Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow

BMC Genomics

Volumn 19, Issue 1, 2018, Pages

  Wright, Erik S ^a   Baum, David A ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Classification; Horizontal gene transfer; Phylogeny; Species; Taxonomy

Indexed keywords

ARTICLE; AVERAGING; BACILLUS; CLADISTICS; GENE FLOW; GENEALOGY; GENOME; GENUS; HORIZONTAL GENE TRANSFER; NONHUMAN; PHYLOGENY; SOUND; STREPTOMYCETACEAE; BACTERIAL GENE; CLASSIFICATION; GENETICS;

GENE FLOW; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; PHYLOGENY; STREPTOMYCETACEAE;

EID: 85054360645     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-018-5099-6     Document Type: Article

References (75)

1. Sneath PH. Some thoughts on bacterial classification. J Gen Microbiol. 1957;17:184-200.
2. Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM, et al. Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci U S A. 2008;105:2504-9.
3. Koeppel AF, Wertheim JO, Barone L, Gentile N, Krizanc D, Cohan FM. Speedy speciation in a bacterial microcosm: new species can arise as frequently as adaptations within a species. ISME J. 2013;7:1080-91.
4. Martiny JBH, Jones SE, Lennon JT, Martiny AC. Microbiomes in light of traits: A phylogenetic perspective. Science. 2015;350:aac9323.
5. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A. 2005;102:2567-72.
6. Venter SN, Palmer M, Beukes CW, Chan W-Y, Shin G, Van Zyl E, et al. Practically delineating bacterial species with genealogical concordance. Antonie Van Leeuwenhoek. 2017;110:1311-25.
7. Bobay L-M, Ochman H. Biological species are universal across Life's domains. Genome Biol Evol. 2017;9:491-501.
8. Riley MA, Lizotte-Waniewski M. Population genomics and the bacterial species concept. Methods Mol Biol. 2009;532:367-77.
9. Dorit RL, Riley MA. Metagenomics: Current Innovations and Future Trends. In: Marco D, edited. Bacterial genealogy: not dead. UK: Caister Academic Press. 2011. p. 21-29.
10. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11(11):2399.
11. Doolittle WF, Papke RT. Genomics and the bacterial species problem. Genome Biol. 2006;7:116.
12. Bapteste E, O'Malley MA, Beiko RG, Ereshefsky M, Gogarten JP, Franklin-Hall L, et al. Prokaryotic evolution and the tree of life are two different things. Biol Direct. 2009;4:34.
13. Rosselló-Móra R, Amann R. Past and future species definitions for Bacteria and archaea. Syst Appl Microbiol. 2015;38:209-16.
14. Doroghazi JR, Buckley DH. A model for the effect of homologous recombination on microbial diversification. Genome Biol Evol. 2011;3:1349-56.
15. Takuno S, Kado T, Sugino RP, Nakhleh L, Innan H. Population genomics in Bacteria: a case study of Staphylococcus aureus. Mol Biol Evol. 2012;29:797-809.
16. Abby SS, Tannier E, Gouy M, Daubin V. Lateral gene transfer as a support for the tree of life. Proc Natl Acad Sci U S A. 2012;109:4962-7.
17. Cohan FM. What are bacterial species? Annu Rev Microbiol. 2002;56:457-87.
18. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. The bacterial species challenge: making sense of genetic and ecological diversity. Science. 2009;323(5915):741-6.
19. Doroghazi JR, Buckley DH. Widespread homologous recombination within and between Streptomyces species. ISME J. 2010;4:1136-43.
20. Husnik F, McCutcheon JP. Functional horizontal gene transfer from bacteria to eukaryotes. Nat Publ Group. 2018;16:67-79.
21. Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet. 2015;16:472-82.
22. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000;405:299-304.
23. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A. 2011;108:7200-5.
24. Cordero OX, Polz MF. Explaining microbial genomic diversity in light of evolutionary ecology. Nat Publ Group. 2014;12:263-73.
25. de Queiroz K. Species concepts and species delimitation. Syst Biol. 2007;56:879-86.
26. Mayden RL. A hierarchy of species concepts: the denouement in the saga of the species problem. In: Wilson MF, H CA RDM, editors. Species: the units of biodiversity. 1st ed. London: Chapman and Hall; 1997. p. 381-424.
27. Velasco JD. When monophyly is not enough: exclusivity as the key to defining a phylogenetic species concept. Biol Philos. 2009;24:473-86.
28. Baum DA. Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon. 2007;56:417-26.
29. Baum DA. Species as ranked taxa. Syst Biol. 2009;58:74-86.
30. Bryant D, Berry V. A structured family of clustering and tree construction methods. Adv Appl Math. 2001;27:705-32.
31. Mallet J. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc Lond B Biol Sci. 2008;363:2971-86.
32. Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B, Vanncanneyt M, et al. Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek. 2011;101:73-104.
33. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR, Ju K-S, et al. Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie Van Leeuwenhoek. 2017;110:563-83.
34. Doroghazi JR, Metcalf WW. Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes. BMC Genomics. 2013;14:611.
35. McDonald BR, Currie CR. Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces. mBio. 2017;8(3):e00644-17.
36. Hopwood DA. Soil to genomics: the Streptomyces chromosome. Annu Rev Genet. 2006;40:1-23.
37. Andam CP, Choudoir MJ, Vinh Nguyen A, Sol Park H, Buckley DH. Contributions of ancestral inter-species recombination to the genetic diversity of extant Streptomyces lineages. ISME J. 2016;10:1731-41.
38. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf. 2010;11:119.
39. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 1997;25:3389-402.
40. Rost B. Enzyme function less conserved than anticipated. J Mol Biol. 2002;318:595-608.
41. Zhu C, Delmont TO, Vogel TM, Bromberg Y. Functional basis of microorganism classification. Orengo CA, editor. PLoS Comput Biol 2015;11:e1004472.
42. Wolf YI, Koonin EV. A tight link between Orthologs and bidirectional best hits in bacterial and archaeal genomes. Genome Biol Evol. 2012;4:1286-94.
43. Kloesges T, Popa O, Martin W, Dagan T. Networks of gene sharing among 329 Proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol Biol Evol. 2011;28:1057-74.
44. Dongen van S. A cluster algorithm for graphs. Amsterdam: National Research Institute for Mathematics and Computer Science in the Netherlands; 2000.
45. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30:1575-84.
46. Wright ES. DECIPHER: harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinf. 2015;16:322.
47. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. 3rd ed. Vienna, Austria: R. Foundation for Statistical Computing; 2018. Available from: http://www.R-project.org.
48. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-3.
49. Paradis E, Claude J, Strimmer K. APE: analyses of Phylogenetics and evolution in R language. Bioinformatics. 2004;20:289-90.
50. Wright ES. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 2016;8:352-9.
51. Steel MA. Distribution of the symmetric difference metric on phylogenetic trees. SIAM J Discret Math. 1988;1(4):541-51.
52. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K, Kyrpides NC, et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res. 2015;43:6761-71.
53. Labeda DP. Taxonomic evaluation of putative Streptomyces scabiei strains held in the ARS culture collection (NRRL) using multi-locus sequence analysis. Antonie Van Leeuwenhoek. 2016;109:349-56.
54. Labeda DP, Doroghazi JR, Ju KS, Metcalf WW. Taxonomic evaluation of Streptomyces albus and related species using multilocus sequence analysis and proposals to emend the description of Streptomyces albus and describe Streptomyces pathocidini sp. nov. Int J Syst Evol Microbiol. 2014;64:894-900.
55. Hahn MW, Jezberová J, Koll U, Saueressig-Beck T, Schmidt J. Complete ecological isolation and cryptic diversity in Polynucleobacter bacteria not resolved by 16S rRNA gene sequences. ISME J. 2016;10:1642-55.
56. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun. 2013;4:2304.
57. Antony-Babu S, Stien D, Eparvier V, Parrot D, Tomasi S, Suzuki MT. Multiple Streptomyces species with distinct secondary metabolomes have identical 16S rRNA gene sequences. Sci Rep. 2017;7:11089.
58. Edgar RC. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics. 2018;34(14):2371-5.
59. Allard G, Ryan FJ, Jeffery IB, Claesson MJ. SPINGO: a rapid species-classifier for microbial amplicon sequences. BMC Bioinf. 2015;16:324.
60. Doroghazi JR, Albright JC, Goering AW, Ju K-S, Haines RR, Tchalukov KA, et al. A roadmap for natural product discovery based on large-scale genomics and metabolomics. Nat Chem Biol. 2014;10:963-8.
61. Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, Hanage WP. Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat Commun. 2014;5:5471.
62. Inglin RC, Meile L, Stevens MJA. Clustering of Pan- and Core-genome of Lactobacillus provides novel evolutionary insights for differentiation. BMC Genomics. 2018;19:284.
63. Kunin V, Ahren D, Goldovsky L, Janssen P, Ouzounis CA. Measuring genome conservation across taxa: divided strains and united kingdoms. Nucleic Acids Res. 2005;33:616-21.
64. Dagan T, Martin W. Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc Natl Acad Sci U S A. 2007;104:870-5.
65. Kannan L, Li H, Rubinstein B, Mushegian A. Models of gene gain and gene loss for probabilistic reconstruction of gene content in the last universal common ancestor of life. Biol Direct. 2013;8:32.
66. Swofford DL. PAUP. Phylogenetic analysis using parsimony (and other methods). 4 ed. Sinauer associates. Massachusetts: Sunderland; 2003.
67. Baum DA, Shaw KL. Genealogical perspectives on the species problem. In: Hoch PC, Stephenson AG, editors. St. Louis: Experimental and Molecular Approaches to Plant Biosystematics. 1995;53:289-303.
68. Rosselló-Móra R, Whitman WB. Dialogue on the nomenclature and classification of prokaryotes. Syst Appl Microbiol; 2018. https://www.sciencedirect.com/science/article/pii/S0723202018301681.
69. Lassalle F, Planel R, Penel S, Chapulliot D, Barbe V, Dubost A, et al. Ancestral genome estimation reveals the history of ecological diversification in Agrobacterium. Genome Biol Evol. 2017;9:3413-31.
70. Parker CT, Tindall BJ, Garrity GM. International code of nomenclature of prokaryotes. Int J Syst Evol Microbiol; 2015. http://ijs.microbiologyresearch.org/content/journal/ijsem/10.1099/ijsem.0.000778#tab2.
71. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotech; 2018. https://www.nature.com/articles/nbt.4229.
72. Coyne JA, Orr HA. Speciation: Sinauer Associates Incorporated. Sinauer Associates is an imprint of Oxford University Press; 2004. p. 9-22.
73. Mishler BD. In: Wilson RA, editor. Getting rid of species? Cambridge, MA: MIT Press; 1999. p. 307-15.
74. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Publ Group. 2014;12:635-45.
75. Brown JR. Ancient horizontal gene transfer. Nat Rev Genet. 2003;4:121-32.