A genomic perspective on a new bacterial genus and species from the Alcaligenaceae family, Basilea psittacipulmonis

BMC Genomics

Jacques Schrenzel⁴  Joachim Frey³  Paola Pilo³  Patrice François²  Laurent Farinelli⁵  Nadia Gaia²  Vladimir Lazarevic²  David Hernandez²  Katrine L Whiteson¹ 

[1] Current address: Department of Biology, San Diego State University, San Diego, CA, USA;Genomic Research Laboratory, Department of Internal Medicine, Service of Infectious Diseases, Geneva University Hospitals, Gabrielle-Perret-Gentil 4, CH-1211 Geneva 14, Switzerland;Institute of Veterinary Bacteriology, University of Bern, Länggassstrasse 122, Postfach, CH-3001 Bern, Switzerland;Clinical Microbiology Laboratory, Department of Internal Medicine, Service of Infectious Diseases, Geneva University Hospitals, Gabrielle-Perret-Gentil 4, CH-1211 Geneva 14, Switzerland;Fasteris SA, CH-1228 Plan-les-Ouates, Switzerland

关键词: Phylogenetic profile;    Genome;    High-throughput sequencing;    Parakeet;    Bacteria;   

Others  :  1217827
DOI  :  10.1186/1471-2164-15-169

 received in 2013-10-04, accepted in 2014-02-06,  发布年份 2014

【 摘 要 】

Background

A novel Gram-negative, non-haemolytic, non-motile, rod-shaped bacterium was discovered in the lungs of a dead parakeet (Melopsittacus undulatus) that was kept in captivity in a petshop in Basel, Switzerland. The organism is described with a chemotaxonomic profile and the nearly complete genome sequence obtained through the assembly of short sequence reads.

Results

Genome sequence analysis and characterization of respiratory quinones, fatty acids, polar lipids, and biochemical phenotype is presented here. Comparison of gene sequences revealed that the most similar species is Pelistega europaea, with BLAST identities of only 93% to the 16S rDNA gene, 76% identity to the rpoB gene, and a similar GC content (~43%) as the organism isolated from the parakeet, DSM 24701 (40%). The closest full genome sequences are those of Bordetella spp. and Taylorella spp. High-throughput sequencing reads from the Illumina-Solexa platform were assembled with the Edena de novo assembler to form 195 contigs comprising the ~2 Mb genome. Genome annotation with RAST, construction of phylogenetic trees with the 16S rDNA (rrs) gene sequence and the rpoB gene, and phylogenetic placement using other highly conserved marker genes with ML Tree all suggest that the bacterial species belongs to the Alcaligenaceae family. Analysis of samples from cages with healthy parakeets suggested that the newly discovered bacterial species is not widespread in parakeet living quarters.

Conclusions

Classification of this organism in the current taxonomy system requires the formation of a new genus and species. We designate the new genus Basilea and the new species psittacipulmonis. The type strain of Basilea psittacipulmonis is DSM 24701 (= CIP 110308 T, 16S rDNA gene sequence Genbank accession number JX412111 and GI 406042063).

【 授权许可】

   
2014 Whiteson et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Lepore J: It’s spreading: outbreaks, media scares, and the parrot panic of 1930. The New Yorker 2009., 46
• [2]Genome List - National Center for Biotechnology Information [http://www.ncbi.nlm.nih.gov/genome/browse/ webcite]
• [3]Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng J-F, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, et al.: A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 2009, 462(7276):1056-1060.
• [4]A Genomic Encyclopedia of Bacteria and Archaea (GEBA). [http://www.jgi.doe.gov/programs/GEBA/ webcite]
• [5]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267.
• [6]Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM: The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009, 37(Database issue):D141-D145.
• [7]Tringe SG, Hugenholtz P: A renaissance for the pioneering 16S rRNA gene. Curr Opin Microbiol 2008, 11(5):442-446.
• [8]Sebaihia M, Preston A, Maskell DJ, Kuzmiak H, Connell TD, King ND, Orndorff PE, Miyamoto DM, Thomson NR, Harris D, Goble A, Lord A, Murphy L, Quail MA, Rutter S, Squares R, Squares S, Woodward J, Parkhill J, Temple LM: Comparison of the genome sequence of the poultry pathogen Bordetella avium with those of B. bronchiseptica, B. pertussis, and B. parapertussis reveals extensive diversity in surface structures associated with host interaction. J Bacteriol 2006, 188(16):6002-6015.
• [9]Hauser H, Richter DC, van Tonder A, Clark L, Preston A: Comparative genomic analyses of the Taylorellae. Vet Microbiol 2012, 159(1–2):195-203.
• [10]Hébert L, Moumen B, Duquesne F, Breuil M-F, Laugier C, Batto J-M, Renault P, Petry S: Genome sequence of Taylorella equigenitalis MCE9, the causative agent of contagious equine metritis. J Bacteriol 2011, 193(7):1785.
• [11]Hébert L, Moumen B, Pons N, Duquesne F, Breuil M-F, Goux D, Batto J-M, Laugier C, Renault P, Petry S: Genomic characterization of the Taylorella genus. PLoS ONE 2012, 7(1):e29953.
• [12]Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D: Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct 2009, 4:13. BioMed Central Full Text
• [13]Faveri M, Mayer MP, Feres M, de Figueiredo LC, Dewhirst FE, Paster BJ: Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol 2008, 23(2):112-118.
• [14]Hernandez D, Francois P, Farinelli L, Osteras M, Schrenzel J: De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome Res 2008, 18(5):802-809.
• [15]Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O: The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75. BioMed Central Full Text
• [16]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [17]Clarke KR: Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 1993, 18(1):117-143.
• [18]Grissa I, Vergnaud G, Pourcel C: CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007, 35(Web Server issue):W52-W57.
• [19]Wu M, Ren Q, Durkin AS, Daugherty SC, Brinkac LM, Dodson RJ, Madupu R, Sullivan SA, Kolonay JF, Haft DH, Nelson WC, Tallon LJ, Jones KM, Ulrich LE, Gonzalez JM, Zhulin IB, Robb FT, Eisen JA: Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLoS Genet 2005, 1(5):e65.
• [20]Gevers D, Vandepoele K, Simillon C, Van de Peer Y: Gene duplication and biased functional retention of paralogs in bacterial genomes. Trends Microbiol 2004, 12(4):148-154.
• [21]Schloss PD, Handelsman J: Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 2005, 71(3):1501-1506.
• [22]Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J: Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 1996, 60(2):407-438.
• [23]Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J: Opinion: re-evaluating prokaryotic species. Nat Rev Microbiol 2005, 3(9):733-739.
• [24]Adékambi T, Shinnick TM, Raoult D, Drancourt M: Complete rpoB gene sequencing as a suitable supplement to DNA–DNA hybridization for bacterial species and genus delineation. Int J Syst Evol Microbiol 2008, 58(8):1807-1814.
• [25]Koski LB, Golding GB: The closest BLAST hit is often not the nearest neighbor. J Mol Evol 2001, 52(6):540-542.
• [26]Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus JC, Cattolico L, Chandler M, Choisne N, Claudel-Renard C, Cunnac S, Demange N, Gaspin C, Lavie M, Moisan A, Robert C, Saurin W, Schiex T, Siguier P, Thébault P, Whalen M, Wincker P, Levy M, Weissenbach J, Boucher CA: Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 2002, 415(6871):497-502.
• [27]Boone DR, Castenholz RW, Garrity GM: Bergey’s manual of systematic bacteriology. 2nd edition. New York: Springer; 2001.
• [28]Goodnow RA: Biology of Bordetella bronchiseptica. Microbiol Rev 1980, 44(4):722-738.
• [29]Ghosh W, George A, Agarwal A, Raj P, Alam M, Pyne P, Gupta SKD: Whole-genome shotgun sequencing of the sulfur-oxidizing chemoautotroph tetrathiobacter kashmirensis. J Bacteriol 2011, 193(19):5553-5554.
• [30]Dworkin M, Falkow S: The prokaryotes : a handbook on the biology of bacteria. 3rd edition. New York; London: Springer; 2006.
• [31]Sirand-Pugnet P, Lartigue C, Marenda M, Jacob D, Barre A, Barbe V, Schenowitz C, Mangenot S, Couloux A, Segurens B, de Daruvar A, Blanchard A, Citti C: Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet 2007, 3(5):e75.
• [32]Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen Y-J, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim J-B, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, et al.: Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437(7057):376-380.
• [33]von Mering C, Hugenholtz P, Raes J, Tringe SG, Doerks T, Jensen LJ, Ward N, Bork P: Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 2007, 315(5815):1126-1130.
• [34]Stark M, Berger SA, Stamatakis A, von Mering C: MLTreeMap - accurate Maximum Likelihood placement of environmental DNA sequences into taxonomic and functional reference phylogenies. BMC Genomics 2010, 11:461. BioMed Central Full Text
• [35]Willner D, Thurber RV, Rohwer F: Metagenomic signatures of 86 microbial and viral metagenomes. Environ Microbiol 2009, 11(7):1752-1766.
• [36]Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM: DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007, 57(Pt 1):81-91.
• [37]Konstantinidis KT, Ramette A, Tiedje JM: Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 2006, 72(11):7286-7293.
• [38]Richter M, Rosselló-Móra R: Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009, 106:19126-19131.
• [39]Kuo CH, Ochman H: The fate of new bacterial genes. FEMS Microbiol Rev 2009, 33(1):38-43.
• [40]Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA: Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19(9):1639-1645.
• [41]Rice P, Longden I, Bleasby A: EMBOSS: the European molecular biology open software suite. Trends Genet 2000, 16(6):276-277.
• [42]Aziz RK, Nizet V: Pathogen microevolution in high resolution. Sci Transl Med 2010, 2(16):16ps14.
• [43]Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, Henningham A, McArthur JD, Dinkla K, Aziz RK, Kansal RG, Simpson AJ, Buchanan JT, Chhatwal GS, Kotb M, Nizet V: DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 2007, 13(8):981-985.
• [44]Tomich M, Planet PJ, Figurski DH: The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 2007, 5(5):363-375.