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Comparative Study
. 2020 Feb 12;20(1):33.
doi: 10.1186/s12866-020-1717-y.

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

Affiliations
Comparative Study

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

Mohamed E Hamid et al. BMC Microbiol. .

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 actinomycetoma - a 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.

Keywords: 16S rRNA gene; Actinomycetoma; Antagonistic potential; In vitro analysis; Phenotyping; S. sudanensis; Soil microbiome; Streptomycetes; Sudan.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Neighbor-joining tree based on 16S rRNA gene sequences showing relationships of soil streptomycetes with related, validly described Streptomyces species (accession numbers in brackets). In vitro inhibition against S. sudanensis, i.e.ratios between inhibition zone and colony diameter, are marked as I: Mean value and standard error. Evolutionary analysis was performed using MEGA7 software [16]
Fig. 2
Fig. 2
Abundance of streptomycetes and their phenotypic diversity related to precipitation level and soil type. Streptomycete abundance (a, c) at the level of mean value of colony forming units (×ばつ 105 / g soil) on humic acid agar and ISP2 agar, and Streptomyces phenotypic diversity (b, c) as related to annual precipitation and soil type, respectively. Precipitation levels 0–100 mm (very low), 101–400 mm (low), 401–600 mm (moderate) and 601–1000 mm (high). Streptomycete abundance was different between Arenosols and Yermosols (p = 0.048) and Vertisols and Yermosols (p = 0.012) according to one way ANOVA and Tukey test
Fig. 3
Fig. 3
Antagonistic potential of soil streptomycetes. The level of antagonism was determined as the ratio between the inhibition zone against S. sudanensis and colony size of soil streptomycetes. Data are presented in dependency of annual precipitation (a), ecoregion (b), soil type (c), Mycetoma (d) Streptomyces abundance (e), and phenotypic diversity of Streptomyces isolates (f). Abundance corresponds to the mean value of colony forming units (×ばつ 105 / g soil) on humic acid and ISP2 agar; Annual precipitation to precipitation levels 0–100 mm (very low), 101–400 mm (low), 401–600 mm (moderate) and 601–1000 mm (high); Ecoregion to East Sudanian savanna (EaSuSa), Sahelian Acacia savanna (SaAcSa) and South Saharan steppe and woodlands (SSaStWo), Mycetoma for the geographical origin of bacteria, from mycetoma belt, with confirmed, and without confirmed actinomycetoma. The Pearson correlation coefficients (R and p-value) are provided as measures of the strength of linear association between two variables
Fig. 4
Fig. 4
Principal coordinate analysis (PCoA) displaying Streptomyces isolate collections from three ecoregions. Streptomyces isolate collections of the three ecoregions in relation to the abundance of Streptomyces strains and Streptomyces phenotypes, level of antagonism against S. sudanensis, soil enzyme activity, pH, phosphorus and average rainfall. The numbers indicate the sites of isolation. Activity: soil enzyme activities; Abundance: number of streptomycetes colonies on HA and ISP2 agar; Antagonism: inhibitory activity against Streptomyces sudanensis
Fig. 5
Fig. 5
Terrestrial ecoregions of Sudan and South Sudan adapted from Burgess et al. [14]. The map shows soil collection sites (black spots), the mycetoma prevalence belt (thick broken red line) according to [27] and the confirmed Streptomyces sudanensis areas (inverted red triangles) from [9]. Key to sites: 1, Juba, Republic of South Sudan; 8, El Muglad, West Kordofan state; 10, Nyala, South Darfur state; 11, Soba, Khartoum state; 13, Kassala, Kassala state; 14, Umm Ruwaba, North Kordofan state; 16, Sennar, Sennar State; 21, Basonda, Al Gadarif state; 2, 4, 5 and 12, Hajj Abd Allah, Gazira state; 23, Al Fashir, North Darfur state; 7 and 19, Hussein Narti Northern state; 27, Ad Douiem, White Nile state; and 29, Ad Damazin, Blue Nile state. Written permission was obtained for the use of this figure from Island Press

References

    1. Kämpfer P. Family Streptomycetaceae. In: Whitman W, Goodfellow M, Kämpfer P, Busse H-J, Trujillo M, Ludwig W, Suzuki K-I, Parte A, editors. Bergey's manual of systematic bacteriology volume 5: the Actinobacteria. New York: Springer-Verlag; 2012.
    1. Lloyd AB. Behaviour of Streptomycetes in soil. J Gen Microbiol. 1969;56:165–170. doi: 10.1099/00221287-56-2-165. - DOI - PubMed
    1. Nicholls PK, Allen G, Irwin PJ. Streptomyces cyaneus dermatitis in a dog. Aust Vet J. 2014;92(1–2):38–40. doi: 10.1111/avj.12135. - DOI - PubMed
    1. Elzein S, Hamid ME, Quintana E, Mahjoub A, Goodfellow M. Streptomyces sp., a cause of fistulous withers in donkeys. Dtsch Tierarztl Wochenschr. 2002;109(10):442–443. - PubMed
    1. Doering-Saad C, Kampfer P, Manulis S, Kritzman G, Schneider J, Zakrzewska-Czerwinska J, et al. Diversity among Streptomyces strains causing potato scab. Appl Environ Microbiol. 1992;58(12):3932–3940. doi: 10.1128/AEM.58.12.3932-3940.1992. - DOI - PMC - PubMed

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