Elsevier

Gene

Volume 566, Issue 2, 25 July 2015, Pages 166-174
Gene

Research paper
Identifying a potential receptor for the antibacterial peptide of sponge Axinella donnani endosymbiont

https://doi.org/10.1016/j.gene.2015.04.070Get rights and content

Highlights

  • The receptor protein of the peptide was identified by comparative genomics approach

  • The active site identification was performed for the functional regions of BamA

  • The 3D structure of the novel peptide was modeled using de novo modeling

  • The BamA protein was docked with the peptide structure using Schrodinger software

  • MD simulations performed for the stability of the peptide and its complex with BamA

Abstract

Marine sponges and their associated bacteria are rich sources of novel secondary metabolites with therapeutic usefulness. In our earlier work, we have identified a novel antibacterial peptide from the marine sponge Axinella donnani endosymbiotic bacteria. In this work, we have carried out a comparative genomic analysis and identified a set of 60 proteins as probable receptor which is common in all the strains. The analysis on binding substrate showed that β barrel assembly machinery (BamA) of the outer membrane protein 85 (omp85) superfamily is a potential receptor protein for the antibacterial peptide. It plays a central role in OMP biogenesis, especially in cell viability. Further, the triplet and quartet motifs RGF and YGDG, respectively in L6 loop are conserved over all the strains and these conserved residues interact with antibacterial peptide to inhibit the BamA function, which is essential for OMP biogenesis.

Introduction

Natural products have been used as foods, fragrances, insecticides etc., and are real sources of most of the active ingredients of medicines. It has been reported that more than 80% of available drugs are from natural products and more than 12,000 antimicrobial compounds have been identified from marine organisms (Jacob and Ravikumar, 2012, Senthilkumar and Kim, 2013). Among the isolated potential metabolites, sponges were the predominant contributors. The identified bioactive substances from sponge associated microorganisms showed therapeutic importance such as anticancer, antibacterial, antifungal, antiviral, antiprotozoal, anthelmintic, anti-inflammatory, immunosuppressive and antifouling activities (Santos-Gandelman et al., 2014). Over the last decade a diverse group of sponge associated microbial metabolite structures were identified and tested for biological activity (Da Silva et al., 2014). The peptide based structural studies form a vital platform eventually leads to target identification and further drug designing. These studies mainly focused on the structure elucidation and function characterization of the steroids, terpenoids and related compounds and the proteomic analysis is not yet well documented. Hence, it is necessary to identify the structure–function relationship of antibacterial peptides. In our previous study, a novel antibacterial peptide from the endosymbiotic bacteria of the sponge Axinella donnani was identified and the antibacterial activity of the endosymbiont was experimentally determined against the human and shrimp pathogenic bacteria (Vimala et al., 2012). Based on these facts, in this work, we have carried out a systematic analysis for identifying the receptor protein using comparative genomics approach. We obtained a set of 60 proteins, which are common among all the eight pathogens and omp85 has been selected as a potential receptor using substrate and docking analysis. The structure of the antibacterial peptide was modeled using de novo modeling and subjected for protein–peptide docking with the BamA. Molecular Dynamics (MD) simulations were performed to assess the conformational stability of the peptide and its complex form with BamA. Our study agrees well with the experimental report (Albrecht et al., 2014) that the antibacterial peptide interacts with BamA at the conserved regions having functional importance.

Section snippets

Antibacterial peptide

We have used the antibacterial peptide, MSASTCLRREYFHCFRVLLIASVLDQPFVRETDQKTETI isolated from the endosymbiotic bacteria of the sponge A. donnani to identify the potential receptor and to study its mode of inhibitory activity.

Receptor identification

We have used the bacterial pathogens of human (Vibrio alginolyticus, Pseudomonas aerogenosa, Areomonas hydrophila and Vibrio harvae) and shrimp (Vibrio fischeri, Escherichia coli, Morgenella morgenii and Bacillus cereus) in the present study (Table 1). The genome sequences

Comparative genomics

The comparative genome analysis revealed the presence of 60 common coding sequences as shown in Fig. 1. We have identified the substrate of the resultant proteins using Interpro database and the information available in the literature. All common coding sequences of eight pathogenic organisms and their binding substrates are shown in Table 2. We found that only three proteins such as omp85 family outer membrane protein, protein-export membrane protein SecF and protein-export membrane protein

Conclusion

The systematic comparative genomics study predicted that BamA, one of the omp85 outer membrane family proteins can serve as a receptor for the broad spectrum of antibacterial peptide. The evolutionarily conserved motifs RGF and YGDG were functionally important in BamA and they were interacting with the peptide inhibitor. The Asp639, Gly640 and Leu641 were located in the L6 loop of extra-cytosolic region of the receptor showed the stable interactions with the peptide. The results found from this

Acknowledgment

We thank Protein Bioinformatics Laboratory, Department of Biotechnology, Bioinformatics Infrastructure Facility and Indian Institute of Technology Madras for computational facilities. A Vimala is a recipient of Women Post-Doctoral Fellowship from the Indian Institute of Technology Madras. We would like to thank the anonymous reviewers for their constructive comments.

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