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Genomic and Phenotypic Analyses of Chitin Degradation and Secondary Metabolite Production in Pseudoalteromonas

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Downloaded from orbit.dtu.dk on: Oct 06, 2021 Genomic and phenotypic analyses of chitin degradation and secondary metabolite production in Pseudoalteromonas Paulsen, Sara Skøtt Publication date: 2020 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): Paulsen, S. S. (2020). Genomic and phenotypic analyses of chitin degradation and secondary metabolite production in Pseudoalteromonas. DTU Bioengineering. 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. Genomic and phenotypic analyses of chitin degradation and secondary metabolite production in Pseudoalteromonas Sara Skøtt Paulsen PhD Thesis March 2020 Preface This present PhD study serves as a partial fulfillment of the requirements to obtain a PhD degree from the Technical University of Denmark (DTU). The work has has been carried out at the Department of Biotechnology and Biomedicine (DTU Bioengineering) from October 2016 to March 2020 under the supervision of Professor Lone Gram and Senior Researcher Eva Sonnenschein. The PhD was supported by the Villum Foundation (Annual Award to Lone Gram) and a PhD stipend from DTU Bioengineering. The work resulted in three research articles which are included in this thesis. Sara Skøtt Paulsen Kgs. Lyngby, March 2020 i Acknowledgements First I would like to thank my supervisor Lone Gram, with whom I was first acquainted with in 2011 during my BSc education. Thank you so much for taking care of me all these years – both scientifically and non-scientifically – and for trusting me with this PhD project. I would also like to thank my co-supervisor Eva Sonnenschein. Thanks for your support and encouragement. You inspire me on so many levels, and I am proud to call you my friend. Thank you! Special thanks go to past and present members of the GramLab. You have always made room for scientific discussions, moral support and fun (with and without C2H6O). Karen, Nicole and Bastian, thanks for being my partners-in-crime from the start to the (semi)end. Also thanks to Thomas & Thomas, Xiyan and Shengda for the good collaborations and Mikael for your endless help with bioinformatics. HUGE thanks to Jette who always helped me in the lab and also just for your kind and loving person. Special thanks go to my family who has always supported me (although they probably still have no clue what I have been doing for the past 3 years). My friends Sarah, Pernille, Katrine, Tina, Christian, Kristian and Gustav – thanks for socializing with me once in a while. Finally, thanks to Udo Fischer. Danke. ii Abstract The continuous emergence and spread of antibiotic resistant bacteria is a huge threat to modern society. We need to find and develop novel antimicrobial compounds to enable treatment of infectious diseases in the future. Bacteria have for decades provided antimicrobial compounds, and along with the genomic sequencing era it has become evident that only a minority of the potential antibiotic compounds encoded in the genomes of bacteria are yet discovered. In the past decades, the marine environment has gained attention because of its rich biodiversity being unexplored from a pharma- and biotech point of view. Marine bacteria are a prolific resource of novel antimicrobials, and in particular those of the genus Pseudoalteromonas. The purpose of this PhD project was to investigate the genus Pseudoalteromonas for its potential to produce novel antimicrobial compounds using in silico and in vitro methods. A global in silico analysis of 157 strains from the genus Pseudoalteromonas confirmed that pigmented species of the genus are potent producers of antimicrobial compounds, dedicating as much as 15% of their genomic content for this purpose. The global analysis also revealed many taxonomic discrepancies within the genus, and led us to pursue the description of a novel species Pseudoalteromonas galatheae. This subsequently contributed to the expansion of phylogeny within the genus and highlighted the importance of incorporating genomic information when describing novel species. Many antimicrobial compounds are encoded in so-called cryptic or silent (or orphan) biosynthetic gene clusters within the genomes, meaning that the chemistry of the compounds produced is not known. Previous studies have shown that using carbon sources mimicking the natural environment of bacteria can induce production of antimicrobial compounds in marine vibrios. In silico analysis of carbohydrate-active enzymes in genomes of Pseudoalteromonas showed that chitin was likely a preferred substrate for the bioactive pigmented species and we thus hypothesized that chitin degradation and production of antimicrobial compounds could be interconnected within the genus Pseudoalteromonas. Using a metabolomics approach as well as constructing chitinase gene deletion mutants it was found that the marine carbon sources did alter the metabolome of two strains, but that chitin was not convincingly inducing production of antimicrobial compounds. Concluding, this work has contributed to the understanding of the genus Pseudoalteromonas, highlighting their immense genetic capacity to produce novel antimicrobial compounds, which is similar to that of our most famous antibiotic producers, the Actinomycetes. This knowledge can be used to target the discovery of novel drugs towards culturable bacteria with a huge unknown bioactivity potential. iii Resumé Den kontinuerlige fremkomst og spredning af antibiotikaresistente bakterier er en stor trussel mod det moderne samfund. Det er nødvendigt at finde og udvikle nye antimikrobielle stoffer for at kunne bekæmpe smitsomme infektioner i fremtiden. Bakterier har i årtier været producent af antimikrobielle stoffer, og i forbindelse med genomsekventerings-æraen er det blevet klart, at kun en brøkdel af de potente antimikrobielle stoffer, som bakteriernes genom koder for, er blevet opdaget. I de sidste årtier har det marine miljø opnået stor opmærksomhed på grund af dets rige samt uudforskede biodiversitet fra et pharma- og biotekrelateret synspunkt. Marine bakterier udgør en rig kilde til nye antimikrobielle stoffer, især bakterier af slægten Pseudoalteromonas. Formålet med dette PhD projekt har været at undersøge slægten Pseudoalteromonas for dens evne til at producere nye antimikrobielle stoffer ved brug af in silico og in vitro metoder. En global in silico analyse af 157 stammer fra slægten Pseudoalteromonas bekræftede at pigmenterede arter i slægten er potente producenter af antimikrobielle stoffer, og dedikerer op til 15 % af deres genetiske materiale til dette formål. Den globale analyse afslørede også flere taksonomiske uoverensstemmelser i slægten, hvilket ledte os til at forfølge beskrivelsen af den nye art Pseudoalteromonas galatheae. Dette har bidraget til udvidelsen af fylogenien samt fremhæver vigtigheden af at inkorporere genomisk information i beskrivelsen af nye arter. Mange antimikrobielle stoffer er kodet for af såkaldte kryptiske eller tavse (eller ’orphan’) biosyntetiske genklynger i genomerne, hvilket betyder at kemien af stofferne ikke er kendt. Tidligere studier har vist at brugen af karbonkilder, som efterligner bakteriernes naturlige miljø, kan inducere produktionen af antimikrobielle stoffer i marine vibrio. En in silico analyse af kulhydrat- aktive enzymer i Pseudoalteromonas genomerne viste, at kitin var et muligt foretrukken substrat for de bioaktive pigmenterede arter og derfor hypoteserede vi, at kitinnedbrydning og produktion af antimikrobielle stoffer kunne være koblet sammen i slægten Pseudoalteromonas. Ved brug af metabolomics samt konstruktion af kitinase gen-deletion mutanter fandt vi, at marine karbonkilder kan påvirke metabolomet af two stammer, men at kitin ikke overbevisende inducerede produktionen af antimikrobielle stoffer. Afslutningsvis har dette værk bidraget til forståelsen af slægten Pseudoalteromonas, og understreger slægtens enorme genetiske kapacitet for at producere nye antimikrobielle stoffer, som er lignende den af vores mest kende antibiotika-producenter, Actinomyceter. Denne viden kan bruges til at målrette opdagelsen af nye stoffer mod kultiverbare bakterier med et stort ukendt bioaktivt potentiale. iv Publications Paulsen, S. S.; Strube, M. L.; Bech, P. K.; Gram, L. & Sonnenschein, E. C. Marine chitinolytic Pseudoalteromonas represents an untapped reservoir of bioactive potential. mSystems 4, (2019). Paulsen, S. S.; Isbrandt, T.; Kirkegaard, M; Buijs, Y; Strube, M. L.; Sonnenschein, E. C.; Ostenfeld, T. & Gram, L. Production of the antimicrobial compound tetrabromopyrrole and the Pseudomonas quinolone system precursor, HHQ, by a novel marine species Pseudoalteromonas galatheae sp. nov. (Submitted to Scientific Reports). Wang, X.; Paulsen, S. S.; Isbrandt, T.; Ostenfeld, T.; Strube, M. L.; Gram, L. & Zhang, S. A conjugation-based gene knock-out
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    International Journal of Systematic and Evolutionary Microbiology (2002), 52, 263–271 Printed in Great Britain Pseudoalteromonas maricaloris sp. nov., NOTE isolated from an Australian sponge, and reclassification of [Pseudoalteromonas aurantia] NCIMB 2033 as Pseudoalteromonas flavipulchra sp. nov. 1 Pacific Institute of Elena P. Ivanova,1† Ludmila S. Shevchenko,1 Tomoo Sawabe,2 Bioorganic Chemistry of 3 4 1 the Far-Eastern Branch of Anatolii M. Lysenko, Vasilii I. Svetashev, Nataliya M. Gorshkova, the Russian Academy of Masataka Satomi,5 Richard Christen6 and Valery V. Mikhailov1 Sciences, 690022 Vladivostok, pr. 100 Let Vladivostoku 159, Russia Author for correspondence: Elena P. Ivanova. Tel: j61 3 9214 5137. Fax: j61 3 9214 5050. 2 Laboratory of e-mail: eivanova!groupwise.swin.edu.au Microbiology, Faculty of Fisheries, Hokkaido University, 3-1-1 Minato- A marine, Gram-negative, aerobic bacterium that produced cytotoxic, lemon- cho, Hakodate 041-8611, yellow, chromopeptide pigments that inhibited the development of sea urchin Japan eggs has been isolated from the Australian sponge Fascaplysinopsis reticulata 3 Institute of Microbiology Hentschel. The cells of the organism were rod-shaped with a single polar of the Russian Academy of Sciences, 117811 Moscow, flagellum and they required NaCl for growth (05–10%) with optimum growth Russia at 1–3% NaCl. The temperature for growth was 10–37 SC, with optimum growth 4 Institute of Marine Biology at 25–30 SC. Growth occurred at pH values from 60to100, with optimum of the Far-Eastern Branch growth at pH 60–80. Major phospholipids were phosphatidylethanolamine, of the Russian Academy of phosphatidylglycerol and lyso-phosphatidylethanolamine. Of 26 fatty acids Sciences, 690041 Vladivostok, Russia with 11–19 carbon atoms that were detected, 16:1ω7, 16:0, 17:1ω8 and 18:1ω7 were predominant.