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Wide Analysis Reveals That Burkholderia Contaminans MS14 ORIGINAL RESEARCH Comparative genome-­wide analysis reveals that Burkholderia contaminans MS14 possesses multiple antimicrobial biosynthesis genes but not major genetic loci required for pathogenesis Peng Deng1, Xiaoqiang Wang1, Sonya M. Baird1, Kurt C. Showmaker2, Leif Smith3, Daniel G. Peterson2 & Shien Lu1 1Departments of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi state, Mississippi 2Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi state, Mississippi 3Department of Biology, Texas A&M University, College Station, Texas Keywords Abstract Antimicrobial, Burkholderia contaminans MS14, comparative genomics, virulence, Burkholderia contaminans MS14 shows significant antimicrobial activities against whole genome sequencing. plant and animal pathogenic fungi and bacteria. The antifungal agent occidi- ofungin produced by MS14 has great potential for development of biopesticides Correspondence and pharmaceutical drugs. However, the use of Burkholderia species as biocontrol Shien Lu, Department of Biochemistry, agent in agriculture is restricted due to the difficulties in distinguishing between Molecular Biology, Entomology and Plant plant growth-­promoting bacteria and the pathogenic bacteria. The complete Pathology, Mississippi State University, MS. Tel: +1 (662) 325-3511; MS14 genome was sequenced and analyzed to find what beneficial and virulence-­ Fax: +1 (662) 325-8955; related genes it harbors. The phylogenetic relatedness of B. contaminans MS14 E-mail: [email protected] and other 17 Burkholderia species was also analyzed. To research MS14′s potential virulence, the gene regions related to the antibiotic production, antibiotic resist- Funding Information ance, and virulence were compared between MS14 and other Burkholderia This research was funded by USDA National ­genomes. The genome of B. contaminans MS14 was sequenced and annotated. Institute of Food and Agriculture NIFA to SL The genomic analyses reveal the presence of multiple gene sets for antimicrobial (MIS-401170). biosynthesis, which contribute to its antimicrobial activities. BLAST results in- Received: 11 September 2015; Revised: 22 dicate that the MS14 genome harbors a large number of unique regions. MS14 November 2015; Accepted: 3 December is closely related to another plant growth-­promoting Burkholderia strain B. lata 2015 383 according to the average nucleotide identity data. Moreover, according to the phylogenetic analysis, plant growth-­promoting species isolated from soils MicrobiologyOpen 2016; 5(3): 353–369 and mammalian pathogenic species are clustered together, respectively. MS14 has multiple antimicrobial activity-­related genes identified from the genome, doi: 10.1002/mbo3.333 but it lacks key virulence-­related gene loci found in the pathogenic strains. Additionally, plant growth-­promoting Burkholderia species have one or more antimicrobial biosynthesis genes in their genomes as compared with nonplant growth-­promoting soil-­isolated Burkholderia species. On the other hand, patho- genic species harbor multiple virulence-associated­ gene loci that are not present in nonpathogenic Burkholderia species. The MS14 genome as well as Burkholderia species genome show considerable diversity. Multiple antimicrobial agent bio- synthesis genes were identified in the genome of plant growth-promoting species of Burkholderia. In addition, by comparing to nonpathogenic Burkholderia spe- cies, pathogenic Burkholderia species have more characterized homologs of the gene loci known to contribute to pathogenicity and virulence to plant and animals. © 2016 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. 353 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Genomics of Burkholderia Contaminans MS14 P. Deng et al. Background contaminans MS14 was isolated from soil in Mississippi, it has a broad range of antifungal activities to plant and Burkholderia is a gram- negative, rod- shaped, motile, and human pathogens by producing an oligopeptide occidio- nonspore- forming bacterium that has been identified in fungin (Lu et al. 2009). It is a novel fungicide that can many diverse ecological niches (Francis et al. 2013). significantly inhibit the growth of pathogens by interfering Currently, 88 species have been recognized in the genus with cell wall synthesis or triggering apoptosis (Ellis et al. Burkholderia (De Meyer et al. 2013). The ecological ver- 2012; Emrick et al. 2013; Ravichandran et al. 2013). satility of these bacteria is likely due to their unusually Genetically, the whole length of the ocf gene cluster required large genomes, which are often comprised of one or mul- for production of occidiofungin has been characterized, tiple large replicons with plasmids (Lessie et al. 1996). which is composed of 16 ORFs (Gu et al. 2009). Among The bacterium has the ability to use a large array of carbon the 16 members of this cluster, ocfD, ocfE, ocfF, ocfH, and sources to synthesize secondary metabolites (el - Banna and ocfJ were predicted to encode nonribosomal peptide syn- Winkelmann 1998; Parke and Gurian- Sherman 2001). thesis (NRPS) or NRPS- polyketide synthase (PKS), which Most Burkholderia species isolated from soil are associ- are directly related to the biosynthesis of the antifungal ated with plants. Some species are related to the promotion compound occidiofungin. The genes ocfA, ocfC, ocfK, ocfL, of plant growth and are considered to be plant growth- ocfM, and ocfN were predicted to be involved in the secre- promoting bacteria (PGPB). For example, B. phenoliruptrix tion and modification of occidiofungin. and B. phymatum are effective in nitrogen fixing (Elliott Burkholderia cepacia complex (Bcc) is a group of et al. 2007; Zuleta et al. 2014), while B. phytofirmans Burkholderia species that some are opportunistic bacteria induces larger root systems (Sessitsch et al. 2005). Interests and could cause lung disease in immunocompromised in the use of Burkholderia species or their secondary individuals (Mahenthiralingam et al. 2005). The Bcc group metabolites in agriculture have increased. For example, composed of nine different genomovars and at least 18 the use of Burkholderia cepacia AMMDR1 could yield as different species. These species include B. cepacia, B. ceno- efficient control of “damping-off” disease caused by Pythium cepacia, B. multivorans, B. vietnamiensis, B. stabilis, species and Rhizoctonia solani as that of the fungicide B. ­ambifaria, B. dolosa, B. anthina, and B. pyrrocinia (Lipuma Captan (Heungens and Parke 2000; Parke and Gurian- 2005). B. cepacia is a common environmental species, but Sherman 2001). The relatively large Burkholderia genome is also an important human pathogen which can create harbors a large variety of antimicrobial biosynthesis genes. respiratory complications for cystic fibrosis (CF) patients Occidiofungin (Gu et al. 2011; Ellis et al. 2012) produced (Mahenthiralingam et al. 2005). B. cenocepacia is a major by B. contaminans MS14 has significant antifungal activity. CF pathogen and is responsible for 70% of the cases of Pyrrolnitrin (el -Banna and Winkelmann 1998) was first Bcc infection (Mahenthiralingam et al. 2005). B. multivorans identified as an antifungal antibiotic produced by is the second most common Bcc species in CF infection Pseudomonas species and later found to be synthesized by (Mahenthiralingam et al. 2002), and some species like B. several Burkholderia cepacia species. Pyoluteorin (Birchall dolosa strains are frequently isolated from the CF patents et al. 1970) and lipopeptide AFC- BC11 (Kang et al. 1998) (Vermis et al. 2004). Bcc infections contribute to the overall are other antibiotics produced by Burkholderia. Siderophores poor health of CF patients (Mahenthiralingam et al. 2002). are bacteriostatic agents that can inhibit pathogenic mi- It is important to be able to distinguish virulent Bcc spe- croorganism’s growth by depleting iron in the soil (Hider cies, as well as some other reported virulent Burkholderia and Kong 2010). Pyochelin (Serino et al. 1997) and orni- species such as B. pseudomallei, from the less- virulent soil- bactin (Meyer et al. 1995) are common siderophores pro- isolated Burkholderia species. duced by Burkholderia species. On the other hand, Resistance to multiple antibiotics and disinfectants is plant- pathogenic species of Burkholderia have also been very common among Burkholderia species. This antibiotic identified, such asB. gladioli and B. glumae, which infect resistance feature makes them hard to treat and is crucial rice and other horticultural plants (Stoyanova et al. 2007; for human pathogenicity of Bcc species. There are several Ham et al. 2011). The commonly produced plant- toxic mechanisms that contribute to antibiotic resistance of the secondary metabolites by Burkholderia species include poly- Bcc strains. First, efflux pumps are responsible for exclu- saccharides and other toxins, such as rice grain rot and sion of antibiotics from the cell. Secondly, some Burkholderia wilt causal agent toxoflavin (Latuasan and Berends 1961) species could significantly lower antimicrobial susceptibility and exopolysaccharide toxin cepacian (Ferreira et al. 2010) by forming biofilm (Sawasdidoln et al. 2010) or by enter- that contribute to the overall pathogenicity and success ing a nonreplicating state (Hamad
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