Identification of a Novel Cathelicidin from the Deinagkistrodon Acutus

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Identification of a Novel Cathelicidin from the Deinagkistrodon Acutus toxins Article Identification of a Novel Cathelicidin from the Deinagkistrodon acutus Genome with Antibacterial Activity by Multiple Mechanisms Lipeng Zhong, Jiye Liu, Shiyu Teng and Zhixiong Xie * Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan 430072, China; [email protected] (L.Z.); [email protected] (J.L.); [email protected] (S.T.) * Correspondence: [email protected] Received: 13 October 2020; Accepted: 1 December 2020; Published: 4 December 2020 Abstract: The abuse of antibiotics and the consequent increase of drug-resistant bacteria constitute a serious threat to human health, and new antibiotics are urgently needed. Research shows that antimicrobial peptides produced by natural organisms are potential substitutes for antibiotics. Based on Deinagkistrodon acutus (known as five-pacer viper) genome bioinformatics analysis, we discovered a new cathelicidin antibacterial peptide which was called FP-CATH. Circular dichromatic analysis showed a typical helical structure. FP-CATH showed broad-spectrum antibacterial activity. It has antibacterial activity to Gram-negative bacteria and Gram-positive bacteria including methicillin-resistant Staphylococcus aureus (MRSA). The results of transmission electron microscopy (TEM) and scanning electron microscopy (SEM) showed that FP-CATH could cause the change of bacterial cell integrity, having a destructive effect on Gram-negative bacteria and inducing Gram-positive bacterial surface formation of vesicular structure. FP-CATH could bind to LPS and showed strong binding ability to bacterial DNA. In vivo, FP-CATH can improve the survival rate of nematodes in bacterial invasion experiments, and has a certain protective effect on nematodes. To sum up, FP-CATH is likely to play a role in multiple mechanisms of antibacterial action by impacting bacterial cell integrity and binding to bacterial biomolecules. It is hoped that the study of FP-CATH antibacterial mechanisms will prove useful for development of novel antibiotics. Keywords: D. acutus cathelicidin; bacterial cell integrity; antimicrobial peptide; DNA binding Key Contribution: FP-CATH binding to bacterial biomolecules affects the integrity of bacterial cells. This study laid the foundation for the design of antimicrobial peptides with multiple mechanisms. 1. Introduction The use of antibiotics is an effective treatment for infectious diseases, but in recent years, the misuse of antibiotics has caused more bacteria to become resistant or become superbugs [1]. Antimicrobial resistance (AMR) is a broad term referring to resistance to drugs that treat infections caused by bacteria. According to research reports, at the current growth rate, AMR could cause 10 million deaths by 2050, and exceed the 8.2 million cancer deaths in 2019 [2]. Perhaps in the near future, there may be no effective antibiotics available to humans, and more people will die from bacterial infections. Antibiotic resistance has become one of the world’s most pressing health problems. Antimicrobial peptides (Amps) are small molecular peptides with biological activity that exist in many organisms. The molecular weight of antimicrobial peptides is about 2000~7000 Da, and they are composed of 20~60 amino acid residues [3]. These active peptides are generally characterized by strong alkalinity, thermal stability, and broad-spectrum antibacterial activity [4–7]. Antimicrobial peptides are an important defense against the invasion of pathogenic microorganisms. Toxins 2020, 12, 771; doi:10.3390/toxins12120771 www.mdpi.com/journal/toxins Toxins 2020, 12, 771 2 of 17 Antimicrobial peptides (Amps) are small molecular peptides with biological activity that exist in many organisms. The molecular weight of antimicrobial peptides is about 2000~7000 Da, and they are composed of 20~60 amino acid residues [3]. These active peptides are generally characterized by strong alkalinity, thermal stability, and broad-spectrum antibacterial activity [4–7]. Antimicrobial peptides are an important defense against the invasion of pathogenic microorganisms. Toxins 2020, 12, 771 2 of 16 Cathelicidins are one of the largest families of structurally diverse antimicrobial peptides and are at least 400 million years old [8,9]. They were first identified in mammalian myeloid cells, and were Cathelicidinsthen found in are a onevariety of the of largestanimals, families including of structurally mammals, diversefish, birds, antimicrobial amphibians peptides, and reptiles and are [at10 least]. Snake 400 c millionathelicidin yearss w oldere [ 8found,9]. They in both were venomous first identified and non in mammalian-venomous snakes myeloid in cells, the literature, and were includingthen found KR in(F/A a variety)KKFFKK of animals,(L/P)K conservative including mammals, motif [11 fish,,12]. birds,They amphibians,showed a certain and reptilesefficacy [ 10in]. killingSnake cathelicidinspathogenic microorganisms, were found in both but venomous the specific and mechanism non-venomous is not snakes very clear. in the literature, including KR(FD/A)KKFFKK(L. acutus is endemic/P)K conservative to southern motif China [11;, 12it ].is They also showedknown aas certain the fi eveffi-cacypacer in viper killing, commonly pathogenic usedmicroorganisms, in traditional but Chinese the specific medicine mechanism. However, is not to verydate clear.no cathelicidin has been identified from D. acutusD.. T acutushis articleis endemic is based to southernon D. acutus China; genome it is also bioinformatics known as the analysis, five-pacer which viper, revealed commonly a usednew memberin traditional of the Chinese snake medicine.cathelicidin However, family tocalled date FP no-C cathelicidinATH. We hasshow beened that identified it possesses from D. potent acutus . broadThis article-spectrum is based and onrapidD. acutus antimicrobialgenome bioinformaticsactivity, low hemolytic analysis, toxicity which revealed, and strong a new anti memberbacterial of efftheect snake on bacterial cathelicidin cell integrity. family called We also FP-CATH. discovered We showed it could that bind it to possesses bacterial potent LPS and broad-spectrum DNA at low concentrationsand rapid antimicrobial. In vivo, FP activity,-CATH low can hemolytic protect nematode toxicity, ands in strongbacterial antibacterial invasion experiment effect on bacterials. Insights cell intointegrity. the mechanism We also discovered employed it could by FP bind-CATH to bacterial will h LPSelp andto fully DNA atunderstand low concentrations. the antibacterialIn vivo , mechanismFP-CATH can and protect guide the nematodes development in bacterial of efficient invasion antibiotics. experiments. Insights into the mechanism employed by FP-CATH will help to fully understand the antibacterial mechanism and guide the 2.development Results of efficient antibiotics. 2.1.2. Results Prediction and Analysis of FP-CATH in the D.acutus Transcriptome and Genome 2.1. PredictionThe D. acutus and Analysistranscriptome of FP-CATH and genome in the D. w acutusere analy Transcriptomezed by local and BLAST Genome program in NCBI. The sequence with the highest similarity peptide blast ExPASy was selected (see www.expasy.org). The resultsThe showD.ed acutus that transcriptomeit had a similarity and genometo cathelicidin were analyzedand had never by local been BLAST reported program before in; it NCBI. was namedThe sequence FP-CATH with. FP the-CATH highest pre similaritymature peptide peptide was blast used ExPASy as a template was selected for genomic (see www.expasy.org localization. It). isThe composed results showed of four thatexons it and had three a similarity introns to and cathelicidin locates at and genomic had never scaffold been 1306 reported (Figure before; 1A). it was named FP-CATH. FP-CATH premature peptide was used as a template for genomic localization. It is composed of four exons and three introns and locates at genomic scaffold 1306 (Figure1A). (A) (B) (C) Figure 1. Cont. ToxinsToxins 20202020,, 1212,, 771771 33 ofof 1617 (D) (E) FigureFigure 1.1. The FP-CATH bioinformatics analysis. (A) FP-CATH chromosomechromosome localization.localization. (B) Tertiary structurestructure predictionprediction ofof FP-CATH.FP-CATH. ((CC)) PropertiesProperties ofof selectedselected aminoamino acidacid residuesresidues formingforming thethe spiralspiral structurestructure ofof FP-CATHFP-CATH werewere calculatedcalculated byby Heli-QuestHeli-Quest WebWeb server.server. Arrow Arrow means (µμH) vectorvector (hydrophobic(hydrophobic momentmoment ofof peptide).peptide). ((DD)) PhylogeneticPhylogenetic analysisanalysis ofof FP-CATH.FP-CATH. TheThe treetree waswas constructedconstructed usingusing thethe neighbor-joining method by 1000 bootstrap replicates based on the immature cathelicidins. ((EE)) AminoAmino acidacid sequencessequences alignalign betweenbetween FP-CATHFP-CATH and and other other snake snake cathelicidins. cathelicidins. PredictingPredicting and and modeling modeling of of FP-CATH FP-CATH secondar secondaryy structure structure was was conducted conducted using using ExPASy. ExPASy. The Thepredicted predicted secondary secondary and tertiary and tertiary structures structures of the protein of the proteinshowed showedthat the thatamino the acids amino at 1-20 acids of atN 1-20fragment of N fragmentwere typical were helical typical structures helical structures as in Fi asgure in Figure1B. The1B. properties The properties of selected of selected amino amino acid acidresidues residues forming forming the thespiral spiral structure structure
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