the microbial cell walls and membranes. RCP perturbed microbial metabolism and particularly affected the tricarboxylic acid cycle (TCA), suggesting that this agent downregulated the levels of succinate dehydrogenase, malate dehydrogenase and ATPase activity in cells. Furthermore, RCP caused the leakage of genetic material from all four microbial strains. In conclusion, RCP effectively inhibited the growth of Gram-negative and Gram-positive bacteria and a fungal species by disrupting energy metabolic processes.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Ning HQ et al (2019) The synergistic antibacterial properties of glycinin basic peptide against bacteria via membrane damage and inactivation of enzymes. Food Biophys 14(2):132–141

    Article  Google Scholar 

  2. Hu W et al (2019) Antibacterial activity and mechanism of Litsea cubeba essential oil against methicillin-resistant Staphylococcus aureus (MRSA). Ind Crops Prod 130:34–41

    Article  CAS  Google Scholar 

  3. Abdelhamid AG, Esaam A, Hazaa MM (2018) Cell free preparations of probiotics exerted antibacterial and antibiofilm activities against multidrug resistant E. coli. Saudi Pharm J 26(5):603–607

    Article  PubMed  PubMed Central  Google Scholar 

  4. Nadhe SB et al (2019) Acinetobacter sp. mediated synthesis of AgNPs, its optimization, characterization and synergistic antifungal activity against C. albicans. J Appl Microbiol 127(2):445–458

    Article  CAS  PubMed  Google Scholar 

  5. Ranjbar M et al (2019) Anti-PcrV IgY antibodies protect against Pseudomonas aeruginosa infection in both acute pneumonia and burn wound models. Mol Immunol 116:98–105

    Article  CAS  PubMed  Google Scholar 

  6. Chelossi E, Faimali M (2006) Comparative assessment of antimicrobial efficacy of new potential biocides for treatment of cooling and ballast waters. Sci Total Environ 356(1–3):1–10

    Article  CAS  PubMed  Google Scholar 

  7. Ymele-Leki P et al (2012) A high-throughput screen identifies a new natural product with broad-spectrum antibacterial activity. PLoS ONE 7(2):8

    Article  CAS  Google Scholar 

  8. Terras FR et al (1993) A new family of basic cysteine-rich plant antifungal proteins from Brassicaceae species. FEBS Lett 316(3):233–240

    Article  CAS  PubMed  Google Scholar 

  9. Clark DP et al (1994) Ranalexin. A novel antimicrobial peptide from bullfrog (Rana catesbeiana) skin, structurally related to the bacterial antibiotic, polymyxin. J Biol Chem 269(14):10849–10855

    CAS  PubMed  Google Scholar 

  10. Cole AM, Weis P, Diamond G (1997) Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder. J Biol Chem 272(18):12008–12013

    Article  CAS  PubMed  Google Scholar 

  11. Xue W et al (2018) Optimization of the extraction of Gastrodia elata protein and its antibacterial. J Chin Inst Food Sci Technol 18(04):176–182

    Google Scholar 

  12. Cai XY et al (2019) Candida albicans vaginitis in a murine model is reduced by polypeptide-enriched Gastrodia elata extracts. Future Microbiol 14(10):839–846

    Article  CAS  PubMed  Google Scholar 

  13. Hancock REW, Rozek A (2002) Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol Lett 206(2):143–149

    Article  CAS  PubMed  Google Scholar 

  14. Wang C et al (2017) Cell surface binding, uptaking and anticancer activity of L-K6, a lysine/leucine-rich peptide, on human breast cancer MCF-7 cells. Sci Rep 7:13

    Article  CAS  Google Scholar 

  15. Wang ZY et al (2015) Characterization and antioxidant activity in vitro and in vivo of polysaccharide purified from Rana chensinensis skin. Carbohydr Polym 126:17–22

    Article  CAS  PubMed  Google Scholar 

  16. Zhang Y et al (2018) Acute toxicity, antioxidant, and antifatigue activities of protein-rich extract from Oviductus ranae. Oxid Med Cell Longev. https://doi.org/10.1155/2018/9021371

    Article  PubMed  PubMed Central  Google Scholar 

  17. Zhang X et al (2017) Polypeptides from the skin of Rana chensinensis exert the antioxidant and antiapoptotic activities on HaCaT cells. Anim Biotechnol 28(1):1–10

    Article  PubMed  CAS  Google Scholar 

  18. Rinaldi AC (2002) Antimicrobial peptides from amphibian skin: an expanding scenario—commentary. Curr Opin Chem Biol 6(6):799–804

    Article  CAS  PubMed  Google Scholar 

  19. Shen M et al (2017) Antimicrobial activity and membrane interaction mechanism of the antimicrobial peptides derived from Rana chensinensis with short sequences. Biologia 72(9):1089–1097

    Article  CAS  Google Scholar 

  20. Jiang YS, Fan WQ, Xu JM (2017) De novo transcriptome analysis and antimicrobial peptides screening in skin of Paa boulengeri. Genes Genomics 39(6):653–665

    Article  CAS  Google Scholar 

  21. Lan-Zhou L et al (2015) Study on preparation and in vitro antibacteral activity of polypeptide from the epidermis of Rana chensinensis. J Food Saf Qual 6(03):1067–1072

    Google Scholar 

  22. Gao YT et al (2017) Targeted modification of a novel amphibian antimicrobial peptide from Phyllomedusa tarsius to enhance its activity against MRSA and microbial biofilm. Front Microbiol 8:9

    Google Scholar 

  23. Kifer D, Muzinic V, Klaric MS (2016) Antimicrobial potency of single and combined mupirocin and monoterpenes, thymol, menthol and 1,8-cineole against Staphylococcus aureus planktonic and biofilm growth. J Antibiot 69(9):689–696

    Article  CAS  PubMed  Google Scholar 

  24. Silva JPB et al (2017) Antifungal activity of hydroalcoholic extract of Chrysobalanus icaco against oral clinical isolates of Candida species. Pharmacogn Res 9(1):96–100

    Article  CAS  Google Scholar 

  25. Sun XH et al (2018) Antibacterial effect and mechanism of anthocyanin rich Chinese wild blueberry extract on various foodborne pathogens. Food Control 94:155–161

    Article  CAS  Google Scholar 

  26. Mandelstam J (1960) The intracellular turnover of protein and nucleic acids and its role in biochemical differentiation. Bacteriol Rev 24(3):289–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shen SX et al (2015) Effects of cinnamaldehyde on Escherichia coli and Staphylococcus aureus membrane. Food Control 47:196–202

    Article  CAS  Google Scholar 

  28. Lin YL et al (2019) Antibacterial properties and possible action mechanism of chelating peptides-zinc nanocomposite against Escherichia coli. Food Control 106:8

    Google Scholar 

  29. Zhang F et al (2019) Effects of C-terminal amidation and heptapeptide ring on the biological activities and advanced structure of amurin-9KY, a novel antimicrobial peptide identified from the brown frog Rana kunyuensis. Zool Res 40(3):198–204

    Article  PubMed  PubMed Central  Google Scholar 

  30. Shi C, Zhang XW, Guo N (2018) The antimicrobial activities and action-mechanism of tea tree oil against food-borne bacteria in fresh cucumber juice. Microb Pathog 125:262–271

    Article  CAS  PubMed  Google Scholar 

  31. Eom SH et al (2014) The mechanism of antibacterial activity of phlorofucofuroeckol-A against methicillin-resistant Staphylococcus aureus. Appl Microbiol Biotechnol 98(23):9795–9804

    Article  CAS  PubMed  Google Scholar 

  32. Ren XY et al (2019) The antibacterial mechanism of pterostilbene derived from Xinjiang wine grape: a novel apoptosis inducer in Staphyloccocus aureus and Escherichia coli. Lwt-Food Sci Technol 101:100–106

    Article  CAS  Google Scholar 

  33. Dannenberg GD et al (2019) Essential oil from pink pepper (Schinus terebinthifolius Raddi): chemical composition, antibacterial activity and mechanism of action. Food Control 95:115–120

    Article  CAS  Google Scholar 

  34. Li YH et al (2017) Tea tree oil exhibits antifungal activity against Botrytis cinerea by affecting mitochondria. Food Chem 234:62–67

    Article  CAS  PubMed  Google Scholar 

  35. Fu Y et al (2014) Effects of sub-chronic aluminum chloride exposure on rat ovaries. Life Sci 100(1):61–66

    Article  CAS  PubMed  Google Scholar 

  36. Ontiveros M et al (2019) Natural flavonoids inhibit the plasma membrane Ca2+-ATPase. Biochem Pharmacol 166:1–11

    Article  CAS  PubMed  Google Scholar 

  37. Bhatt DK, Bano M (2009) Modulation of tricarboxylic acid cycle dehydrogenases during hepatocarcinogenesis induced by hexachlorocyclohexane in mice. Exp Toxicol Pathol 61(4):325–332

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was funded by the Special Projects of the Cooperation between Jilin University and Jilin Province (Grant No. SXGJXX2017-1), and Industrial Technology Research and Development Projects from Development and Reform Commission of Jilin Province (Grant No. 2019C050-8).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Di Wang or Guirong Zhang.

Ethics declarations

Conflict of interest

The authors have declared that there is no conflict of interest.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, R., Zhai, S., Liang, Y. et al. Antibacterial effects of a polypeptide-enriched extract of Rana chensinensis via the regulation of energy metabolism. Mol Biol Rep 47, 4477–4483 (2020). https://doi.org/10.1007/s11033-020-05508-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-05508-1

Keywords

Navigation