Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential
Marine polychaetes represent an extremely rich and underexplored source of novel families of antimicrobial peptides (AMPs). The rapid development of next generation sequencing technologies and modern bioinformatics approaches allows us to apply them for characterization of AMP-derived genes and the...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-12-01
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| Series: | Marine Drugs |
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| Online Access: | https://www.mdpi.com/1660-3397/21/12/639 |
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| author | Pavel V. Panteleev Victoria N. Safronova Shuting Duan Alexey S. Komlev Ilia A. Bolosov Roman N. Kruglikov Tatiana I. Kombarova Olga V. Korobova Eugenia S. Pereskokova Alexander I. Borzilov Igor A. Dyachenko Olga V. Shamova Yu Huang Qiong Shi Tatiana V. Ovchinnikova |
| author_facet | Pavel V. Panteleev Victoria N. Safronova Shuting Duan Alexey S. Komlev Ilia A. Bolosov Roman N. Kruglikov Tatiana I. Kombarova Olga V. Korobova Eugenia S. Pereskokova Alexander I. Borzilov Igor A. Dyachenko Olga V. Shamova Yu Huang Qiong Shi Tatiana V. Ovchinnikova |
| author_sort | Pavel V. Panteleev |
| collection | DOAJ |
| description | Marine polychaetes represent an extremely rich and underexplored source of novel families of antimicrobial peptides (AMPs). The rapid development of next generation sequencing technologies and modern bioinformatics approaches allows us to apply them for characterization of AMP-derived genes and the identification of encoded immune-related peptides with the aid of genome and transcriptome mining. Here, we describe a universal bioinformatic approach based on the conserved BRICHOS domain as a search query for the identification of novel structurally unique AMP families in annelids. In this paper, we report the discovery of 13 novel BRICHOS-related peptides, ranging from 18 to 91 amino acid residues in length, in the cosmopolitan marine worm <i>Heteromastus filiformis</i> with the assistance of transcriptome mining. Two characteristic peptides with a low homology in relation to known AMPs—the α-helical amphiphilic linear peptide, consisting of 28 amino acid residues and designated as HfBRI-28, and the 25-mer β-hairpin peptide, specified as HfBRI-25 and having a unique structure stabilized by two disulfide bonds—were obtained and analyzed as potential antimicrobials. Interestingly, both peptides showed the ability to kill bacteria via membrane damage, but mechanisms of their action and spectra of their activity differed significantly. Being non-cytotoxic towards mammalian cells and stable to proteolysis in the blood serum, HfBRI-25 was selected for further <i>in vivo</i> studies in a lethal murine model of the <i>Escherichia coli</i> infection, where the peptide contributed to the 100% survival rate in animals. A high activity against uropathogenic strains of <i>E. coli</i> (UPEC) as well as a strong ability to kill bacteria within biofilms allow us to consider the novel peptide HfBRI-25 as a promising candidate for the clinical therapy of urinary tract infections (UTI) associated with UPEC. |
| first_indexed | 2024-03-08T20:34:31Z |
| format | Article |
| id | doaj.art-0d4a4a8fe7e14fa5b140590dbd98ea0d |
| institution | Directory Open Access Journal |
| issn | 1660-3397 |
| language | English |
| last_indexed | 2024-03-08T20:34:31Z |
| publishDate | 2023-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Marine Drugs |
| spelling | doaj.art-0d4a4a8fe7e14fa5b140590dbd98ea0d2023-12-22T14:22:25ZengMDPI AGMarine Drugs1660-33972023-12-01211263910.3390/md21120639Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic PotentialPavel V. Panteleev0Victoria N. Safronova1Shuting Duan2Alexey S. Komlev3Ilia A. Bolosov4Roman N. Kruglikov5Tatiana I. Kombarova6Olga V. Korobova7Eugenia S. Pereskokova8Alexander I. Borzilov9Igor A. Dyachenko10Olga V. Shamova11Yu Huang12Qiong Shi13Tatiana V. Ovchinnikova14M.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaM.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaM.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaInstitute of Experimental Medicine, WCRC “Center for Personalized Medicine”, 197022 St. Petersburg, RussiaM.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaM.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaState Research Center for Applied Microbiology & Biotechnology (SRCAMB), 142279 Obolensk, RussiaState Research Center for Applied Microbiology & Biotechnology (SRCAMB), 142279 Obolensk, RussiaState Research Center for Applied Microbiology & Biotechnology (SRCAMB), 142279 Obolensk, RussiaState Research Center for Applied Microbiology & Biotechnology (SRCAMB), 142279 Obolensk, RussiaThe Branch of M.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 142290 Pushchino, RussiaInstitute of Experimental Medicine, WCRC “Center for Personalized Medicine”, 197022 St. Petersburg, RussiaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen 518081, ChinaM.M. Shemyakin & Yu.A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997 Moscow, RussiaMarine polychaetes represent an extremely rich and underexplored source of novel families of antimicrobial peptides (AMPs). The rapid development of next generation sequencing technologies and modern bioinformatics approaches allows us to apply them for characterization of AMP-derived genes and the identification of encoded immune-related peptides with the aid of genome and transcriptome mining. Here, we describe a universal bioinformatic approach based on the conserved BRICHOS domain as a search query for the identification of novel structurally unique AMP families in annelids. In this paper, we report the discovery of 13 novel BRICHOS-related peptides, ranging from 18 to 91 amino acid residues in length, in the cosmopolitan marine worm <i>Heteromastus filiformis</i> with the assistance of transcriptome mining. Two characteristic peptides with a low homology in relation to known AMPs—the α-helical amphiphilic linear peptide, consisting of 28 amino acid residues and designated as HfBRI-28, and the 25-mer β-hairpin peptide, specified as HfBRI-25 and having a unique structure stabilized by two disulfide bonds—were obtained and analyzed as potential antimicrobials. Interestingly, both peptides showed the ability to kill bacteria via membrane damage, but mechanisms of their action and spectra of their activity differed significantly. Being non-cytotoxic towards mammalian cells and stable to proteolysis in the blood serum, HfBRI-25 was selected for further <i>in vivo</i> studies in a lethal murine model of the <i>Escherichia coli</i> infection, where the peptide contributed to the 100% survival rate in animals. A high activity against uropathogenic strains of <i>E. coli</i> (UPEC) as well as a strong ability to kill bacteria within biofilms allow us to consider the novel peptide HfBRI-25 as a promising candidate for the clinical therapy of urinary tract infections (UTI) associated with UPEC.https://www.mdpi.com/1660-3397/21/12/639antimicrobial peptideAnnelidaPolychaeta<i>Heteromastus filiformis</i>transcriptome miningBRICHOS domain |
| spellingShingle | Pavel V. Panteleev Victoria N. Safronova Shuting Duan Alexey S. Komlev Ilia A. Bolosov Roman N. Kruglikov Tatiana I. Kombarova Olga V. Korobova Eugenia S. Pereskokova Alexander I. Borzilov Igor A. Dyachenko Olga V. Shamova Yu Huang Qiong Shi Tatiana V. Ovchinnikova Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential Marine Drugs antimicrobial peptide Annelida Polychaeta <i>Heteromastus filiformis</i> transcriptome mining BRICHOS domain |
| title | Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential |
| title_full | Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential |
| title_fullStr | Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential |
| title_full_unstemmed | Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential |
| title_short | Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm <i>Heteromastus filiformis</i>: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential |
| title_sort | novel brichos related antimicrobial peptides from the marine worm i heteromastus filiformis i transcriptome mining synthesis biological activities and therapeutic potential |
| topic | antimicrobial peptide Annelida Polychaeta <i>Heteromastus filiformis</i> transcriptome mining BRICHOS domain |
| url | https://www.mdpi.com/1660-3397/21/12/639 |
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