Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes

Antibiotic producers have mainly been isolated from soil, which often has led to the rediscovery of known compounds. In this study, we identified the freshwater snail<i> Physa acuta</i> as an unexplored source for new antibiotic producers. The bacterial diversity associated with the snai...

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Main Authors: Nasim Safaei, Yvonne Mast, Michael Steinert, Katharina Huber, Boyke Bunk, Joachim Wink
Format: Article
Language:English
Published: MDPI AG 2021-12-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/10/1/22
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spelling doaj-574318d5fd6e40e89f27e18073e456e12020-12-30T00:04:50ZengMDPI AGAntibiotics2079-63822021-12-0110222210.3390/antibiotics10010022Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing ActinomycetesNasim Safaei0Yvonne Mast1Michael Steinert2Katharina Huber3Boyke Bunk4Joachim Wink5Department of microbial Strain Collection, Helmholtz Centre for Infection Research, Inhoffenstrasse 7, D-38124 Braunschweig, GermanyLeibniz Institute DSMZ, German Center for Infection Research (DZIF), Inhoffenstrasse 7, D-38124 Braunschweig, GermanyTechnical University of Braunschweig, Spielmannstr. 7, 38106 Braunschweig, GermanyLeibniz Institute DSMZ, German Center for Infection Research (DZIF), Inhoffenstrasse 7, D-38124 Braunschweig, GermanyLeibniz Institute DSMZ, German Center for Infection Research (DZIF), Inhoffenstrasse 7, D-38124 Braunschweig, GermanyDepartment of microbial Strain Collection, Helmholtz Centre for Infection Research, Inhoffenstrasse 7, D-38124 Braunschweig, GermanyAntibiotic producers have mainly been isolated from soil, which often has led to the rediscovery of known compounds. In this study, we identified the freshwater snail<i> Physa acuta</i> as an unexplored source for new antibiotic producers. The bacterial diversity associated with the snail was characterized by a metagenomic approach using cultivation-independent high-throughput sequencing. Although Actinobacteria represented only 2% of the bacterial community, the focus was laid on the isolation of the genus <i>Streptomyces</i> due to its potential to produce antibiotics. Three <i>Streptomyces</i> strains (7NS1, 7NS2 and 7NS3) were isolated from <i>P. acuta</i>, and the antimicrobial activity of the crude extracts were tested against a selection of Gram-positive and Gram-negative bacteria and fungi. 7NS3 showed the strongest activity against Gram-positive bacteria and, thus, was selected for genome sequencing and a phylogenomic analysis. 7NS3 represents a novel <i>Streptomyces</i> species, which was deposited as <i>Streptomyces</i> sp. DSM 110735 at the Leibniz Institute-German Collection of Microorganisms and Cell Cultures (DSMZ). Bioassay-guided high-performance liquid chromatography (HPLC) and high-resolution electrospray ionization-mass spectrometry (HR-ESI-MS) analyses of crude extract fractions resulted in the detection of four compounds, one of which matched the compound characteristics of emycin A, an angucycline-like aromatic polyketide. Genome mining studies based on the whole-genome sequence of 7NS3 resulted in the identification of a gene cluster potentially coding for emycin A biosynthesis. Our study demonstrates that freshwater snails like <i>P. acuta</i> can represent promising reservoirs for the isolation of new antibiotic-producing actinobacterial species.https://www.mdpi.com/2079-6382/10/1/22Actinobacteria<i>Physa acuta</i><i>Streptomyces</i>antibioticsangucycline
collection DOAJ
language English
format Article
sources DOAJ
author Nasim Safaei
Yvonne Mast
Michael Steinert
Katharina Huber
Boyke Bunk
Joachim Wink
spellingShingle Nasim Safaei
Yvonne Mast
Michael Steinert
Katharina Huber
Boyke Bunk
Joachim Wink
Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
Antibiotics
Actinobacteria
<i>Physa acuta</i>
<i>Streptomyces</i>
antibiotics
angucycline
author_facet Nasim Safaei
Yvonne Mast
Michael Steinert
Katharina Huber
Boyke Bunk
Joachim Wink
author_sort Nasim Safaei
title Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
title_short Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
title_full Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
title_fullStr Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
title_full_unstemmed Angucycline-Like Aromatic Polyketide from a Novel <i>Streptomyces</i> Species Reveals Freshwater Snail <i>Physa acuta</i> as Underexplored Reservoir for Antibiotic-Producing Actinomycetes
title_sort angucycline-like aromatic polyketide from a novel <i>streptomyces</i> species reveals freshwater snail <i>physa acuta</i> as underexplored reservoir for antibiotic-producing actinomycetes
publisher MDPI AG
series Antibiotics
issn 2079-6382
publishDate 2021-12-01
description Antibiotic producers have mainly been isolated from soil, which often has led to the rediscovery of known compounds. In this study, we identified the freshwater snail<i> Physa acuta</i> as an unexplored source for new antibiotic producers. The bacterial diversity associated with the snail was characterized by a metagenomic approach using cultivation-independent high-throughput sequencing. Although Actinobacteria represented only 2% of the bacterial community, the focus was laid on the isolation of the genus <i>Streptomyces</i> due to its potential to produce antibiotics. Three <i>Streptomyces</i> strains (7NS1, 7NS2 and 7NS3) were isolated from <i>P. acuta</i>, and the antimicrobial activity of the crude extracts were tested against a selection of Gram-positive and Gram-negative bacteria and fungi. 7NS3 showed the strongest activity against Gram-positive bacteria and, thus, was selected for genome sequencing and a phylogenomic analysis. 7NS3 represents a novel <i>Streptomyces</i> species, which was deposited as <i>Streptomyces</i> sp. DSM 110735 at the Leibniz Institute-German Collection of Microorganisms and Cell Cultures (DSMZ). Bioassay-guided high-performance liquid chromatography (HPLC) and high-resolution electrospray ionization-mass spectrometry (HR-ESI-MS) analyses of crude extract fractions resulted in the detection of four compounds, one of which matched the compound characteristics of emycin A, an angucycline-like aromatic polyketide. Genome mining studies based on the whole-genome sequence of 7NS3 resulted in the identification of a gene cluster potentially coding for emycin A biosynthesis. Our study demonstrates that freshwater snails like <i>P. acuta</i> can represent promising reservoirs for the isolation of new antibiotic-producing actinobacterial species.
topic Actinobacteria
<i>Physa acuta</i>
<i>Streptomyces</i>
antibiotics
angucycline
url https://www.mdpi.com/2079-6382/10/1/22
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