Angucycline-like Aromatic Polyketide from a Novel Streptomyces Species Reveals Freshwater Snail Physa acuta as Underexplored Reservoir for Antibiotic-Producing Actinomycetes

Nasim Safaei,Boyke Bunk,Katharina Huber,Yvonne Mast,Joachim Wink,Michael Steinert

doi:10.3390/antibiotics10010022

Abstract

Simple SummaryThe current study shows that freshwater snails can be considered as new sources for bioactive metabolites, since a novel Streptomyces species 7NS3 produced four active compounds against Gram-positive bacteria. One of the compounds was an angucycline-like aromatic polyketide matched with a known compound, emycin A. 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.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 Physa acuta 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 Streptomyces due to its potential to produce antibiotics. Three Streptomyces strains (7NS1, 7NS2 and 7NS3) were isolated from P. acuta, 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 Streptomyces species, which was deposited as Streptomyces 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 P. acuta can represent promising reservoirs for the isolation of new antibiotic-producing actinobacterial species.

Highlights

Actinobacteria are one of the largest bacterial phyla in terms of the variety of identified species [1]
Our study demonstrates that freshwater snails like P. acuta can represent promising reservoirs for the isolation of new antibiotic-producing actinobacterial species
Insects and marine animals, including gastropods, benefit from Streptomyces-produced antibiotics to protect themselves against pathogens [28]

Summary

Introduction

Actinobacteria are one of the largest bacterial phyla in terms of the variety of identified species [1]. Due to a steady decline in new compound discoveries from terrestrial microbial sources, there is a growing interest to explore under-investigated habitats [5]. Such underexplored habitats are, for example, represented by natural symbiotic ecosystems. One of the widely studied mutualistic symbioses is evident in insect-associated Actinobacteria, as exemplified by the European beewolf that harbors the antibiotic-producing “Candidatus Streptomyces philanthi” in antennal glands to protect wasp larvae from fungal infections [7]. The host provides nutrition and a competition-free ecological niche for the bacterium [6,8] Another example of symbiotic association for protection of the host against antagonistic fungi is observed in the beetle Dendroctonus frontalis [9]. SPB74, prevents the growth of Ophiostoma minus, which is the beetle’s fungal antagonist [10]

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