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Genome-Based Analysis of the Potential Bioactivity of the Terrestrial Streptomyces vinaceusdrappus Strain AC-40

Biology · 8 authors, 6 centres

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TL;DR

This study reports the isolation and whole-genome sequencing of Streptomyces vinaceusdrappus strain AC-40 from the rhizosphere of Pelargonium graveolens. The strain exhibited potent broad-spectrum antibacterial and antifungal activity, and genome mining revealed 27 biosynthetic gene clusters, including clusters related to known antimicrobials (candicidin, albaflavenone, streptothricin) and several with no known homology, suggesting potential for novel antibiotic discovery. The findings highlight the value of plant-associated Streptomyces as a source of new bioactive secondary metabolites for pharmaceutical and agricultural applications.

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**Background:** The rise of antimicrobial resistance poses a critical threat to global public health, driving an urgent need for novel antibiotics. Actinobacteria, particularly the genus Streptomyces, are prolific producers of bioactive secondary metabolites, with a single genome capable of harboring 25–70 biosynthetic gene clusters (BGCs), many of which remain silent under standard laboratory conditions. Plant-associated Streptomyces are especially promising due to their roles in biocontrol and plant growth promotion. This study aimed to genomically characterize Streptomyces vinaceusdrappus strain AC-40, isolated from the rhizosphere of the medicinal plant Pelargonium graveolens, and to identify its biosynthetic potential.

**Methods:** Strain AC-40 was isolated from P. graveolens rhizosphere soil on starch casein agar. Its antimicrobial activity was assessed via agar well diffusion against Staphylococcus aureus ATCC 6538, MRSA, Bacillus cereus ATCC 33018, Pseudomonas aeruginosa ATCC 27853, Escherichia coli O157:H7, and Candida albicans ATCC 60193, using gentamycin and itraconazole as positive controls. Whole-genome sequencing was performed on the Illumina MiSeq platform. Reads were assembled with Unicycler v0.4.8, scaffolded using RagTag v2.1.0 with Streptomyces sp. Osf17 as reference, and annotated via RAST and Prokka. Phylogenetic analysis used concatenated 16S rRNA, gyrB, and rpoB sequences with maximum likelihood (MegaX, Kimura 2-parameter, 1000 bootstrap). Average nucleotide identity (ANI) and in silico DDH were calculated using JSpecies and GGDC, respectively. BGCs were identified with AntiSMASH bacterial v6.0. Plant growth-promoting (PGP) genes were manually screened from Prokka annotations. Pan-genome and comparative genomic analyses were performed with Roary, PATRIC proteome comparison, and OrthoVenn2 against three related genomes: S. plicatus JCM 4504, S. vinaceusdrappus JCM 4529, and S. rochei 7434AN4.

**Key Results:** The de novo assembly yielded 1048 contigs covering 7,493,232 bp with 72.41% GC content. RAST annotated 7241 CDS (5059 functional), 35 tRNAs, and 3 rRNAs; Prokka annotated 6983 CDS (3303 functional), 82 tRNAs, and 3 rRNAs. Phylogenetic and ANI/DDH analyses identified the isolate as S. vinaceusdrappus strain AC-40 within the S. rochei group. The cell-free supernatant and ethyl acetate extract showed broad-spectrum antimicrobial activity against all tested pathogens, with effects equivalent to or exceeding positive controls. AntiSMASH detected 27 BGCs, including clusters highly similar to those for candicidin (antifungal polyene), albaflavenone (sesquiterpene antibiotic), and streptothricin (broad-spectrum N-glycoside antibiotic). Other BGCs corresponded to isorenieratene (antioxidant), ectoine (osmoprotectant), hopene, coelichelin, coelibactin, desferrioxamine, SapB, and geosmin. Several BGCs showed little or no similarity to known clusters, including a lanthipeptide class-I cluster and a lanthipeptide class-V cluster. Screening for PGP traits revealed genes for nitrogen assimilation, phosphate solubilization, siderophore production, chitinases, proteases, lipases, catalases, and peroxidases. KEGG pathway reconstruction identified 2530 annotated gene products across 327 pathways and 59 complete modules, including dissimilatory nitrate reduction to ammonia, assimilatory sulfate reduction, and crassulacean acid metabolism. Pan-genome analysis of the four S. rochei group genomes identified 246 core genes and 15,638 accessory genes. Comparative BGC analysis showed that most clusters were conserved between AC-40, S. vinaceusdrappus JCM 4529, and S. plicatus JCM 4504, while S. rochei 7434AN4 was the most divergent. Notably, region 26 (streptothricin-like) was absent in S. plicatus JCM 4504, and region 27 (hybrid PKS-II/butyrolactone) was absent in both S. vinaceusdrappus JCM 4529 and S. plicatus JCM 4504. Seven protein clusters (26 sequences) were unique to AC-40.

**Clinical Implications:** S. vinaceusdrappus strain AC-40 demonstrates potent, broad-spectrum antimicrobial activity and harbors multiple BGCs, including those for known clinically relevant antibiotics (candicidin, streptothricin) and several novel or uncharacterized clusters. The presence of unique BGCs and PGP traits positions this strain as a promising candidate for both pharmaceutical drug discovery and agricultural biocontrol applications. The conservation of several BGCs within the understudied S. rochei group suggests this phylogenetic group warrants further investigation as a source of novel bioactive metabolites.

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infectious_disease

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ORIGINAL PAPER

PMC10044865

Genome-Based Analysis of the Potential Bioactivity of the Terrestrial Streptomyces vinaceusdrappus Strain AC-40

Biology

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ABSTRACT

Simple Summary The problem of antimicrobial resistance represents a real danger to mankind. There is a crucial necessity to search for new antibiotics. The current advances in sequencing techniques and bioinformatics represent a critical tool for finding out the hidden biosynthetic capabilities within bacterial genomes and finding out novel active secondary metabolites. In this work, we managed to recover the Streptomyces vinaceusdrappus strain AC-40, a rhizobacterium with potent and broad-spectrum antimicrobial activity. We made whole genome sequencing and genome mining for the genes and gene clusters related to beneficial traits such as the production of secondary metabolites and plant growth promotion. Abstract Streptomyces are factories of antimicrobial secondary metabolites. We isolated a Streptomyces species associated with the Pelargonium graveolens rhizosphere. Its total metabolic extract exhibited potent antibacterial and antifungal properties against all the tested pathogenic microbes. Whole genome sequencing and genome analyses were performed to take a look at its main characteristics and to reconstruct the metabolic pathways that can be associated with biotechnologically useful traits. AntiSMASH was used to identify the secondary metabolite gene clusters. In addition, we searched for known genes associated with plant growth-promoting characteristics. Finally, a comparative and pan-genome analysis with three closely related genomes was conducted. It was identified as Streptomyces vinaceusdrappus strain AC-40. Genome mining indicated the presence of several secondary metabolite gene clusters. Some of them are identical or homologs to gene clusters of known metabolites with antimicrobial, antioxidant, and other bioactivities. It also showed the presence of several genes related to plant growth promotion traits. The comparative genome analysis indicated that at least five of these gene clusters are highly conserved through rochei group genomes. The genotypic and phenotypic characteristics of S. vinaceusdrappus strain AC-40 indicate that it is a promising source of beneficial secondary metabolites with pharmaceutical and biotechnological applications.

CITATION EXPORT

Abdelrahman M. Sedeek, Israa Salah, Hasnaa L. Kamel et al.. Genome-Based Analysis of the Potential Bioactivity of the Terrestrial Streptomyces vinaceusdrappus Strain AC-40. Biology. (2023). https://doi.org/10.3390/biology12030345

AUTHORS

8 · 6 CENTRES

Abdelrahman M. Sedeek, Israa Salah, Hasnaa L. Kamel, Mohamed A. Soltan, Eman Nour, Abdulrahman Alshammari, Muhammad Shahid Riaz Rajoka, Tarek R. Elsayed

1Department of Microbiology and Immunology, Faculty of Pharmacy, Sinai University—Kantara Branch, Ismailia 41522, Egypt
2Faculty of Pharmacy, Modern University for Technology and Information (MTI), Cairo 11585, Egypt
3Faculty of Organic Agriculture, Heliopolis University for Sustainable Development, Cairo 11785, Egypt
4Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University, Post Box 2455, Riyadh 11451, Saudi Arabia
5School of Dentistry, University of Maryland, Baltimore, MD 21201, USA
6Department of Agricultural Microbiology, Faculty of Agriculture, Cairo University, Giza 12613, Egypt

EDITOR / REVIEWER

Fengli Zhang, Michel Denis