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. 2020 Mar 20;8(3):441.
doi: 10.3390/microorganisms8030441.

Taxonomic Characterization and Secondary Metabolite Analysis of NEAU-wh3-1: An Embleya Strain with Antitumor and Antibacterial Activity

Affiliations

Taxonomic Characterization and Secondary Metabolite Analysis of NEAU-wh3-1: An Embleya Strain with Antitumor and Antibacterial Activity

Han Wang et al. Microorganisms. .

Abstract

Cancer is a serious threat to human health. With the increasing resistance to known drugs, it is still urgent to find new drugs or pro-drugs with anti-tumor effects. Natural products produced by microorganisms have played an important role in the history of drug discovery, particularly in the anticancer and anti-infective areas. The plant rhizosphere ecosystem is a rich resource for the discovery of actinomycetes with potential applications in pharmaceutical science, especially Streptomyces. We screened Streptomyces-like strains from the rhizosphere soil of wheat (Triticum aestivum L.) in Hebei province, China, and thirty-nine strains were obtained. Among them, the extracts of 14 isolates inhibited the growth of colon tumor cell line HCT-116. Strain NEAU-wh-3-1 exhibited better inhibitory activity, and its active ingredients were further studied. Then, 16S rRNA gene sequence similarity studies showed that strain NEAU-wh3-1 with high sequence similarities to Embleya scabrispora DSM 41855T (99.65%), Embleya hyalina MB891-A1T (99.45%), and Streptomyces lasii 5H-CA11T (98.62%). Moreover, multilocus sequence analysis based on the five other house-keeping genes (atpD, gyrB, rpoB, recA, and trpB) and polyphasic taxonomic approach comprising chemotaxonomic, phylogenetic, morphological, and physiological characterization indicated that the isolate should be assigned to the genus Embleya and was different from its closely related strains, therefore, it is proposed that strain NEAU-wh3-1 may be classified as representatives of a novel species of the genus Embleya. Furthermore, active substances in the fermentation broth of strain NEAU-wh-3-1 were isolated by bioassay-guided analysis and identified by nuclear magnetic resonance (NMR) and mass spectrometry (MS) analyses. Consequently, one new Zincophorin analogue together with seven known compounds was detected. The new compound showed highest antitumor activity against three human cell lines with the 50% inhibition (IC50) values of 8.8-11.6 μg/mL and good antibacterial activity against four pathogenic bacteria, the other known compounds also exhibit certain biological activity.

Keywords: Embleya; NEAU-wh-3-1; Rhizosphere soil; antibacterial activity; antitumor activity; compound.

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Conflict of interest statement

The authors declare that there are no conflict of interest.

Figures

Figure 1
Figure 1
Antitumor activities of extracts obtained from fourteen isolates against human colon tumor cell line HCT-116.
Figure 2
Figure 2
Scanning electron micrograph of spore chains of strain NEAU-wh3-1 grown on ISP 3 agar for 2 weeks at 28 °C.
Figure 3
Figure 3
Neighbor-joining tree showing the phylogenetic position of strain NEAU-wh3-1 (1487 bp) and related taxa based on 16S rRNA gene sequences. Bootstrap values > 50% (based on 1000 replications) are shown at branch points. Arthrobacter globiformis DSM 20124T (M23411) was used as an outgroup. Asterisks indicate branches also recovered in the maximum-likelihood tree; Bar, 0.01 substitutions per nucleotide position.
Figure 4
Figure 4
Neighbor-joining tree based on multilocus sequence analysis (MLSA) analysis of the concatenated partial sequences (1979 bp) from five housekeeping genes (atpD, gyrB, recA, rpoB, and trpB) of strain NEAU-wh3-1 (in bold) with related taxa. Only bootstrap values above 50% (percentages of 1000 replications) are indicated. Asterisks indicate branches also recovered in the maximum-likelihood tree; Bar, 0.05 substitutions per nucleotide position.
Figure 5
Figure 5
The structures of compounds 18. Compound 1 was isolated as white solid with [α]D25 + 15 (c 0.043, EtOH) and UV (EtOH) λmax nm (log ε): 202 (4.53). Its molecular formula was established as C31H56O7 by HR-ESI-MS at m/z 539.3942 [M-H]- (calcd 539.3953 as C31H55O7). The IR spectrum revealed hydroxyl absorption at 3320 cm−1 and carbonyl absorption at 1735 cm−1, as well as methyl and methylene absorptions at 2953 cm−1 and 2924 cm−1.
Figure 6
Figure 6
2D nuclear magnetic resonance (NMR) correlations of compound 1.

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