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Genomic Characterization of Six Novel Bacillus Pumilus Bacteriophages

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Genomic Characterization of Six Novel Bacillus Pumilus Bacteriophages View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Virology 444 (2013) 374–383 Contents lists available at ScienceDirect Virology journal homepage: www.elsevier.com/locate/yviro Genomic characterization of six novel Bacillus pumilus bacteriophages Laura Lorenz a, Bridget Lins b, Jonathan Barrett a, Andrew Montgomery a, Stephanie Trapani a, Anne Schindler a, Gail E. Christie c, Steven G. Cresawn d, Louise Temple a,n a Department of Integrated Science and Technology, James Madison University, Harrisonburg, VA 22807, USA b Department of Biochemistry and Molecular biology, College of Medicine, University of Florida, Gainesville, FL 32610, USA c Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, VA 23298, USA d Department of Biology, James Madison University, Harrisonburg, VA 22807, USA article info abstract Article history: Twenty-eight bacteriophages infecting the local host Bacillus pumilus BL-8 were isolated, purified, and Received 1 March 2013 characterized. Nine genomes were sequenced, of which six were annotated and are the first of this host Returned to author for revisions submitted to the public record. The 28 phages were divided into two groups by sequence and 7 April 2013 morphological similarity, yielding 27 cluster BpA phages and 1 cluster BpB phage, which is a BL-8 Accepted 4 July 2013 prophage. Most of the BpA phages have a host range restricted to distantly related strains, B. pumilus and Available online 30 July 2013 B. simplex,reflecting the complexities of Bacillus taxonomy. Despite isolation over wide geographic and Keywords: temporal space, the six cluster BpA phages share most of their 23 functionally annotated protein features Bacillus pumilus and show a high degree of sequence similarity, which is unique among phages of the Bacillus genera. This Bacteriophage is the first report of B. pumilus phages since 1981. Genomics & 2013 Elsevier Inc. All rights reserved. Host range Bacillus taxonomy Introduction 1999). B. pumilus spores have been shown to survive in extreme environments, even in spacecraft and space-related facilities after The genus Bacillus contains a diverse group of 165 bacterial strict sterilization techniques (La Duc et al., 2004). The only fully species that are generally Gram-positive, aerobic sporeformers sequenced and assembled B. pumilus genome, strain SAFR-032, (Logan and Halket, 2011). The wide range of phenotypic diversity was isolated from a spacecraft in an assembly facility and showed and ecological origin of species in this genus has complicated resistance up to three times the concentration of hydrogen Bacillus taxonomy; for example, the Bacillus cereus group, com- peroxide and 7.5 times the concentration of UV exposure than prised of the six species B. cereus, Bacillus thuringiensis, Bacillus related Bacillus species (Gioia et al., 2007). anthracis, Bacillus mycoides, Bacillus pseudomycoides, and Bacillus A number of bacteriophages (phages) in the genus Bacillus have weihenstephanensis, do not resolve by 16S rDNA sequence analysis been described. Bacteriophages are arguably the most abundant but show high phenotypic variability (Maughan and Van, 2011). organisms on Earth, with an estimated global population of 1031 Despite difficulties in classifying taxonomy, a number of specific phage particles, and the potential genetic diversity is nearly Bacillus species are used in industry, i.e. in molecule production limitless (Hatfull et al., 2010). Phages are utilized in applications and food fermentation. In addition, two Bacillus species infect as diverse as therapy for human bacterial infections, biocontrol of humans; B. cereus and B. anthracis are the causative agents of food- pathogens on produce or animal products, gene or vaccine borne illness and anthrax, respectively. A number of other Bacillus delivery systems, protein display systems, and bacterial typing species have intermittently been implicated in food-associated (Haq et al., 2012). Bacillus species phages show great diversity in illness, including Bacillus licheniformis, Bacillus subtilis, and Bacillus morphology, sequence length, sequence content, and host range, pumilus (From et al., 2007; Logan, 2012; Salkinoja-Salonen et al., reflecting the high variability among and within species in this genus. Sequenced phage records exist in the GenBank database for B. anthracis, B. subtilis, B. thuringiensis, Bacillus clarkii, and B. cereus, n Correspondence to: MSC 4415, 701 Carrier Drive, Harrisonburg, VA 22807, USA. including the extensively studied superfamily reference phages E-mail addresses: [email protected] (L. Lorenz), [email protected] SPO1 and φ29 (Klumpp et al., 2010; Meijer et al., 2001) 2010 and (B. Lins), [email protected] (J. Barrett), [email protected] B. anthracis typing phage Gamma (Abshire et al., 2005). Prior to (A. Montgomery), [email protected] (S. Trapani), [email protected] (A. Schindler), [email protected] (G.E. Christie), this study, at least 33 other B. pumilus phages were reported [email protected] (S.G. Cresawn), [email protected] (L. Temple). (Bramucci et al., 1977; Reanney and Teh, 1976; van Elsas and 0042-6822/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.virol.2013.07.004 L. Lorenz et al. / Virology 444 (2013) 374–383 375 Penido, 1981), but none have been sequenced and the latest study Finn ranged between 49,259 and 50,161 bp in length and between was published in 1981 (van Elsas and Penido, 1981). 75 and 79 number of genes, and contain a terminal redundancy In this study, 28 B. pumilus phages were isolated, purified, and between 794 and 852 bp. These and other genometrics of the characterized. Nine genomes were sequenced, and the annotation Cluster BpA phages are described in Table 2. The accessioned of six of them is described here. This report is the first genomic Cluster BpA phages, Andromeda, Taylor, Eoghan, Gemini, Curly, analysis of B. pumilus phages and nearly doubles the number of and Finn, were annotated and their gene organization analyzed. B. pumilus phage isolates shown in the literature. Putative functions were described for 23 genes in each genome and they showed similar organizational structure to each other, schematically depicted in Fig. 2. Results The Cluster BpB phage, Pleiades, was uncovered as a separate contig in the Polaris (Cluster BpA phage) sequence assembly and Isolation and characterization of novel B. pumilus phages visualized as a podovirus by electron microscopy of lysates resulting from infection with Cluster BpA phages (Fig. 1). Pleiades Twenty-eight phages (Table 1) were isolated from various soil was discovered to exist as a prophage when Pleiades-specific samples over a period of four years using the locally isolated host primers produced amplicons in samples of B. pumilus BL-8 B. pumilus BL-8. Viral morphology of 21 of the phages was genomic DNA (Fig. 3). Pleiades appears to be uninducible by either visualized by negative stain transmission electron microscopy. UV or mitomicin-C; however, no sensitive strain for plaque The siphoviridae morphotype was observed for 20 of the imaged tests exists for Pleiades, hampering efforts at further analysis. phages and the podoviridae for one phage. Representative TEM Preliminary experiments with additional B. pumilus strains images are depicted in Fig. 1. Nine of the isolated phages were revealed a dependence of Cluster BpA phage infection on the sequenced. Six of these sequenced phages (Andromeda, Taylor, presence of a similar prophage in partially sequenced strain ATCC Eoghan, Gemini, Finn, Curly) have been annotated and accessioned 7061 (accession number ABRX00000000.1) (data not shown). in the GenBank database. The final three sequenced phages Pleiades-specific sequences have been found in varying ratios in (Pleiades, Polaris, and BC) are in varying stages of sequence all of the Cluster BpA phage sequence assemblies, suggesting there finishing and annotation. is some relationship between Cluster BpA phage infection and expression of the BL-8 prophage; these studies are ongoing. Analysis of the sequenced phages Genome organization and annotation of the finished cluster Genome comparisons of the nine sequenced genomes yielded BpA phages two groups of genomically distinct phages: the Cluster BpA phages (Andromeda, Taylor, Eoghan, Gemini, Curly, Finn, BC, and Polaris) The six accessioned Cluster BpA phages showed a uniform and the Cluster BpB phage, Pleiades. The sequenced Cluster BpA structural organization consisting of three putative gene cassettes phages shared an average of 82% genome similarity to each other. for structural genes, lysis genes, and replication genes, based on The genomes of Andromeda, Taylor, Eoghan, Gemini, Curly, and the 23 functionally annotated features. All genomes began with a Table 1 Isolation information of the 28 phages presented in this study ordered by isolation date. Shaded rows are phages that have been sequenced. All phages except for phages Taylor and Eoghan came from distinct soil samples. Name Isolation date Isolation source GPS coordinates Polarisa 2008 Greenhouse soil, JMU campus 38.439329, À78.872169 Pleiades 2008 Greenhouse soil, JMU campus 38.439329, À78.872169 BC a 2008 Greenhouse soil, JMU campus 38.439329, À78.872169 JG a 2008 Greenhouse soil, JMU campus 38.439329, À78.872169 Leonitasa 2008 Greenhouse soil, JMU campus 38.439329, À78.872169 Andromeda a 2009 Grassy area, Harrisonburg VA 38.4234667, À78.8846667
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