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Elucidation of the Burkholderia Cenocepacia Hopanoid Biosynthesis Pathway Uncovers Functions for Conserved Proteins in Hopanoid- Producing Bacteria Schmerk, C

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Elucidation of the Burkholderia Cenocepacia Hopanoid Biosynthesis Pathway Uncovers Functions for Conserved Proteins in Hopanoid- Producing Bacteria Schmerk, C Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid- producing bacteria Schmerk, C. L., Welander, P. V., Hamad, M. A., Bain, K. L., Bernards, M. A., Summons, R. E., & Valvano, M. A. (2015). Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria. Environmental Microbiology, 17(3), 735-750. https://doi.org/10.1111/1462-2920.12509 Published in: Environmental Microbiology Document Version: Early version, also known as pre-print Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights © 2015 The Authors This is the pre-peer reviewed version of the following article: Schmerk, C. L., Welander, P. V., Hamad, M. A., Bain, K. L., Bernards, M. A., Summons, R. E. and Valvano, M. A. (2015), Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers functions for conserved proteins in hopanoid-producing bacteria. Environmental Microbiology, 17: 735–750, which has been published in final form at http://onlinelibrary.wiley.com/wol1/doi/10.1111/1462-2920.12509/abstract. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:01. Oct. 2021 1 Elucidation of the Burkholderia cenocepacia hopanoid biosynthesis pathway uncovers 2 functions for conserved proteins in hopanoid-producing bacteria 3 4 Crystal L. Schmerk,1 Paula V. Welander,2 Mohamad A. Hamad,1 Katie L. Bain,1 Mark A. 5 Bernards, 3 Roger E. Summons,4 Miguel A. Valvano1,5* 6 7 1 Department of Microbiology and Immunology, University of Western Ontario, London, Ontario, 8 N6A 5C1, Canada. 9 2 Department of Environmental Earth System Science, Stanford University, Stanford, California, 10 United States. 11 3 Department of Biology, University of Western Ontario, London, Ontario, N6A 5C1, Canada. 12 4 Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, 13 Cambridge, Massachusetts, United States. 14 5 Centre for Infection and Immunity, Queen's University Belfast, Belfast, BT9 5AE, United Kingdom. 15 16 17 18 19 20 Running title: Hopanoid Biosynthesis in B. cenocepacia K56-2 21 22 23 24 25 26 * For correspondence. E-mail: [email protected]; Tel. (+44) 28 9097 2878; Fax: (+44) 28 9097 27 2671. 28 29 30 Summary 31 Hopanoids are bacterial surrogates of eukaryotic membrane sterols and among earth's most 32 abundant natural products. Their molecular fossils remain in sediments spanning more than a 33 billion years. However, hopanoid metabolism and function are not fully understood. 34 Burkholderia species are environmental opportunistic pathogens that produce hopanoids and 35 also occupy diverse ecological niches. We investigated hopanoids biosynthesis in B. cenocepacia 36 by deletion mutagenesis and structural characterization of the hopanoids produced by the 37 mutants. The enzymes encoded by hpnH and hpnG were essential for production of all C35 38 extended hopanoids, including bacteriohopanetetrol (BHT), BHT glucosamine and BHT cyclitol 39 ether. Deletion of hpnI resulted in BHT production, while ΔhpnJ produced only BHT 40 glucosamine. Thus, HpnI is required for BHT glucosamine production while HpnJ is 41 responsible for its conversion to the cyclitol ether. The ΔhpnH and ΔhpnG mutants could not 42 grow under any stress condition tested, whereas ΔhpnI, ΔhpnJ, and ΔhpnK displayed wild type 43 growth rates when exposed to detergent, but varying levels of sensitivity to low pH and 44 polymyxin B. This study not only elucidates the biosynthetic pathway of hopanoids in B. 45 cenocepacia, but also uncovers a biosynthetic role for the conserved proteins HpnI, HpnJ, and 46 HpnK in other hopanoid-producing bacteria. 47 48 Keywords: hopanoids/Burkholderia cenocepacia/membrane permeability 49 50 51 2 52 Introduction 53 Hopanoids are bacterial membrane lipids ubiquitous in modern day environments dominated by 54 microbes and readily preserved in ancient sedimentary rock (Ourisson and Albrecht, 1992), making 55 them ideal tools for reconstructing and understanding microbial ecosystems (Brocks et al., 2004; 56 Summons and Lincoln, 2012). Due to size and structural similarities, hopanoids are considered 57 bacterial surrogates of eukaryotic sterols, possibly regulating the fluidity and permeability of the 58 bacterial membrane (Ourisson et al., 1987; Kannenberg, 1999). Only recently have studies focused on 59 determining the biological function of hopanoids using genetic manipulation and in vivo 60 experimentation. Such studies confirm that hopanoids are involved in enhancing the stability and 61 impermeability of the bacterial membrane, conferring resistance to multiple stress conditions 62 including pH, temperature, and exposure to detergents and antibiotics (Doughty et al., 2009; Welander 63 et al., 2009; Schmerk et al., 2011; Malott et al., 2012). However, it remains unclear what functional 64 importance can be ascribed to particular variations in the hopanoid core and side chain structures. 65 Hopanoids in lower eukaryotes and bacteria are derived from the direct cyclization of squalene 66 (Rohmer et al., 1984; Ochs et al., 1992), which results in a pentacyclic triterpenoid core commonly 67 modified by unsaturation, methylation and/or the addition of diverse C5 ribose-derived side chains 68 (Flesch and Rohmer, 1988; Rohmer, 1993). To date, few studies have successfully investigated the 69 genes or proteins involved in modifying the hopanoid core. HpnP and HpnR have been identified as 70 the radical S-adenosylmethionine (SAM) enzymes responsible for production of 2- and 3- 71 methylhopanoids, respectively (Welander et al., 2010; Welander and Summons, 2012). The 72 production of C-3 methylated hopanoids is important for late stationary survival and maintenance of 73 intracytoplasmic membranes in Methylococcus capsulatus (Welander and Summons, 2012), while the 74 production of C-2 methylated hopanoids is important for stress tolerance (Welander and Summons, 75 2012; Kulkarni et al., 2013). Hopanoids with C35 extended side chains are common among hopanoid 76 producers, but little is known about their biosynthesis or their function(s). The B-12 binding radical 77 SAM protein HpnH and the nucleoside phosphorylase HpnG catalyze the first and second steps in 78 hopanoid side chain biosynthesis, respectively (Bradley et al., 2010; Welander et al., 2012b). In 79 Rhodopseudomonas palustris, the deletion of hpnH resulted in a strain only capable of producing C30 3 80 hopanoids, and with compromised integrity of the outer membrane (Welander et al., 2012b). These 81 discoveries have provided much needed insight into the initiation of C35 hopanoid production; 82 however, the additional enzymes involved in side chain biosynthesis and the specific role that 83 different functionalized hopanoids play in membrane stability and stress tolerance remain to be 84 elucidated. 85 Burkholderia cenocepacia is one of the 17 species of genetically related bacteria known as the B. 86 cepacia complex (Bcc). These bacteria are widely spread in aquatic and soil environments where they 87 play beneficial roles including the promotion of plant growth and the degradation of pollutants 88 (Coenye and Vandamme, 2003). Bcc bacteria are also opportunistic pathogens, causing infections in 89 cystic fibrosis patients and other immune-compromised individuals (Vandamme et al., 1997; Speert, 90 2002). Given their particular environmental niche, it is not surprising that Burkholderia species are 91 intrinsically resistant to most clinically relevant antibiotics and antimicrobial peptides (Waters and 92 Ratjen, 2006; Loutet and Valvano, 2011). Resistance to antimicrobials depends, in part, on the 93 production of hopanoids (Schmerk et al., 2011). The deletion of both squalene-hopene cyclase (Shc) 94 encoding genes in B. cenocepacia K56-2 resulted in a strain (Δshc) that could not produce hopanoids 95 and displayed increased sensitivity to low pH, detergent, and various antibiotics. The mutant was also 96 unable to produce flagella, resulting in severely diminished motility (Schmerk et al., 2011). Several 97 Burkholderia species produce various C35 extended hopanoids, including bacteriohopanetetrol (BHT), 98 BHT glucosamine, and BHT cyclitol ether; however, the functional importance of these individual 99 hopanoids has not been explored (Cvejic et al., 2000; Talbot et al., 2007b). 100 This study identifies the types of extended hopanoids produced by B. cenocepacia and utilizes 101 genetic tools to generate a collection of mutants in predicted hopanoid biosynthetic genes. 102 Environmental stress tests performed with the mutants lead to new suggestions about the
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