Diversity and geographic distribution of soil streptomycetes with antagonistic potential against actinomycetoma-causing Streptomyces sudanensis in Sudan and South Sudan

Abstract

Background: Production of antibiotics to inhibit competitors affects soil microbial community composition and contributes to disease suppression. In this work, we characterized whether Streptomyces bacteria, prolific antibiotics producers, inhibit a soil borne human pathogenic microorganism, Streptomyces sudanensis. S. sudanensis represents the major causal agent of actinomycetomaa largely under-studied and dreadful subcutaneous disease of humans in the tropics and subtropics. The objective of this study was to evaluate the in vitro S. sudanensis inhibitory potential of soil streptomycetes isolated from different sites in Sudan, including areas with frequent (mycetoma belt) and rare actinomycetoma cases of illness.Results: Using selective media, 173 Streptomyces isolates were recovered from 17 sites representing three ecoregions and different vegetation and ecological subdivisions in Sudan. In total, 115 strains of the 173 (66.5%) displayed antagonism against S. sudanensis with different levels of inhibition. Strains isolated from the South Saharan steppe and woodlands ecoregion (Northern Sudan) exhibited higher inhibitory potential than those strains isolated from the East Sudanian savanna ecoregion located in the south and southeastern Sudan, or the strains isolated from the Sahelian Acacia savanna ecoregion located in central and western Sudan. According to 16S rRNA gene sequence analysis, isolates were predominantly related to Streptomyces werraensis, S. enissocaesilis, S. griseostramineus and S. prasinosporus. Three clusters of isolates were related to strains that have previously been isolated from human and animal actinomycetoma cases: SD524 (Streptomyces sp. subclade 6), SD528 (Streptomyces griseostramineus) and SD552 (Streptomyces werraensis). Conclusion:The in vitro inhibitory potential against S. sudanensis was proven for more than half of the soil streptomycetes isolates in this study and this potential may contribute to suppressing the abundance and virulence of S. sudanensis. The streptomycetes isolated from the mycetoma free South Saharan steppe ecoregion show the highest average inhibitory potential. Further analyses suggest that mainly soil properties and rainfall modulate the structure and function of Streptomyces species, including their antagonistic activity against S. sudanensis.

Isolation and Identification of Streptomyces spp. from Desert and Savanna Soils in Sudan

“…Streptomyces species are not just free-living soil organisms; they have a valuable ecological function in the soil as they have evolved to exist in symbiosis with plants, fungi, and animals [ 29 ]. Streptomycetes are recognized to yield many secondary metabolites that can reduce the growth of pathogens, including plant pathogens [ 30 , 31 ] and human pathogens [ 32 , 33 , 34 ]. It is probable that these antibiotics evolved as a direct result of their interactions with other organisms namely in symbiosis with fungi, plants, and animals [ 29 , 35 ].…”

Systematic whole-genome sequencing reveals an unexpected diversity among actinomycetoma pathogens and provides insights into their antibacterial susceptibilities

“…Extracts from the 16S rRNA phylogenies of Streptomyces (full figure in SI Fig 1 and https://itol.embl.de/shared/1MX60mtB0Ohk3) showing the placement of isolates (green dots) with related rRNA sequences from the ezBioCloud 16S rRNA database (blue dot), soil isolates from Sudan (yellow dots [42]) and isolates collected by Sengupta, Goodfellow and Hamid (unpublished) from human actinomycetoma (purple) and from donkey withers (lilac). Inferred using iqtree2 and the GTR+F+R5 model.…”

“…The identification of isolates of S. sudanensis and S. warraenensis with similarity to samples previously isolated from donkey withers by Sengupta, Goodfellow and Hamid (unpublished) suggests that some actinomycetoma causing strains may have the potential to infect multiple host species [42]. Epidemic outbreaks of eumycetoma ( Sporothrix brasiliensis ) have previously been linked with zoonotic transmission from cats to humans [66], and the identification of multi-host actinomycetoma causing strains also raises zoonosis as a possible route for transmission of the bacterial disease.…”

Bioinformatics in Sudan: Status and challenges case study: The National University-Sudan

“…The articles relating to subjects from Sudan are usually collaborative projects between scientists in Sudanese institutions and those in regional or international research centers. These projects include studies that have analyzed the full genome sequence of Dromedary camels to evaluate the genomic diversity and signatures of positive selection [ 27 ], the phylogenetic tree analysis of Streptomyces isolates from soil [ 28 ], and anti-hepatitis B virus activity isolated from Guiera senegalensis leaves [ 29 ]. The studies also included articles that investigated the prediction of the appropriate Middle East Respiratory Syndrome Coronavirus (MERS-CoV) epitope vaccine [ 30 ], identification of mutations in the Theileria annulata prolyl isomerase I gene ( TaPIN1 ) [ 31 ], malaria drug resistance molecular markers [ 32 ], whole genome sequencing of Klebsiella pneumoniae [ 33 ] and Acinetobacter baumannii [ 34 ], and the function of EIL/EIN3 transcription factor genes in cotton fiber development [ 35 ].…”