Defining bacterial species in the genomic era: insights from the genus Acinetobacter

BMC Microbiology - Tập 12 Số 1 - 2012
Jacqueline Chan1, Mihail Halachev1, Nicholas J. Loman1, Chrystala Constantinidou1, Mark J. Pallen1
1Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, B15 2TT, UK

Tóm tắt

Abstract Background Microbial taxonomy remains a conservative discipline, relying on phenotypic information derived from growth in pure culture and techniques that are time-consuming and difficult to standardize, particularly when compared to the ease of modern high-throughput genome sequencing. Here, drawing on the genus Acinetobacter as a test case, we examine whether bacterial taxonomy could abandon phenotypic approaches and DNA-DNA hybridization and, instead, rely exclusively on analyses of genome sequence data. Results In pursuit of this goal, we generated a set of thirteen new draft genome sequences, representing ten species, combined them with other publically available genome sequences and analyzed these 38 strains belonging to the genus. We found that analyses based on 16S rRNA gene sequences were not capable of delineating accepted species. However, a core genome phylogenetic tree proved consistent with the currently accepted taxonomy of the genus, while also identifying three misclassifications of strains in collections or databases. Among rapid distance-based methods, we found average-nucleotide identity (ANI) analyses delivered results consistent with traditional and phylogenetic classifications, whereas gene content based approaches appear to be too strongly influenced by the effects of horizontal gene transfer to agree with previously accepted species. Conclusion We believe a combination of core genome phylogenetic analysis and ANI provides an appropriate method for bacterial species delineation, whereby bacterial species are defined as monophyletic groups of isolates with genomes that exhibit at least 95% pair-wise ANI. The proposed method is backwards compatible; it provides a scalable and uniform approach that works for both culturable and non-culturable species; is faster and cheaper than traditional taxonomic methods; is easily replicable and transferable among research institutions; and lastly, falls in line with Darwin’s vision of classification becoming, as far as is possible, genealogical.

Từ khóa


Tài liệu tham khảo

Linnaeus C: Systema naturæ, sive regna tria naturæ systematice proposita per classes, ordines, genera, & species. 1735, Leiden: Apud Theodorum Haak

Darwin C: On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1859, London: John Murray, Albemarle Street

Godreuil S, Cohan F, Shah H, Tibayrenc M: Which species concept for pathogenic bacteria?: An E-Debate. Infect Genet Evol. 2005, 5: 375-387. 10.1016/j.meegid.2004.03.004.

Konstantinidis KT, Ramette A, Tiedje JM: The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci. 2006, 361: 1929-1940. 10.1098/rstb.2006.1920.

Van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M, for the European Society of Clinical M, Infectious Diseases Study Group on Epidemiological M: Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect. 2007, 13: 1-46.

Sneath PHA, Sokal RR: Numerical taxonomy: The principles and practice of numerical classification. 1973, San Francisco: W. H. Freeman

Lee KY, Wahl R, Barbu E: Contenu en bases purique et pyrimidiques des acides deoxyribonucleiques des bacteries. Ann Inst Pasteur. 1956, 91: 212-224.

Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Truper HG: Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol. 1987, 37: 463-464.

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: 733-739. 10.1038/nrmicro1236.

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: 81-91. 10.1099/ijs.0.64483-0.

Rosselló-Mora R, Amann R: The species concept for prokaryotes. FEMS Microbiol Rev. 2001, 25: 39-67.

Rappé MS, Giovannoni SJ: The uncultured microbial majority. Annu Rev Microbiol. 2003, 57: 369-394. 10.1146/annurev.micro.57.030502.090759.

Eisen JA, Fraser CM: Phylogenomics: intersection of evolution and genomics. Science. 2003, 300: 1706-1707. 10.1126/science.1086292.

Konstantinidis KT, Tiedje JM: Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol. 2007, 10: 504-509. 10.1016/j.mib.2007.08.006.

Jolley KA, Bliss CM, Bennet JS, Bratcher HB, Brehoney CM, Colles FM, Wimalarathna HM, Harrison OB, Sheppard SK, Cody AJ, Maiden MCJ: Ribosomal multi-locus sequence typing: universal characterisation of bacteria from domain to strain. Microbiology. 2012, 158: 1005-1015. 10.1099/mic.0.055459-0.

Coenye T, Gevers D, de Peer YV, Vandamme P, Swings J: Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev. 2005, 29: 147-167.

Thompson C, Vicente A, Souza R, Vasconcelos A, Vesth T, Alves N, Ussery D, Iida T, Thompson F: Genomic taxonomy of Vibrios. BMC Evol Biol. 2009, 9: 258-10.1186/1471-2148-9-258.

Thompson CC, Vieira NM, Vicente ACP, Thompson FL: Towards a genome based taxonomy of Mycoplasmas. Infect Genet Evol. 2011, 11: 1798-1804. 10.1016/j.meegid.2011.07.020.

Ibrahim A, Gerner-Smidt P, Liesack W: Phylogenetic relationship of the twenty-One DNA groups of the genus Acinetobacter as revealed by 16S ribosomal DNA sequence analysis. Int J Syst Evol Microbiol. 1997, 47: 837-841.

Janda JM, Abbott SL: 16S RRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol. 2007, 45: 2761-2764. 10.1128/JCM.01228-07.

Fox GE, Wisotzkey JD, Jurtshuk P: How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Evol Microbiol. 1992, 42: 166-170.

Brisou J, Prevot AR: Etudes de systematique bacterienne. X. Revision des especes reunies dans le genre Achromobacter. Ann Inst Pasteur. 1954, 86: 722-728.

Baumann P, Doudoroff M, Stanier RY: A study of the Moraxella group II. Oxidative-negative species (genus Acinetobacter). J Bacteriol. 1968, 95: 1520-1541.

Peleg AY, Seifert H, Paterson DL: Acinetobacter baumannii: Emergence of a Successful Pathogen. Clin Microbiol Rev. 2008, 21: 538-582. 10.1128/CMR.00058-07.

Lorenz MG, Reipschlager K, Wackernagel W: Plasmid transformation of naturally competent Acinetobacter calcoaceticus in non-sterile soil extract and groundwater. Arch Microbiol. 1992, 157: 355-360. 10.1007/BF00248681.

Poirel L, Figueiredo S, Cattoir V, Carattoli A, Nordmann P: Acinetobacter radioresistens as a silent source of carbapenem resistance for Acinetobacter spp. Antimicrob Agents Chemother. 2008, 52: 1252-1256. 10.1128/AAC.01304-07.

Vaneechoutte M, Young DM, Ornston LN, De Baere T, Nemec A, Van Der Reijden T, Carr E, Tjernberg I, Dijkshoorn L: Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl Environ Microbiol. 2006, 72: 932-936. 10.1128/AEM.72.1.932-936.2006.

Baumann P: Isolation of Acinetobacter from soil and water. J Bacteriol. 1968, 96: 39-42.

Jung J, Park W, Baek JH: Complete genome sequence of the diesel-degrading Acinetobacter sp. strain DR1. J Bacteriol. 2010, 192: 4794-4795. 10.1128/JB.00722-10.

Zhan Y, Yu H, Yan Y, Chen M, Lu W, Li S, Peng Z, Zhang W, Ping S, Wang J, Lin M: Genes involved in the benzoate catabolic pathway in Acinetobacter calcoaceticus PHEA-2. Curr Microbiol. 2008, 57: 609-614. 10.1007/s00284-008-9251-4.

Park YS, Lee H, Lee KS, Hwang SS, Cho YK, Kim HY, Uh Y, Chin BS, Han SH, Jeong SH, Lee K, Kim JM: Extensively drug-resistant Acinetobacter baumannii: risk factors for acquisition and prevalent OXA-type carbapenemases—a multicentre study. Int J Antimicrob Ag. 2010, 36: 430-435. 10.1016/j.ijantimicag.2010.06.049.

Grosso F, Quinteira S, Peixe L: Emergence of an extreme-drug-resistant (XDR) Acinetobacter baumannii carrying blaOXA-23 in a patient with acute necrohaemorrhagic pancreatitis. J Hosp Infect. 2010, 75: 82-83. 10.1016/j.jhin.2010.01.007.

Turton JF, Shah J, Ozongwu C, Pike R: Incidence of Acinetobacter species other than A. baumannii among clinical isolates of Acinetobacter: Evidence for emerging species. J Clin Microbiol. 2010, 48: 1445-1449. 10.1128/JCM.02467-09.

Gerner-Smidt P, Tjernberg I, Ursing J: Reliability of phenotypic tests for identification of Acinetobacter species. J Clin Microbiol. 1991, 29: 277-282.

Janssen P, Maquelin K, Coopman R, Tjernberg I, Bouvet P, Kersters K, Dijkshoorn L: Discrimination of Acinetobacter Genomic Species by AFLP Fingerprinting. Int J Syst Bacteriol. 1997, 47: 1179-1187. 10.1099/00207713-47-4-1179.

Janssen P, Coopman R, Huys G, Swings J, Bleeker M, Vos P, Zabeau M, Kersters K: Evaluation of the DNA fingerprinting method AFLP as a new tool in bacterial taxonomy. Microbiology. 1996, 142: 1881-1893. 10.1099/13500872-142-7-1881.

Dijkshoorn L, van Harsselaar B, Tjernberg I, Bouvet PJM, Vaneechoutte M: Evaluation of Amplified Ribosomal DNA Restriction Analysis for Identification of Acinetobacter Genomic Species. Syst Appl Microbiol. 1998, 21: 33-39. 10.1016/S0723-2020(98)80006-4.

Vaneechoutte M, Dijkshoorn L, Tjernberg I, Elaichouni A, de Vos P, Claeys G, Verschraegen G: Identification of Acinetobacter genomic species by amplified ribosomal DNA restriction analysis. J Clin Microbiol. 1995, 33: 11-15.

Nemec A, Krizova L, Maixnerova M, van der Reijden TJK, Deschaght P, Passet V, Vaneechoutte M, Brisse S, Dijkshoorn L: Genotypic and phenotypic characterization of the Acinetobacter calcoaceticus-Acinetobacter baumannii complex with the proposal of Acinetobacter pittii sp. nov. (formerly Acinetobacter genomic species 3) and Acinetobacter nosocomialis sp. nov. (formerly Acinetobacter genomic species 13TU). Res Microbiol. 2011, 162: 393-404. 10.1016/j.resmic.2011.02.006.

Nemec A, De Baere T, Tjernberg I, Vaneechoutte M, van der Reijden TJ, Dijkshoorn L: Acinetobacter ursingii sp. nov. and Acinetobacter schindleri sp. nov., isolated from human clinical specimens. Int J Syst Evol Microbiol. 2001, 51: 1891-1899. 10.1099/00207713-51-5-1891.

Bonnin RA, Poirel L, Nordmann P: AbaR-type transposon structures in Acinetobacter baumannii. J Antimicrob Chemother. 2012, 67: 234-236. 10.1093/jac/dkr413.

Bouvet PJM, Grimont PAD: Taxonomy of the Genus Acinetobacter with the Recognition of Acinetobacter baumannii sp. nov., Acinetobacter haemolyticus sp. nov., Acinetobacter johnsonii sp. nov., and Acinetobacter junii sp. nov. and Emended Descriptions of Acinetobacter calcoaceticus and Acinetobacter lwoffii. Int J Syst Evol Microbiol. 1986, 36: 228-240.

Kim Y-O, Kim W-J, Choi S-H, Kim D-S, Kim D-W, Lee J-S, Kong HJ, Nam B-H, Kim B-S, Lee S-J, Park H-S, Chae S-H: Genome Sequence of Acinetobacter sp. Strain P8–3–8, Isolated from Fistularia commersonii in Vietnam. J Bacteriol. 2011, 193: 4288-4289. 10.1128/JB.05333-11.

Heuer H, Kopmann C, Binh CTT, Top EM, Smalla K: Spreading antibiotic resistance through spread manure: characteristics of a novel plasmid type with low %G+C content. Environ Microbiol. 2009, 11: 937-949. 10.1111/j.1462-2920.2008.01819.x.

Nemec A, Dijkshoorn L, Cleenwerck I, De Baere T, Janssens D, van der Reijden TJK, Jezek P, Vaneechoutte M: Acinetobacter parvus sp. nov., a small-colony-forming species isolated from human clinical specimens. Int J Syst Evol Microbiol. 2003, 53: 1563-1567. 10.1099/ijs.0.02631-0.

Lima-Mendez G, Van Helden J, Toussaint A, Leplae R: Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics. 2008, 24: 863-865. 10.1093/bioinformatics/btn043.

Nemec A, Musílek M, Šedo O, De Baere T, Maixnerová M, van der Reijden TJK, Zdráhal Z, Vaneechoutte M, Dijkshoorn L: Acinetobacter bereziniae sp. nov. and Acinetobacter guillouiae sp. nov., to accommodate Acinetobacter genomic species 10 and 11, respectively. Int J Syst Evol Microbiol. 2010, 60: 896-903. 10.1099/ijs.0.013656-0.

Nishimura Y, Ino T, Iizuka H: Acinetobacter radioresistens sp. nov. Isolated from Cotton and Soil. Int J Syst Evol Microbiol. 1988, 38: 209-211.

Pessione E, Giunta C: Acinetobacter radioresistens metabolizing aromatic compounds. 2. Biochemical and microbiological characterization of the strain. Microbios. 1997, 89: 105-117.

Stackebrandt E, Goebel BM: Taxonomic note: A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol. 1994, 44: 846-849.

Keswani J, Whitman WB: Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. Int J Syst Evol Microbiol. 2001, 51: 667-678.

Stackebrandt E, Ebers J: Taxonomic parameters revisited: tarnished gold standards. Microbiol Today. 2006, 33: 152-155.

Xu Y, Chen M, Zhang W, Lin M: Genetic organization of genes encoding phenol hydroxylase, benzoate 1,2-dioxygenase alpha subunit and its regulatory proteins Acinetobacter calcoaceticus PHEA-2. Curr Microbiol. 2003, 46: 235-240. 10.1007/s00284-002-3840-4.

Dijkshoorn L, Aucken H, Gerner-Smidt P, Janssen P, Kaufmann ME, Garaizar J, Ursing J, Pitt TL: Comparison of outbreak and nonoutbreak Acinetobacter baumannii strains by genotypic and phenotypic methods. J Clin Microbiol. 1996, 34: 1519-1525.

Qi J, Wang B, Hao B-I: Whole proteome prokaryote phylogeny without sequence alignment: a K-string composition approach. J Mol Evol. 2004, 58: 1-11. 10.1007/s00239-003-2493-7.

Kislyuk A, Haegeman B, Bergman N, Weitz J: Genomic fluidity: an integrative view of gene diversity within microbial populations. BMC Genomics. 2011, 12: 32-10.1186/1471-2164-12-32.

Janssen P, Maquelin K, Coopman R, Tjernberg I, Bouvet P, Kersters K, Dijkshoorn L: Discrimination of Acinetobacter Genomic Species by AFLP Fingerprinting. Int J Syst Evol Microbiol. 1997, 47: 1179-1187.

Bennett JS, Jolley KA, Earle SG, Corton C, Bentley SD, Parkhill J, Maiden MCJ: A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria. Microbiology. 2012, 158: 1570-1580. 10.1099/mic.0.056077-0.

Rosselló-Mora R: Updating Prokaryotic Taxonomy. J Bacteriol. 2005, 187: 6255-6257. 10.1128/JB.187.18.6255-6257.2005.

Konstantinidis KT, Tiedje JM: Towards a genome-based taxonomy for prokaryotes. J Bacteriol. 2005, 187: 6257-6264.

Richter M, Rosselló-Móra R: Shifting the genomic gold standard for the prokaryotic species definition. PNAS. 2009, 106: 19126-19131. 10.1073/pnas.0906412106.

Chaudhuri RR, Loman NJ, Snyder LAS, Bailey CM, Stekel DJ, Pallen MJ: xBASE2: a comprehensive resource for comparative bacterial genomics. Nucleic Acids Res. 2008, 36: D543-D546.

Li L, Stoeckert CJ, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003, 13: 2178-2189. 10.1101/gr.1224503.

Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32: 1792-1797. 10.1093/nar/gkh340.

Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007, 56: 564-577. 10.1080/10635150701472164.

Bruen TC, Philippe H, Bryant D: A simple and robust statistical test for detecting the presence of recombination. Genetics. 2006, 172: 2665-2681.

Smith JM: Analyzing the mosaic structure of genes. J Mol Evol. 1992, 34: 126-129.

Jakobsen IB, Easteal S: A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. Comput Appl Biosci. 1996, 12: 291-295.

Price MN, Dehal PS, Arkin AP: FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix. Mol Biol Evol. 2009, 26: 1641-1650. 10.1093/molbev/msp077.

Felsenstein J: PHYLIP -- Phylogeny Inference Package (Version 3.2). Cladistics. 1989, 5: 164-166.

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25: 3389-3402. 10.1093/nar/25.17.3389.

Thông tin
Thông tin xuất bản

BMC Microbiology

Tập 12 Số 1

Thông tin tác giả