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Pyramidobacter Piscolens Gen. Nov., Sp. Nov., a Member of the Phylum 'Synergistetes' Isolated from the Human Oral Cavity

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Pyramidobacter Piscolens Gen. Nov., Sp. Nov., a Member of the Phylum 'Synergistetes' Isolated from the Human Oral Cavity University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in Food Science and Technology Food Science and Technology Department 2009 Pyramidobacter piscolens gen. nov., sp. nov., a member of the phylum ‘Synergistetes’ isolated from the human oral cavity Julia Downes Sonia R. Vartoukian Floyd E. Dewhirst Jacques Izard Tsute Chen See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/foodsciefacpub Part of the Food Science Commons This Article is brought to you for free and open access by the Food Science and Technology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in Food Science and Technology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Julia Downes, Sonia R. Vartoukian, Floyd E. Dewhirst, Jacques Izard, Tsute Chen, Wen-Han Yu, Iain C. Sutcliffe, and William G. Wade International Journal of Systematic and Evolutionary Microbiology (2009), 59, 972–980 DOI 10.1099/ijs.0.000364-0 Pyramidobacter piscolens gen. nov., sp. nov., a member of the phylum ‘Synergistetes’ isolated from the human oral cavity Julia Downes,1 Sonia R. Vartoukian,1 Floyd E. Dewhirst,2 Jacques Izard,2 Tsute Chen,2 Wen-Han Yu,2 Iain C. Sutcliffe3 and William G. Wade1,2 Correspondence 1King’s College London Dental Institute, Infection Research Group, London SE1 9RT, UK W. G. Wade 2Department of Molecular Genetics, The Forsyth Institute, Boston, MA 02115, USA [email protected] 3Division of Biomedical Sciences, School of Applied Sciences, Northumbria University, Newcastle upon Tyne NE1 8ST, UK Four strains of anaerobic, Gram-negative bacilli isolated from the human oral cavity were subjected to a comprehensive range of phenotypic and genotypic tests and were found to comprise a homogeneous group distinct from any species with validly published names. 16S rRNA and 23S rRNA gene sequence analyses and DNA–DNA reassociation data revealed that the strains constituted a novel group within the phylum ‘Synergistetes’ and were most closely related to Jonquetella anthropi. Two libraries of randomly cloned DNA were prepared from strain W5455T and were sequenced to provide a genome survey as a resource for metagenomic studies. A new genus and novel species, Pyramidobacter piscolens gen. nov., sp. nov., is proposed to accommodate these strains. The genus Pyramidobacter comprises strains that are anaerobic, non-motile, asaccharolytic bacilli that produce acetic and isovaleric acids and minor to trace amounts of propionic, isobutyric, succinic and phenylacetic acids as end products of metabolism. P. piscolens gen. nov., sp. nov. produced hydrogen sulphide but was otherwise largely biochemically unreactive. Growth was stimulated by the addition of glycine to broth media. The G+C content of the DNA of the type strain was 59 mol%. The type strain of Pyramidobacter piscolens sp. nov. is W5455T (5DSM 21147T5CCUG 55836T). INTRODUCTION several of these genera were initially misclassified as belonging to the ‘Firmicutes’ (Baena et al., 1999a, b, 2000; Synergistes jonesii, a species comprising Gram-negative, Menes & Muxi, 2002; Zavarzina et al., 2000). The anaerobic rods, isolated from goat rumen (Allison et al., neighbouring phylum contains organisms of the genera 1992) was originally thought to be the sole representative Deferribacter and Flexistipes, among others, and has of a novel division, ‘Synergistes’ of the domain Bacteria therefore been referred to as ‘Deferribacter’or‘Flexistipes’. (Hugenholtz et al., 1998). Subsequently, however, a number of other genera, including Aminobacterium, Although ‘Synergistes’ is distinct from this neighbouring Aminomonas, Aminiphilus, Anaerobaculum, Dethiosul- phylum, the Bergey’s Manual and NCBI taxonomic fovibrio, Jonquetella, Thermanaerovibrio and Thermovirga, schemes currently, and incorrectly, lump these groups were shown to belong to this group (Hugenholtz, 2002; together as ‘Deferribacter’. No formal phylum name has Jumas-Bilak et al., 2007; Vartoukian et al., 2007), although been proposed for the group currently known as ‘Synergistes’, although the names ‘Aminanaerobia’ Abbreviations: FAME, fatty acid methyl ester; IS, insertion sequence; (Warnecke et al., 2007) and ‘Synergistetes’ have been ORF, open reading frame. suggested (Jumas-Bilak et al., 2007). For the purposes of The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene this article, we will use ‘Synergistetes’, as its relationship sequences of strains W5455T, AHN 11662 and P4G_18 are with ‘Synergistes’ is obvious and has an appropriate EU309492, EU309493 and AY207056, respectively. phylum-level construction. Tables showing the 16S–23S rRNA gene intervening sequences and Culture-independent molecular methods based on 16S 23S rRNA primers, and fatty acid methyl ester profiles of strains of rRNA gene sequences have been used widely to characterize Pyramidobacter piscolens gen. nov., sp. nov., Jonquetella anthropi and Dethiosulfovibrio peptidovorans and static annotations of partial and full- bacterial communities associated with a wide range of length open reading frames in genomic libraries 1 and 2 are available as environmental habitats and habitats associated with supplementary material with the online version of this paper. human and animal diseases. In one such study, a 16S 972 000364 G 2009 IUMS Printed in Great Britain Pyramidobacter piscolens gen. nov., sp. nov. rRNA gene library constructed from subgingival bacterial (bioMe´rieux), according to the manufacturer’s instructions, with plaque from a patient with refractory periodontal disease bacteria harvested from Columbia agar plates (LabM) supplemented contained a novel clone, BA121, representing a novel taxon with 5 % horse blood; the test was performed in triplicate. Susceptibility to amoxicillin (10 mg), ampicillin (2 mg), cefoxitin in the phylum ‘Synergistetes’ (Paster et al., 2001). (10 mg), ciprofloxacin (5 mg), clindamycin (2 mg), gentamicin Subsequently, we identified 18 clones with essentially an (10 mg), metronidazole (5 mg), penicillin (1.5 units), tetracycline identical sequence in five libraries from individuals with (5 mg) and trimethoprim (2.5 mg) was investigated using a disc- acute ulcerative necrotizing gingivitis, advanced caries or diffusion method and Iso-Sensitest agar with 5 % horse blood endodontic infections (Munson et al., 2002, 2004; F. E. (Oxoid). Zones of inhibition of ¢30 mm in diameter were recorded Dewhirst, unpublished data), suggesting that this novel as representing antibiotic susceptibility, whereas the absence of zones of inhibition around the 7 mm discs was designated as representing taxon is a true member of the human oral microbiome. antibiotic resistance. The isolation of four strains with essentially identical 16S rRNA gene sequences from samples associated with oral Growth at 25, 30, 37 and 42 uC was assessed using PY medium. infections now allows the characterization of a species Utilization of amino acids was determined by adding alanine, arginine, cysteine, glycine, leucine and lysine (each at 10 mM) to previously known only as a clone phylotype. Because the both DP (Magot et al., 1997) and PY media. Growth was measured only gene sequences currently available for any organism of for up to 10 days by means of spectrophotometric measurement of the ‘Synergistetes’ phylum are 16S rRNA sequences, we turbidity at 580 nm. The requirement of NaCl (3 %) for growth and undertook a genome survey using shotgun sequencing to the utilization of thiosulphate, sulphate and sulphite were investigated get a genomic ‘snapshot’ of this poorly studied phylum to by adding 20 mM of the sodium salt of each compound to DP obtain additional sequence data that might be of medium prior to incubation at 37 uC. The cellular fatty acid composition was determined using acid-catalysed methanolysis to phylogenetic and taxonomic interest and also provide a release fatty acid methyl esters (FAMEs) from lyophilized whole cells, resource for metagenomic studies. as described previously (Sutcliffe, 2000). The FAMEs were extracted into hexane and concentrated under nitrogen gas before being analysed using GC (Sutcliffe, 2000). FAMEs were identified by METHODS comparison with authentic FAME standards (Sigma). Bacterial strains and growth conditions. Strains W5455T and Genetic analyses. The DNA G+C contents of strains W5455T and AHN 11662 were isolated from odontogenic abscesses, strain P4G_18 AHN 11662 were determined using an HPLC method as described was from an inflamed gingival crevice and strain D031B-08-1 was previously (Wade et al., 1999). The base composition was also from a periodontal pocket. Strain AHN 11662 was donated by the late estimated from the genome survey nucleic acid sequence data, by Dr H. Jousimies-Somer of the Anaerobe Reference Laboratory, direct counting. A thermal denaturation method (Huß et al., 1983) National Public Health Institute, Helsinki, Finland, and strain was used to determine the extent of DNA–DNA relatedness between D031B-08-1 came from the Virginia Polytechnic Institute Anaerobe the strains. Laboratory collection of L. V. H. Moore and the late W. E. C. Moore and was kindly made available by Dr A. Tanner. Jonquetella anthropi The 16S rRNA genes of the four strains were sequenced as described ADV 126T was obtained from the CCUG (CCUG 53819T) and J. previously (Downes et al., 2005). Sequences were assembled using the anthropi E3_33 was isolated from an infected
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