A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities
Antimicrobial peptides (AMPs) may be the most promising substitute for antibiotics due to their effective bactericidal activity and multiple antimicrobial modes against pathogenic bacteria. In this study, a new functional gene named Spgillcin was identified in Scylla paramamosain, which encoded 216...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.928220/full |
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| author | Xiaofei Wang Xiao Hong Fangyi Chen Fangyi Chen Fangyi Chen Ke-Jian Wang Ke-Jian Wang Ke-Jian Wang |
| author_facet | Xiaofei Wang Xiao Hong Fangyi Chen Fangyi Chen Fangyi Chen Ke-Jian Wang Ke-Jian Wang Ke-Jian Wang |
| author_sort | Xiaofei Wang |
| collection | DOAJ |
| description | Antimicrobial peptides (AMPs) may be the most promising substitute for antibiotics due to their effective bactericidal activity and multiple antimicrobial modes against pathogenic bacteria. In this study, a new functional gene named Spgillcin was identified in Scylla paramamosain, which encoded 216 amino acids of mature peptide. In vivo, Spgillcin was dominantly expressed in the gills of male and female crabs, offering the highest expression level among all tested organs or tissues. The expression pattern of Spgillcin was significantly altered when challenged by Staphylococcus aureus, indicating a positive immune response. In vitro, a functional truncated peptide Spgillcin177–189 derived from the amino acid sequence of Spgillcin was synthesized and showed a broad-spectrum and potent antibacterial activity against several bacterial strains, including the clinical isolates of multidrug-resistant (MDR) strains, with a range of minimum inhibitory concentrations from 1.5 to 48 μM. Spgillcin177–189 also showed rapid bactericidal kinetics for S. aureus and Pseudomonas aeruginosa but did not display any cytotoxicity to mammalian cells and maintained its antimicrobial activity in different conditions. Mechanistic studies indicated that Spgillcin177–189 was mainly involved in the disruption of cell membrane integrity where the membrane components lipoteichoic acid and lipopolysaccharide could significantly inhibit the antimicrobial activity in a dose-dependent manner. In addition, Spgillcin177–189 could change the membrane permeability and cause the accumulation of intracellular reactive oxygen species. No resistance was generated to Spgillcin177–189 when the clinical isolates of methicillin-resistant S. aureus and MDR P. aeruginosa were treated with Spgillcin177–189 and then subjected to a long term of continuous culturing for 50 days. In addition, Spgillcin177–189 exerted a strong anti-biofilm activity by inhibiting biofilm formation and was also effective at killing extracellular S. aureus in the cultural supernatant of RAW 264.7 cells. Taken together, Spgillcin177–189 has strong potential as a substitute for antibiotics in future aquaculture and medical applications. |
| first_indexed | 2024-12-10T15:48:48Z |
| format | Article |
| id | doaj.art-a686b9cee8f744fcaacad5dab7a00a67 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-12-10T15:48:48Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-a686b9cee8f744fcaacad5dab7a00a672022-12-22T01:42:51ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-08-011210.3389/fcimb.2022.928220928220A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activitiesXiaofei Wang0Xiao Hong1Fangyi Chen2Fangyi Chen3Fangyi Chen4Ke-Jian Wang5Ke-Jian Wang6Ke-Jian Wang7State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState-Province Joint Engineering Laboratory of Marine Bioproducts and Technology, College of Ocean and Earth Sciences, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaFujian Innovation Research Institute for Marine Biological Antimicrobial Peptide Industrial Technology, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaState-Province Joint Engineering Laboratory of Marine Bioproducts and Technology, College of Ocean and Earth Sciences, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaFujian Innovation Research Institute for Marine Biological Antimicrobial Peptide Industrial Technology, College of Ocean and Earth Sciences, Xiamen University, Xiamen, ChinaAntimicrobial peptides (AMPs) may be the most promising substitute for antibiotics due to their effective bactericidal activity and multiple antimicrobial modes against pathogenic bacteria. In this study, a new functional gene named Spgillcin was identified in Scylla paramamosain, which encoded 216 amino acids of mature peptide. In vivo, Spgillcin was dominantly expressed in the gills of male and female crabs, offering the highest expression level among all tested organs or tissues. The expression pattern of Spgillcin was significantly altered when challenged by Staphylococcus aureus, indicating a positive immune response. In vitro, a functional truncated peptide Spgillcin177–189 derived from the amino acid sequence of Spgillcin was synthesized and showed a broad-spectrum and potent antibacterial activity against several bacterial strains, including the clinical isolates of multidrug-resistant (MDR) strains, with a range of minimum inhibitory concentrations from 1.5 to 48 μM. Spgillcin177–189 also showed rapid bactericidal kinetics for S. aureus and Pseudomonas aeruginosa but did not display any cytotoxicity to mammalian cells and maintained its antimicrobial activity in different conditions. Mechanistic studies indicated that Spgillcin177–189 was mainly involved in the disruption of cell membrane integrity where the membrane components lipoteichoic acid and lipopolysaccharide could significantly inhibit the antimicrobial activity in a dose-dependent manner. In addition, Spgillcin177–189 could change the membrane permeability and cause the accumulation of intracellular reactive oxygen species. No resistance was generated to Spgillcin177–189 when the clinical isolates of methicillin-resistant S. aureus and MDR P. aeruginosa were treated with Spgillcin177–189 and then subjected to a long term of continuous culturing for 50 days. In addition, Spgillcin177–189 exerted a strong anti-biofilm activity by inhibiting biofilm formation and was also effective at killing extracellular S. aureus in the cultural supernatant of RAW 264.7 cells. Taken together, Spgillcin177–189 has strong potential as a substitute for antibiotics in future aquaculture and medical applications.https://www.frontiersin.org/articles/10.3389/fcimb.2022.928220/fullScylla paramamosainantimicrobial peptideSpgillcin177–189drug resistanceS. aureus and P. aeruginosa |
| spellingShingle | Xiaofei Wang Xiao Hong Fangyi Chen Fangyi Chen Fangyi Chen Ke-Jian Wang Ke-Jian Wang Ke-Jian Wang A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities Frontiers in Cellular and Infection Microbiology Scylla paramamosain antimicrobial peptide Spgillcin177–189 drug resistance S. aureus and P. aeruginosa |
| title | A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities |
| title_full | A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities |
| title_fullStr | A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities |
| title_full_unstemmed | A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities |
| title_short | A truncated peptide Spgillcin177–189 derived from mud crab Scylla paramamosain exerting multiple antibacterial activities |
| title_sort | truncated peptide spgillcin177 189 derived from mud crab scylla paramamosain exerting multiple antibacterial activities |
| topic | Scylla paramamosain antimicrobial peptide Spgillcin177–189 drug resistance S. aureus and P. aeruginosa |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.928220/full |
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