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The Antibiotic Andrimid Produced by Vibrio Coralliilyticus Increases Expression of Biosynthetic Gene Clusters and Antibiotic Production in Photobacterium Galatheae

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The Antibiotic Andrimid Produced by Vibrio Coralliilyticus Increases Expression of Biosynthetic Gene Clusters and Antibiotic Production in Photobacterium Galatheae Downloaded from orbit.dtu.dk on: Oct 05, 2021 The Antibiotic Andrimid Produced by Vibrio coralliilyticus Increases Expression of Biosynthetic Gene Clusters and Antibiotic Production in Photobacterium galatheae Buijs, Yannick; Isbrandt, Thomas; Zhang, Sheng-Da; Larsen, Thomas O.; Gram, Lone Published in: Frontiers in Microbiology Link to article, DOI: 10.3389/fmicb.2020.622055 Publication date: 2020 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): Buijs, Y., Isbrandt, T., Zhang, S-D., Larsen, T. O., & Gram, L. (2020). The Antibiotic Andrimid Produced by Vibrio coralliilyticus Increases Expression of Biosynthetic Gene Clusters and Antibiotic Production in Photobacterium galatheae. Frontiers in Microbiology, 11, [622055]. https://doi.org/10.3389/fmicb.2020.622055 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. fmicb-11-622055 December 16, 2020 Time: 15:27 # 1 ORIGINAL RESEARCH published: 22 December 2020 doi: 10.3389/fmicb.2020.622055 The Antibiotic Andrimid Produced by Vibrio coralliilyticus Increases Expression of Biosynthetic Gene Clusters and Antibiotic Production in Photobacterium galatheae Yannick Buijs, Thomas Isbrandt, Sheng-Da Zhang, Thomas Ostenfeld Larsen and Lone Gram* Department of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark The development and spread of multidrug resistant pathogens have reinforced Edited by: the urgency to find novel natural products with antibiotic activity. In bacteria, Harold J. Schreier, orphan biosynthetic gene clusters (BGCs) far outnumber the BGCs for which University of Maryland, Baltimore County, United States chemistry is known, possibly because they are transcriptionally silent under laboratory Reviewed by: conditions. A strategy to trigger the production of this biosynthetic potential is Blake Ushijima, to challenge the microorganism with low concentrations of antibiotics, and by University of North Carolina, Wilmington, United States using a Burkholderia genetic reporter strain (Seyedsayamdost, Proc Natl Acad Sci Avena Ross, 111:7266–7271), we found BGC unsilencing activity for the antimicrobial andrimid, Queen’s University, Canada produced by the marine bacterium Vibrio coralliilyticus. Next, we challenged another *Correspondence: marine Vibrionaceae, Photobacterium galatheae, carrier of seven orphan BGCs with Lone Gram [email protected] sub-inhibitory concentrations of andrimid. A combined approach of transcriptional and chemical measurements of andrimid-treated P. galatheae cultures revealed Specialty section: a 10-fold upregulation of an orphan BGC and, amongst others, a 1.6–2.2-fold This article was submitted to Microbial Physiology and Metabolism, upregulation of the gene encoding the core enzyme for biosynthesis of holomycin. a section of the journal Also, addition of andrimid caused an increase, based on UV-Vis peak area, of Frontiers in Microbiology 4-fold in production of the antibiotic holomycin. Transcriptional measurements of Received: 27 October 2020 Accepted: 30 November 2020 stress response related genes in P. galatheae showed a co-occurrence of increased Published: 22 December 2020 transcript levels of rpoS (general stress response) and andrimid induced holomycin Citation: overproduction, while in trimethoprim treated cultures attenuation of holomycin Buijs Y, Isbrandt T, Zhang S-D, production coincided with a transcriptional increase of recA (SOS stress response). Larsen TO and Gram L (2020) The Antibiotic Andrimid Produced by This study shows that using antimicrobial compounds as activators of secondary Vibrio coralliilyticus Increases metabolism can be a useful strategy in eliciting biosynthetic gene clusters and facilitate Expression of Biosynthetic Gene Clusters and Antibiotic Production natural product discovery. Potentially, such interactions could also have ecological in Photobacterium galatheae. relevant implications. Front. Microbiol. 11:622055. doi: 10.3389/fmicb.2020.622055 Keywords: biosynthetic gene cluster, Vibrionaceae, antibiotics, natural product discovery, stress response Frontiers in Microbiology| www.frontiersin.org 1 December 2020| Volume 11| Article 622055 fmicb-11-622055 December 16, 2020 Time: 15:27 # 2 Buijs et al. Andrimid Increases Antibiotic Holomycin Production INTRODUCTION products, mostly from Gram-positive Actinobacteria (Xu et al., 2017, 2019; Moon et al., 2019a,b). These studies show the Microbial natural products have provided humankind with a potential to use “old” antibiotics as a tool to un-silencing orphan broad range of medically useful molecules (Patridge et al., BGCs. It also poses the question of what the ecological advantage 2016). These natural products, or secondary metabolites, for bacteria could be to increase secondary metabolite output in play important physiological and ecological roles for the the face of chemical danger. producing microorganism and can shape microbial communities The competition sensing hypothesis addresses this question, (Pishchany and Kolter, 2020). Due to the alarming development and predicts that bacteria can employ their stress responses and spread of multidrug resistant pathogens (Michael et al., to sense competition and use this as a cue to increase their 2014), there is a need to discover novel bioactive products, in own antibiotic production (Cornforth and Foster, 2013). For particular, novel natural products with antibacterial activity to example, in the prolific antibiotic producing genus Streptomyces, supplement our array of clinical effective antibiotics (Moellering, competing strains modulate the antibiotic output of a focal 2011). In bacteria, genes encoding for the enzymes necessary to strain by chemical cues (Abrudan et al., 2015; Westhoff biosynthesize a natural product are almost exclusively clustered et al., 2020). Likewise, Chromobacterium violaceum increases together on so-called biosynthetic gene clusters (BGCs) (Walsh production of the purple pigment and antibacterial violacein and Fischbach, 2010). This genetic organization makes it possible when it is challenged with sub-MICs of antibiotics targeting to query the potential for production of secondary metabolites the polypeptide elongation step in protein synthesis (Lozano in genome-sequenced bacteria using specialized bioinformatics et al., 2020). This response was mediated by a newly identified tools (Medema et al., 2011). Genome mining studies have two-component regulatory system. In B. thailandensis, sub-MICs revealed that the majority of BGCs have not yet been linked to of trimethoprim change intracellular metabolite concentrations, a molecule, prompting the term “orphan BGCs” (Cimermancic which leads to the overproduction of malleilactone (Li et al., et al., 2014; Machado et al., 2015b; Jensen, 2016). For instance, 2020). These examples add to our knowledge on how, on the natural products of 25 out of 35 BGCs in Streptomyces galbus a mechanistic and molecular level, sub-MICs of antibiotics strain KCCM 41354 remain to be discovered (Blin et al., 2019). induce physiological and transcriptional responses in microbes Analogously, the red pigment prodigiosin is the only compound (Andersson and Hughes, 2014). that could be identified from Pseudoalteromonas rubra strain The marine Gram-negative Vibrionaceae family is a S4059 culture extract although genome mining identified 16 relatively underexplored source of natural products despite BGCs, excluding the prodigiosin cluster (Vynne et al., 2011; their widespread antagonistic behavior (Gram et al., 2010; Paulsen et al., 2019). Revealing the chemical products from Rypien et al., 2010; Wietz et al., 2010; Cordero et al., 2012) orphan BGCs is an important point at the agenda of discovering and genomic potential for secondary metabolite production novel natural products and potential novel drugs. (Machado et al., 2015b). We have demonstrated that Vibrio One commonly put-forward explanation for the high number coralliilyticus strain S2052 and Photobacterium galatheae S2753 of orphan BGCs is that, under the laboratory conditions used, produce the antimicrobial compounds andrimid, inhibitor these BGCs are transcriptionally silent (Rutledge and Challis, of fatty acid synthesis (Freiberg et al., 2004), and holomycin, 2015). Examples of culture condition dependent production of a potential intracellular zinc chelator (Chan et al., 2017), secondary metabolites (Giubergia et al., 2016; Romano et al., respectively (Wietz et al., 2010). Both species belong to the 2018; Tomm et al., 2019) suggest indeed that the right culture Vibrionaceae family and have similar ecological niches in the variables can lead to activation of otherwise silent BGCs and marine environment (Takemura et al., 2014; Labella et al., expression in the native host will greatly facilitate further studies. 2017). Genome
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