Comparative Genomics of Marine Sponge-Derived Streptomyces spp. Isolates SM17 and SM18 With Their Closest Terrestrial Relatives Provides Novel Insights Into Environmental Niche Adaptations and Secondary Metabolite Biosynthesis Potential

Abstract

The emergence of antibiotic resistant microorganisms has led to an increased need for the discovery and development of novel antimicrobial compounds. Frequent rediscovery of the same natural products (NPs) continues to decrease the likelihood of the discovery of new compounds from soil bacteria. Thus, efforts have shifted toward investigating microorganisms and their secondary metabolite biosynthesis potential, from diverse niche environments, such as those isolated from marine sponges. Here we investigated at the genomic level two Streptomyces spp. strains, namely SM17 and SM18, isolated from the marine sponge Haliclona simulans , with previously reported antimicrobial activity against clinically relevant pathogens; using single molecule real-time (SMRT) sequencing. We performed a series of comparative genomic analyses on SM17 and SM18 with their closest terrestrial relatives, namely S. albus J1074 and S. pratensis ATCC 33331 respectively; in an effort to provide further insights into potential environmental niche adaptations (ENAs) of marine sponge-associated Streptomyces , and on how these adaptations might be linked to their secondary metabolite biosynthesis potential. Prediction of secondary metabolite biosynthetic gene clusters (smBGCs) indicated that, even though the marine isolates are closely related to their terrestrial counterparts at a genomic level; they potentially produce different compounds. SM17 and SM18 displayed a better ability to grow in high salinity medium when compared to their terrestrial counterparts, and further analysis of their genomes indicated that they possess a pool of 29 potential ENA genes that are absent in S. albus J1074 and S. pratensis ATCC 33331. This ENA gene pool included functional categories of genes that are likely to be related to niche adaptations and which could be grouped based on potential biological functions such as osmotic stress, defense; transcriptional regulation; symbiotic interactions; antimicrobial compound production and resistance; ABC transporters; together with horizontal gene transfer and defense-related features.

New Insight into Antimicrobial Compounds from Food and Marine-Sourced Carnobacterium Species through Phenotype and Genome Analyses

“…The dereplication process consists of the comparison of these predictions with databases to identify original BGCs. Phylogenetically-related organisms isolated from different ecological niches likely exhibit different genetic and phenotypic traits [ 19 , 20 ] and have the potential to biosynthesize various secondary metabolites [ 21 ]. In particular, organisms of marine origin are a promising source of innovative secondary metabolites [ 22 , 23 ].…”

Anthracycline Shunt Metabolites From Philippine Marine Sediment-Derived Streptomyces Destroy Cell Membrane Integrity of Multidrug-Resistant Staphylococcus aureus

“…The condition in the marine environment is remarkably different from that of the terrestrial environment. It is a hostile niche (Aneiros and Garateix, 2004;Imada, 2005;Valli et al, 2012), where marine microorganisms are exposed to low nutrition, high salinity, and high-pressure (Soliev et al, 2011;Almeida et al, 2019). As a result, marine microorganisms developed unique metabolic and physiological ability to survive by activating their environment adaptation genes (ENAs) (Almeida et al, 2019).…”

“…It is a hostile niche (Aneiros and Garateix, 2004;Imada, 2005;Valli et al, 2012), where marine microorganisms are exposed to low nutrition, high salinity, and high-pressure (Soliev et al, 2011;Almeida et al, 2019). As a result, marine microorganisms developed unique metabolic and physiological ability to survive by activating their environment adaptation genes (ENAs) (Almeida et al, 2019). Because of this, they produce different secondary metabolites that their terrestrial counterparts do not have (Imada, 2005;Zheng et al, 2011;Dholakiya et al, 2017).…”

“…These microorganisms contain high GC content in their DNA sequences and are reported to have antibiotic-producing biosynthetic gene clusters (BGC) (Hopwood, 2007;Dhakal et al, 2017;Romano et al, 2018) that produces about 75% of the clinically available antibacterial drugs in the market (Kemung et al, 2018). However, in the last 20 years, the re-discovery of previously characterized bioactive compounds and strain redundancy decreased the interest in these soil-dwelling bacteria as a source of novel bioactive compounds (Yang and Song, 2017;Almeida et al, 2019). Thus, Streptomyces living in other niches, such as the marine environment, gained value because of their chemodiversity (Chelvan et al, 2016;Dhakal et al, 2017;Yang and Song, 2017;Kemung et al, 2018;Romano et al, 2018;Al-Dhabi et al, 2019;Almeida et al, 2019).…”

In silico Screening and Heterologous Expression of a Polyethylene Terephthalate Hydrolase (PETase)-Like Enzyme (SM14est) With Polycaprolactone (PCL)-Degrading Activity, From the Marine Sponge-Derived Strain Streptomyces sp. SM14

“…Recent efforts to exploit the biotechnological potential of Streptomyces species have largely focused on the identification of bioactive small molecules and secondary metabolites biosynthetic gene clusters (Chevrette et al, 2019; Manteca and Yagüe, 2019). In this respect, the focus has started to shift toward Streptomyces isolates derived from varied niche environments, such as those isolated from the marine environment, which are still not well-characterized and majorly unexplored organisms, when compared to the previously more commonly studied soil-derived isolates (Dharmaraj, 2010; Hassan et al, 2017; Jin et al, 2018; Xu et al, 2018; Almeida et al, 2019).…”