Antonie van Leeuwenhoek

, Volume 110, Issue 10, pp 1287–1309 | Cite as

Phylogenomic resolution of the bacterial genus Pantoea and its relationship with Erwinia and Tatumella

  • Marike Palmer
  • Emma T. Steenkamp
  • Martin P. A. Coetzee
  • Wai-Yin Chan
  • Elritha van Zyl
  • Pieter De Maayer
  • Teresa A. Coutinho
  • Jochen Blom
  • Theo H. M. Smits
  • Brion Duffy
  • Stephanus N. VenterEmail author
Original Paper


Investigation of the evolutionary relationships between related bacterial species and genera with a variety of lifestyles have gained popularity in recent years. For analysing the evolution of specific traits, however, a robust phylogeny is essential. In this study we examined the evolutionary relationships among the closely related genera Erwinia, Tatumella and Pantoea, and also attempted to resolve the species relationships within Pantoea. To accomplish this, we used the whole genome sequence data for 35 different strains belonging to these three genera, as well as nine outgroup taxa. Multigene datasets consisting of the 1039 genes shared by these 44 strains were then generated and subjected to maximum likelihood phylogenetic analyses, after which the results were compared to those using conventional multi-locus sequence analysis (MLSA) and ribosomal MLSA (rMLSA) approaches. The robustness of the respective phylogenies was then explored by considering the factors typically responsible for destabilizing phylogenetic trees. We found that the nucleotide datasets employed in the MLSA, rMLSA and 1039-gene datasets contained significant levels of homoplasy, substitution saturation and differential codon usage, all of which likely gave rise to the observed lineage specific rate heterogeneity. The effects of these factors were much less pronounced in the amino acid dataset for the 1039 genes, which allowed reconstruction of a fully supported and resolved phylogeny. The robustness of this amino acid tree was also supported by different subsets of the 1039 genes. In contrast to the smaller datasets (MLSA and rMLSA), the 1039 amino acid tree was also not as sensitive to long-branch attraction. The robust and well-supported evolutionary hypothesis for the three genera, which confidently resolved their various inter- and intrageneric relationships, represents a valuable resource for future studies. It will form the basis for studies aiming to understand the forces driving the divergence and maintenance of lineages, species and biological traits in this important group of bacteria.


Phylogenetics Non-phylogenetic signal MLSA Core genome Enterobacteriaceae 



We would like to acknowledge the Centre for Bioinformatics and Computational Biology, University of Pretoria, for the use of the facility and server access. For genome sequencing, we want to acknowledge the Ion Torrent Sequencing Facility at the University of Pretoria and Markus Oggenfuss and Jürg E. Frey for sequencing at Agroscope (Wädenswil, Switzerland). We would also like to acknowledge the Genome Research Institute (GRI) as well as the Centre of Excellence in Tree Health Biotechnology (CTHB) at the University of Pretoria for additional funding. THMS and BD acknowledge the funding by the Swiss Federal Office of Agriculture ACHILLES project (BLW/FOAG Project ACHILLES) as part of the Agroscope Research Programme ProfiCrops and the Department of Life Sciences and Facility Management of ZHAW.

Supplementary material

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10482_2017_852_MOESM2_ESM.pdf (229 kb)
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  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedGoogle Scholar
  2. Alvarez-Ponce D, Sabater-Muñoz B, Toft C, Ruiz-González MX, Fares MA (2016) essentiality is a strong determinant of protein rates of evolution during mutation accumulation experiments in Escherichia coli. Genome Biol Evol 8:2914–2927PubMedGoogle Scholar
  3. Anda M, Ohtsubo Y, Okubo T, Sugawara M, Nagata Y, Tsuda M, Minamisawa K, Mitsui H (2015) Bacterial clade with the ribosomal RNA operon on a small plasmid rather than the chromosome. Proc Natl Acad Sci USA 112:14343–14347PubMedPubMedCentralGoogle Scholar
  4. Andam CP, Gogarten JP (2011) Biased gene transfer in microbial evolution. Nat Rev Microbiol 9:543–555PubMedGoogle Scholar
  5. Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de Los Santos P, Yang P, Song N, Kano S, Caballero-Mellado J, de Faria SM, Dakora FD, Weinstock G, Hirsch AM (2014) Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS ONE 9:e83779PubMedPubMedCentralGoogle Scholar
  6. Aziz R, Bartels D, Best A, Dejongh M, Disz T, Edwards R, Formsma K, Gerdes S, Glass E, Kubal M, Meyer F, Olsen G, Olson R, Osterman A, Overbeek R, Mcneil L, Paarmann D, Paczian T, Parrello B, Pusch G, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75Google Scholar
  7. Bennett JS, Jolley KA, Earle SG, Corton C, Bentley SD, Parkhill J, Maiden MCJ (2012) A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria. Microbiology 158:1570–1580PubMedPubMedCentralGoogle Scholar
  8. Bergsten J (2005) A review of long-branch attraction. Cladistics 21:163–193Google Scholar
  9. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C, Ernst C, Goesmann A (2016) EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 44:W22–W28PubMedPubMedCentralGoogle Scholar
  10. Boto L (2010) Horizontal gene transfer in evolution: facts and challenges. Proc R Soc B Biol Sci 277:819–827Google Scholar
  11. Boucher Y, Douady CJ, Sharma AK, Kamekura M, Doolittle FW (2004) Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J Bacteriol 186:3980–3990PubMedPubMedCentralGoogle Scholar
  12. Brady C, Venter S, Cleenwerck I, Vancanneyt M, Swings J, Coutinho T (2007) A FALFP system for the improved identification of plant-pathogenic and plant-associated species of the genus Pantoea. Syst Appl Microbiol. doi: 10.1111/j.1472-765X.2009.02692.x PubMedGoogle Scholar
  13. Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T (2008) Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31:447–460PubMedGoogle Scholar
  14. Brady CL, Venter SN, Cleenwerck I, Engelbeen K, Vancanneyt M, Swings J, Coutinho TA (2009) Pantoea vagans sp. nov., Pantoea eucalypti sp. nov., Pantoea deleyi sp. nov. and Pantoea anthophila sp. nov. Int J Syst Evol Microbiol 59:2339–2345PubMedGoogle Scholar
  15. Brady CL, Cleenwerck I, Venter SN, Engelbeen K, De Vos P, Coutinho TA et al (2010a) Emended description of the genus Pantoea, description of four species from human clinical samples, Pantoea septica sp. nov., Pantoea eucrina sp. nov., Pantoea brenneri sp. nov. and Pantoea conspicua sp. nov., and transfer of Pectobacterium cypripedii (Hori 1911) Brenner et al. 1973 emend. Hauben et al. 1998 to the genus as Pantoea cypripedii comb. nov. Int J Syst Evol Microbiol 60:2430–2440PubMedGoogle Scholar
  16. Brady CL, Venter SN, Cleenwerck I, Vandemeulebroecke K, de Vos P, Coutinho TA (2010b) Transfer of Pantoea citrea, Pantoea punctata and Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov. and Tatumella terrea comb. nov. and description of Tatumella morbirosei sp. nov. Int J Syst Evol Microbiol 60:484–494PubMedGoogle Scholar
  17. Brady CL, Goszczynska T, Venter SN, Cleenwerck I, De Vos P, Gitaitis RD, Coutinho TA (2011) Pantoea allii sp. nov., isolated from onion plants and seed. Int J Syst Evol Microbiol 61:932–937PubMedGoogle Scholar
  18. Brady CL, Cleenwerck I, Van Der Westhuizen L, Venter SN, Coutinho TA, De Vos P (2012) Pantoea rodasii sp. nov., Pantoea rwandensis sp. nov. and Pantoea wallisii sp. nov., isolated from Eucalyptus. Int J Syst Evol Microbiol 62:1457–1464PubMedGoogle Scholar
  19. Bremer KR (1994) Branch support and tree stability. Cladistics 10:295–304Google Scholar
  20. Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL, Land ML, Lu T-YS, Schadt CW, Doktycz MJ, Pelletier DA (2012) Twenty-one genome sequences from Pseudomonas species and 19 genome sequences from diverse bacteria isolated from the rhizosphere and endosphere of Populus deltoides. J Bacteriol 194:5991–5993PubMedPubMedCentralGoogle Scholar
  21. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedGoogle Scholar
  22. Chan JZM, Halachev MR, Loman NJ, Constantinidou C, Pallen MJ (2012) Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol 12:302PubMedPubMedCentralGoogle Scholar
  23. Cleenwerck I, Vandemeulebroecke K, Janssens D, Swings J (2002) Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 52:1551–1558PubMedGoogle Scholar
  24. Coenye T, Gevers D, van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. Fed Eur Microbiol Soc Microbiol Rev 29:147–167Google Scholar
  25. Cohen O, Gophna U, Pupko T (2011) The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol 28:1481–1489PubMedGoogle Scholar
  26. Conlan S, Thomas PJ, Deming C, Park M, Lau AF, Dekker JP, Snitkin ES, Clark TA, Luong K, Song Y, Tsai Y-C, Boitano M, Dayal J, Brooks SY, Schmidt B, Young AC, Thomas JW, Bouffard GG, Blakesley RW, Mullikin JC, Korlach J, Henderson DK, Frank KM, Palmore TN, Segre JA (2014) Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci Transl Med 6:254ra126PubMedPubMedCentralGoogle Scholar
  27. Conville PS, Witebsky FG (2007) Analysis of multiple differing copies of the 16S rRNA gene in five clinical isolates and three type strains of Nocardia species and implications for species assignment. J Clin Microbiol 45:1146–1151PubMedPubMedCentralGoogle Scholar
  28. Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans—a plant pathogen causing human disease. J Clin Microbiol 45:1989–1992PubMedPubMedCentralGoogle Scholar
  29. Daubin V, Gouy M, Perrière G (2002) A phylogenomic approach to bacterial phylogeny: evidence of a core of genes sharing a common history. Genome Res 12:1080–1090PubMedPubMedCentralGoogle Scholar
  30. de Baere T, Verhelst R, Labit C, Verschraegen G, Wauters G, Claeys G, Vaneechoutte M (2004) Bacteremic infection with Pantoea ananatis. J Clin Microbiol 42:4393–4395PubMedPubMedCentralGoogle Scholar
  31. de Maayer P, Chan W-Y, Blom J, Venter SN, Duffy B, Smits THM, Coutinho TA (2012) The large universal Pantoea plasmid LPP-1 plays a major role in biological and ecological diversification. BMC Genom 13:625Google Scholar
  32. de Maayer P, Chan W-Y, Rubagotti E, Venter SN, Toth IK, Birch PRJ, Coutinho TA (2014) Analysis of the Pantoea ananatis pan-genome reveals factors underlying its ability to colonize and interact with plant, insect and vertebrate hosts. BMC Genom 15:1–28Google Scholar
  33. Desper R, Gascuel O (2002) Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 9:687–705PubMedGoogle Scholar
  34. Dutilh BE, Huynen MA, Bruno WJ, Snel B (2004) the consistent phylogenetic signal in genome trees revealed by reducing the impact of noise. J Mol Evol 58:527–539PubMedGoogle Scholar
  35. Dutilh BE, Snel B, Ettema TJG, Huynen MA (2008) Signature genes as a phylogenomic tool. Mol Biol Evol 25:1659–1667PubMedPubMedCentralGoogle Scholar
  36. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralGoogle Scholar
  37. Felsenstein, J. 2005. SEQBOOT—bootstrap, jackknife or permutation resampling of molecular sequence, restriction site, gene frequency or character dataGoogle Scholar
  38. Fouts DE, Matthias MA, Adhikarla H, Adler B, Amorim-Santos L, Berg DE, Bulach D, Buschiazzo A, Chang Y-F, Galloway RL, Haake DA, Haft DH, Hartskeerl R, Ko AI, Levett PN, Matsunaga J, Mechaly AE, Monk JM, Nascimento ALT, Nelson KE, Palsson B, Peacock SJ, Picardeau M, Ricaldi JN, Thaipandungpanit J, Wunder EA, Yang JR, Yang XF, Zhang J-J, Vinetz JM (2016) What makes a bacterial species pathogenic? Comparative genomic analysis of the genus Leptospira. PLoS Negl Trop Dis 10:e0004403PubMedPubMedCentralGoogle Scholar
  39. Fox GE, Wisotzkey JD, Jurtshuk PJ (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Bacteriol 42:166–170PubMedGoogle Scholar
  40. Galtier N, Daubin V (2008) Dealing with incongruence in phylogenomic analyses. Philos Trans R Soc B Biol Sci 363:4023–4029Google Scholar
  41. Galtier N, Gouy M (1995) Inferring phylogenies from DNA sequences of unequal base compositions. Proc Natl Acad Sci USA 92:11317–11321PubMedPubMedCentralGoogle Scholar
  42. Gavini F, Holmes B, Izard D, Beji A, Bernigaud A, Jakubczak E (1989a) Numerical taxonomy of Pseudomonas alcaligenes, P. pseudoalcaligenes, P. mendocina, P. stutzeri, and related bacteria. Int J Syst Evol Microbiol 39:135–144Google Scholar
  43. Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, De Ley J (1989b) Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov. Int J Syst Bacteriol 39:337–345Google Scholar
  44. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev 3:733–739Google Scholar
  45. Glaeser SP, Kämpfer P (2015) Multilocus sequence analysis (MLSA) in prokaryotic taxonomy. Syst Appl Microbiol 38:237–245PubMedGoogle Scholar
  46. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238PubMedGoogle Scholar
  47. Gordon A, Hannon GJ (2010) Fastx-toolkit. FASTQ/A short-reads pre-processing tools. Unpublished
  48. Gueule D, Fourny G, Ageron E, Le Flèche-Matéos A, Vandenbogaert M, Grimont PAD, Cilas C (2015) Pantoea coffeiphila sp. nov., cause of the ‘potato taste’ of Arabica coffee from the African Great Lakes region. Int J Syst Evol Microbiol 65:23–29PubMedGoogle Scholar
  49. Guindon SP, Dufayard J-FO, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedGoogle Scholar
  50. Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity. EMBO Rep 2:376–381PubMedPubMedCentralGoogle Scholar
  51. Hacker JRH, Dobrindt U, Kurth R (2012) Genome plasticity and infectious diseases. ASM Press, WashingtonGoogle Scholar
  52. Hall T (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61Google Scholar
  53. He M, Sebaihia M, Lawley TD, Stabler RA, Dawson LF, Martin MJ, Holt KE, Seth-Smith HMB, Quail MA, Rance R, Brooks K, Churcher C, Harris D, Bentley SD, Burrows C, Clark L, Corton C, Murray V, Rose G, Thurston S, van Tonder A, Walker D, Wren BW, Dougan G, Parkhill J (2010) Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci USA 107:7527–7532PubMedPubMedCentralGoogle Scholar
  54. Heath TA, Hedtke SM, Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. J Syst Evol 46:239–257Google Scholar
  55. Hillis DM (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst Biol 47:3–8PubMedGoogle Scholar
  56. Hong K-W, Gan HM, Low S-M, Lee PKY, Chong Y-M, Yin W-F, Chan K-G (2012) Draft genome sequence of Pantoea sp. strain A4, a Rafflesia-associated bacterium that produces N-acylhomoserine lactones as quorum-sensing molecules. J Bacteriol 194:6610PubMedPubMedCentralGoogle Scholar
  57. Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 96:3801–3806PubMedPubMedCentralGoogle Scholar
  58. Jain R, Rivera MC, Moore JE, Lake JA (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61:489–495PubMedGoogle Scholar
  59. Jeffroy O, Brinkmann H, Delsuc FDR, Philippe H (2006) Phylogenomics: the beginning of incongruence? Trends Genet 22:225–231PubMedGoogle Scholar
  60. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MCJ (2012) Ribosomal multi-locus sequence typing: universal characterisation of bacteria from domain to strain. PhD, University of OxfordGoogle Scholar
  61. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci: CABIOS 8:275–282PubMedGoogle Scholar
  62. Kamber T, Smits THM, Rezzonico F, Duffy B (2012) Genomics and current genetic understanding of Erwinia amylovora and the fire blight antagonist Pantoea vagans. Trees 26:227–238Google Scholar
  63. Kim J (1996) General inconsistency conditions for maximum parsimony: effects of branch lengths and increasing numbers of taxa. Syst Biol 45:363–374Google Scholar
  64. Kim HJ, Lee JH, Kang BR, Rong X, McspaddenGardener BB, Ji HJ, Park C-S, Kim YC (2012) Draft genome sequence of Pantoea ananatis B1-9, a nonpathogenic plant growth-promoting bacterium. J Bacteriol 194:729PubMedPubMedCentralGoogle Scholar
  65. Klenk HP, Göker M (2010) En route to a genome-based classification of archaea and bacteria? Syst Appl Microbiol 33:175–182PubMedGoogle Scholar
  66. Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264PubMedPubMedCentralGoogle Scholar
  67. Konstantinidis KT, Tiedje JM (2006) Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 72:7286–7293PubMedPubMedCentralGoogle Scholar
  68. Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509PubMedGoogle Scholar
  69. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338PubMedGoogle Scholar
  70. Koonin EV, Wolf YI (2006) Evolutionary systems biology: links between gene evolution and function. Curr Opin Biotechnol 17:481–487PubMedGoogle Scholar
  71. Kuck P, Longo G (2014) FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Front Zool 11:81PubMedPubMedCentralGoogle Scholar
  72. Lan R, Reeves PR (2000) Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8:396–401PubMedGoogle Scholar
  73. Lang JM, Darling AE, Eisen JA (2013) Phylogeny of bacterial and archaeal genomes using conserved genes: supertrees and supermatrices. PLoS ONE 8:e62510PubMedPubMedCentralGoogle Scholar
  74. Lerat E, Daubin V, Moran NA (2003) From gene trees to organismal phylogeny in prokaryotes: the case of the γ-proteobacteria. PLoS Biol 1:e19PubMedPubMedCentralGoogle Scholar
  75. Lim J-A, Lee DH, Kim B-Y, Heu S (2014) Draft genome sequence of Pantoea agglomerans R190, a producer of antibiotics against phytopathogens and foodborne pathogens. J Biotechnol 188:7–8PubMedGoogle Scholar
  76. Lukjancenko O, Wassenaar T, Ussery D (2012) Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60:708–720Google Scholar
  77. Ma H-W, Zeng A-P (2004) Phylogenetic comparison of metabolic capacities of organisms at genome level. Mol Phylogenet Evol 31:204–213PubMedGoogle Scholar
  78. Ma Y, Yin Y, Rong C, Chen S, Liu Y, Wang S, Xu F (2016) Pantoea pleuroti sp. nov., isolated from the fruiting bodies of Pleurotus eryngii. Curr Microbiol 72:207–212PubMedGoogle Scholar
  79. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Díaz-Muñiz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103:15611–15616PubMedPubMedCentralGoogle Scholar
  80. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen Y-J, Chen Z (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedPubMedCentralGoogle Scholar
  81. Mergaert J, Verdonck L, Kersters K (1993) Transfer of Erwinia ananas (synonym, Erwinia uredovora) and Erwinia stewartii to the genus Pantoea emend. as Pantoea ananas (Serrano 1928) comb. nov. and Pantoea stewartii (Smith 1898) comb. nov., respectively, and description of Pantoea stewartii subsp. indologenes subsp. nov. Int J Syst Bacteriol 43:162–173Google Scholar
  82. Mitchell A, Mitter C, Regier JC (2000) More taxa or more characters revisited: combining data from nuclear protein-encoding genes for phylogenetic analyses of Noctuoidea (Insecta: Lepidoptera). Syst Biol 49:202–224PubMedGoogle Scholar
  83. Nabhan AR, Sarkar IN (2012) The impact of taxon sampling on phylogenetic inference: a review of two decades of controversy. Brief Bioinform 13:122–134PubMedGoogle Scholar
  84. Naum M, Brown EW, Mason-Gamer RJ (2008) Is 16S rDNA a reliable phylogenetic marker to characterize relationships below the family level in the enterobacteriaceae? J Mol Evol 66:630–642PubMedGoogle Scholar
  85. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  86. Palmer M, de Maayer P, Poulsen M, Steenkamp ET, van Zyl E, Coutinho TA, Venter SN (2016) Draft genome sequences of Pantoea agglomerans and Pantoea vagans isolates associated with termites. Stand Genom Sci 11:1–11Google Scholar
  87. Philippe H, Forterre P (1999) The rooting of the universal tree of life is not reliable. J Mol Evol 49:509–523PubMedGoogle Scholar
  88. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602PubMedPubMedCentralGoogle Scholar
  89. Pond SLK, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New YorkGoogle Scholar
  90. Popp A, Cleenwerck I, Iversen C, de Vos P, Stephan R (2010) Pantoea gaviniae sp. nov. and Pantoea calida sp. nov., isolated from infant formula and an infant formula production environment. Int J Syst Evol Microbiol 60:2786–2792PubMedGoogle Scholar
  91. Prakash O, Nimonkar Y, Vaishampayan A, Mishra M, Kumbhare S, Josef N, Shouche YS (2015) Pantoea intestinalis sp. nov., isolated from the human gut. Int J Syst Evol Microbiol 65:3352–3358PubMedGoogle Scholar
  92. Prasanna AN, Mehra S (2013) Comparative phylogenomics of pathogenic and non-pathogenic Mycobacterium. PLoS ONE 8:e71248PubMedPubMedCentralGoogle Scholar
  93. Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490PubMedPubMedCentralGoogle Scholar
  94. Rezzonico F, Smits TH, Montesinos E, Frey JE, Duffy B (2009) Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol 9:204PubMedPubMedCentralGoogle Scholar
  95. Rezzonico F, Smits THM, Born Y, Blom J, Frey JE, Goesmann A, Cleenwerck I, de Vos P, Bonaterra A, Duffy B, Montesinos E (2016) Erwinia gerundensis sp. nov., a cosmopolitan epiphyte originally isolated from pome fruit trees. Int J Syst Evol Microbiol 66:1583–1592Google Scholar
  96. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106:19126–19131PubMedPubMedCentralGoogle Scholar
  97. Rivera MC, Jain R, Moore JE, Lake JA (1998) Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci USA 95:6239–6244PubMedPubMedCentralGoogle Scholar
  98. Rong C, Ma Y, Wang S, Liu Y, Chen S, Huang B, Wang J, Xu F (2016) Pantoea hericii sp. nov., isolated from the fruiting bodies of Hericium erinaceus. Curr Microbiol 72:738–743PubMedGoogle Scholar
  99. Salichos L, Rokas A (2013) Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497:327–333PubMedGoogle Scholar
  100. Sarkar SF, Guttman DS (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 70:1999–2012PubMedPubMedCentralGoogle Scholar
  101. Segata N, Huttenhower C (2011) Toward an efficient method of identifying core genes for evolutionary and functional microbial phylogenies. PLoS ONE 6:e24704PubMedPubMedCentralGoogle Scholar
  102. Smits THM, Rezzonico F, Kamber T, Goesmann A, Ishimaru CA, Stockwell VO, Frey JE, Duffy B (2010) Genome sequence of the biocontrol agent Pantoea vagans strain C9-1. J Bacteriol 192:6486–6487PubMedPubMedCentralGoogle Scholar
  103. Smits THM, Rezzonico F, Kamber T, Blom J, Goesmann A, Ishimaru CA, Frey JE, Stockwell VO, Duffy B (2011) Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoea vagans C9-1. PLoS ONE 6:e22247PubMedPubMedCentralGoogle Scholar
  104. Smits THM, Rezzonico F, López MM, Blom J, Goesmann A, Frey JE, Duffy B (2013) Phylogenetic position and virulence apparatus of the pear flower necrosis pathogen Erwinia piriflorinigrans CFBP 5888T as assessed by comparative genomics. Syst Appl Microbiol 36:449–456PubMedGoogle Scholar
  105. Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Philos Trans R Soc B Biol Sci 361:1899–1909Google Scholar
  106. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313PubMedPubMedCentralGoogle Scholar
  107. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  108. Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607PubMedPubMedCentralGoogle Scholar
  109. Tambong JT, Xu R, Kaneza C-A, Nshogozabahizi J-C (2014) An in-depth analysis of a multilocus phylogeny identifies leuS as a reliable phylogenetic marker for the genus Pantoea. Evolut Bioinform Online 10:115–125Google Scholar
  110. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis Version 6.0. Mol Biol Evol 30:2725–2729PubMedPubMedCentralGoogle Scholar
  111. Tanaka YK, Horie N, Mochida K, Yoshida Y, Okugawa E, Nanjo F (2015) Pantoea theicola sp. nov., isolated from black tea. Int J Syst Evol Microbiol 65:3313–3319Google Scholar
  112. Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 17:57–86Google Scholar
  113. Tian H, Jing C (2014) Genome sequence of the aerobic arsenate-reducing bacterium Pantoea sp. Genome Announc, Strain IMH. doi: 10.1128/genomeA.00267-14 Google Scholar
  114. Walterson AM, Stavrinides J (2015) Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol Rev 39:968–984PubMedGoogle Scholar
  115. Wan X, Hou S, Phan N, Malone Moss JS, Donachie SP, Alam M (2015) Draft genome sequence of Pantoea anthophila strain 11-2 from Hypersaline Lake Laysan. Genome Announc, Hawaii. doi: 10.1128/genomeA.00321-15 Google Scholar
  116. Wang X, Yang F, von Bodman SB (2011) The genetic and structural basis of two distinct terminal side branch residues in stewartan and amylovoran exopolysaccharides and their potential role in host adaptation. Mol Microbiol 83:195–207PubMedGoogle Scholar
  117. Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci 97:8392–8396PubMedPubMedCentralGoogle Scholar
  118. Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV (2001) Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evol Biol 1:8PubMedPubMedCentralGoogle Scholar
  119. Wu Q, Du J, Zhuang G, Jing C (2013) Bacillus sp. SXB and Pantoea sp. IMH, aerobic As (V)-reducing bacteria isolated from arsenic-contaminated soil. J Appl Microbiol 114:713–721PubMedGoogle Scholar
  120. Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373PubMedGoogle Scholar
  121. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7PubMedGoogle Scholar
  122. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University PressGoogle Scholar
  123. Zhang Y, Qiu S (2015) Examining phylogenetic relationships of Erwinia and Pantoea species using whole genome sequence data. Antonie Van Leeuwenhoek 108:1037–1046PubMedGoogle Scholar
  124. Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Syst Biol 51:588–598PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Marike Palmer
    • 1
  • Emma T. Steenkamp
    • 1
  • Martin P. A. Coetzee
    • 2
  • Wai-Yin Chan
    • 1
  • Elritha van Zyl
    • 1
  • Pieter De Maayer
    • 3
  • Teresa A. Coutinho
    • 1
  • Jochen Blom
    • 4
  • Theo H. M. Smits
    • 5
  • Brion Duffy
    • 5
  • Stephanus N. Venter
    • 1
    Email author
  1. 1.Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  2. 2.Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI),University of PretoriaPretoriaSouth Africa
  3. 3.School of Molecular and Cell BiologyUniversity of the WitwatersrandJohannesburgSouth Africa
  4. 4.Computational Genomics, Center for Biotechnology (CeBiTec)Bielefeld UniversityBielefeldGermany
  5. 5.Environmental Genomics and Systems Biology Research Group, Institute of Natural Resource SciencesZürich University of Applied Sciences (ZHAW)WädenswilSwitzerland

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