Comparative analyses of Legionella species identifies genetic features of strains causing Legionnaires' disease

Genome Biology

Volumn 15, Issue 11, 2014, Pages

  Gomez Valero, Laura ^a,b   Rusniok, Christophe ^a,b   Rolando, Monica ^a,b   Neou, Mario ^a,b   Dervins Ravault, Delphine ^a,b   Demirtas, Jasmin ^a,b   Rouy, Zoe ^h   Moore, Robert J ⁱ   Chen, Honglei ⁱ   Petty, Nicola K ^c   Jarraud, Sophie ^d,e   Etienne, Jerome ^d,e   Steinert, Michael ^f   Heuner, Klaus ^g   Gribaldo, Simonetta ^a   Médigue, Claudine ^h   Glöckner, Gernot ^j,k   Hartland, Elizabeth L ^l   Buchrieser, Carmen ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^d CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^e HOSPICES CIVILS DE LYON   (France)

^f TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^g ROBERT KOCH INSTITUTE   (Germany)

^h DIF   (France)

ⁱ CSIRO   (Australia)

^j UNIVERSITY OF COLOGNE   (Germany)

^k LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^l UNIVERSITY OF MELBOURNE   (Australia)

more..

Author keywords

Eukaryotic like proteins; Genome; Legionella; Legionnaires' disease; Mobilome

Indexed keywords

CLATHRIN; COATOMER PROTEIN; SYNAPTOBREVIN; THAUMATIN;

AMOEBA (LIFE CYCLE STAGE); ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; COMPARATIVE STUDY; CONTROLLED STUDY; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC HETEROGENEITY; GENETIC SCREENING; GENOME ANALYSIS; HUMAN; HUMAN CELL; LEGIONELLA; LEGIONELLA FALLONII; LEGIONELLA HACKELIAE; LEGIONNAIRE DISEASE; MACROPHAGE; NONHUMAN; PROPHAGE; PROTEIN DOMAIN; PROTEIN MOTIF; TATLOCKIA MICDADEI; TYPE IV SECRETION SYSTEM; CELL LINE; EPIDEMIC; GENETICS; HIGH THROUGHPUT SEQUENCING; INTERSPERSED REPEAT; LEGIONELLA PNEUMOPHILA; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; SPECIES DIFFERENCE;

AMOEBA; BASE SEQUENCE; CELL LINE; DISEASE OUTBREAKS; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MOLECULAR SEQUENCE ANNOTATION; SPECIES SPECIFICITY;

EID: 84965188538     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-014-0505-0     Document Type: Article

References (93)

1. Newton HJ, Ang DK, van Driel IR, Hartland EL: Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 2010, 23:274-298
2. Yu VL, Plouffe JF, Pastoris MC, Stout JE, Schousboe M, Widmer A, Summersgill J, File T, Heath CM, Paterson DL, Chereshsky A: Distribution of Legionella species and serogroups isolated by culture in patients with sporadic community-acquired legionellosis: an international collaborative survey. J Infect Dis 2002, 186:127-128
3. Doleans A, Aurell H, Reyrolle M, Lina G, Freney J, Vandenesch F, Etienne J, Jarraud S: Clinical and environmental distributions of Legionella strains in France are different. J Clin Microbiol 2004, 42:458-460
4. Svarrer CW, Uldum SA: The occurrence of Legionella species other than Legionella pneumophila in clinical and environmental samples in Denmark identified by mip gene sequencing and matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Microbiol Infect 2012, 18:1004-1009
5. Alli OA, Zink S, von Lackum NK, Abu-Kwaik Y: Comparative assessment of virulence traits in Legionella spp. Microbiology 2003, 149:631-641
6. Hägele S, Kohler R, Merkert H, Schleicher M, Hacker J, Steinert M: Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2000, 2:135-171
7. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, Ma L, Tichit M, Jarraud S, Bouchier C, Vandenesch F, Kunst F, Etienne J, Glaser P, Buchrieser C: Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 2004, 36:1165-1173
8. Chien M, Morozova I, Shi S, Sheng H, Chen J, Gomez SM, Asamani G, Hill K, Nuara J, Feder M, Rineer J, Greenberg JJ, Steshenko V, Park SH, Zhao B, Teplitskaya E, Edwards JR, Pampou S, Georghiou A, Chou IC, Iannuccilli W, Ulz ME, Kim DH, Geringer-Sameth A, Goldsberry C, Morozov P, Fischer SG, Segal G, Qu X, Rzhetsky A, et al: The genomic sequence of the accidental pathogen Legionella pneumophila. Science 2004, 305:1966-1968
9. Cazalet C, Gomez-Valero L, Rusniok C, Lomma M, Dervins-Ravault D, Newton HJ, Sansom FM, Jarraud S, Zidane N, Ma L, Bouchier C, Etienne J, Hartland EL, Buchrieser C: Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet 2010, 6:e1000851
10. Kozak NA, Buss M, Lucas CE, Frace M, Govil D, Travis T, Olsen-Rasmussen M, Benson RF, Fields BS: Virulence factors encoded by Legionella longbeachae identified on the basis of the genome sequence analysis of clinical isolate D-4968. J Bacteriol 2010, 192:1030-1044
11. D'Auria G, Jimenez-Hernandez N, Peris-Bondia F, Moya A, Latorre A: Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 2010, 11:181
12. Gomez-Valero L, Rusniok C, Jarraud S, Vacherie B, Rouy Z, Barbe V, Medigue C, Etienne J, Buchrieser C: Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 2011, 12:536
13. Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, Wee B, Fry NK, Harrison TG, Newton HJ, Thomson NR, Beatson SA, Dougan G, Hartland EL, Frankel G: Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins. J Bacteriol 2010, 192:6001-6016
14. Steinert M, Heuner K, Buchrieser C, Albert-Weissenberger C, Glockner G: Legionella pathogenicity: genome structure, regulatory networks and the host cell response. Int J Med Microbiol 2007, 297:577-587
15. Brzuszkiewicz E, Schulz T, Rydzewski K, Daniel R, Gillmaier N, Dittmann C, Holland G, Schunder E, Lautner M, Eisenreich W, Lück C, Heuner K: Legionella oakridgensis ATCC 33761 genome sequence and phenotypic characterization reveals its replication capacity in amoebae. Int J Med Microbiol 2013, 303:514-528
16. Wilkinson HW, Thacker WL, Steigerwalt AG, Brenner DJ, Ampel NM, Wing EJ: Second serogroup of Legionella hackeliae isolated from a patient with pneumonia. J Clin Microbiol 1985, 22:488-489
17. Birtles RJ, Rowbotham TJ, Raoult D, Harrison TG: Phylogenetic diversity of intra-amoebal Legionellae as revealed by 16S rRNA gene sequence comparison. Microbiology 1996, 142:3525-3530
18. Neumeister B, Reiff G, Faigle M, Dietz K, Northoff H, Lang F: Influence of Acanthamoeba castellanii on intracellular growth of different Legionella species in human monocytes. Appl Environ Microbiol 2000, 66:914-919
19. Albers U, Reus K, Shuman HA, Hilbi H: The amoebae plate test implicates a paralogue of lpxB in the interaction of Legionella pneumophila with Acanthamoeba castellanii. Microbiology 2005, 151:167-182
20. MicroScope Microbial Genome Annotation & AnalysisPlatform containing the sequenced and annotated Legionella genomes [https://www.genoscope.cns.fr/agc/microscope/about/collabprojects. php?P_id=27]
21. LegioList Integrated Genome database, containing the annotated genome sequences [http://genolist.pasteur.fr/LegioList/]
22. Coscolla M, Comas I, Gonzalez-Candelas F: Quantifying nonvertical inheritance in the evolution of Legionella pneumophila. Mol Biol Evol 2011, 28:985-1001
23. Grattard F, Ginevra C, Riffard S, Ros A, Jarraud S, Etienne J, Pozzetto B: Analysis of the genetic diversity of Legionella by sequencing the 23S-5S ribosomal intergenic spacer region: from phylogeny to direct identification of isolates at the species level from clinical specimens. Microbes Infect 2006, 8:73-83
24. Rubin CJ, Thollesson M, Kirsebom LA, Herrmann B: Phylogenetic relationships and species differentiation of 39 Legionella species by sequence determination of the RNase P RNA gene rnpB. Int J Syst Evol Microbiol 2005, 55:2039-2049
25. Adeleke A, Pruckler J, Benson R, Rowbotham T, Halablab M, Fields B: Legionella-like amebal pathogens-phylogenetic status and possible role in respiratory disease. Emerg Infect Dis 1996, 2:225-230
26. Adeleke AA, Fields BS, Benson RF, Daneshvar MI, Pruckler JM, Ratcliff RM, Harrison TG, Weyant RS, Birtles RJ, Raoult D, Halablab MA: Legionella drozanskii sp. nov., Legionella rowbothamii sp. nov. and Legionella fallonii sp. nov.: three unusual new Legionella species. Int J Syst Evol Microbiol 2001, 51:1151-1160
27. Roy CR, Isberg RR: Topology of Legionella pneumophila DotA: an inner membrane protein required for replication in macrophages. Infect Immun 1997, 65:571-578
28. Berger KH, Merriam JJ, Isberg RR: Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 1994, 14:809-822
29. Bardill JP, Miller JL, Vogel JP: IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 2005, 56:90-103
30. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR: A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 2002, 295:679-682
31. Feldman M, Segal G: A specific genomic location within the icm/dot pathogenesis region of different Legionella species encodes functionally similar but nonhomologous virulence proteins. Infect Immun 2004, 72:4503-4511
32. Feldman M, Zusman T, Hagag S, Segal G: Coevolution between nonhomologous but functionally similar proteins and their conserved partners in the Legionella pathogenesis system. Proc Natl Acad Sci U S A 2005, 102:12206-12211
33. Luo ZQ, Isberg RR: Multiple substrates of the Legionella pneumophila Dot/ Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 2004, 101:841-846
34. Zusman T, Yerushalmi G, Segal G: Functional similarities between the icm/ dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila. Infect Immun 2003, 71:3714-3723
35. Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I: Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 2002, 43:793-808
36. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U: The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 2001, 39:1452-1463
37. Welander PV, Hunter RC, Zhang L, Sessions AL, Summons RE, Newman DK: Hopanoids play a role in membrane integrity and pH homeostasis in Rhodopseudomonas palustris TIE-1. J Bacteriol 2009, 191:6145-6156
38. Volkman JK: Sterols in microorganisms. Appl Microbiol Biotechnol 2003, 60:495-506
39. Schmerk CL, Bernards MA, Valvano MA: Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia. J Bacteriol 2011, 193:6712-6723
40. Vadake RS: Biotransformation of Chitin to Chitosan. United States Patent 5739015. 1998. United States Patent
41. Campos-Gongora E, Ebert F, Willhoeft U, Said-Fernandez S, Tannich E: Characterization of chitin synthases from Entamoeba. Protist 2004, 155:323-330
42. Grigor'ev AA, Bondarev VP, Borisevich IV, Darmov IV, Mironin AV, Zolotarev AG, Pogorel'skii IP, Ianov DS: Temperate Legionella bacteriophage: discovery and characteristics. Zh Mikrobiol Epidemiol Immunobiol 2008, 4:86-88
43. Lammertyn E, Vande Voorde J, Meyen E, Maes L, Mast J, Anné J: Evidence for the presence of Legionella bacteriophages in environmental water samples. Microb Ecol 2008, 56:191-197
44. Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, Tateda K, Swanson MS: Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 2006, 17:1093-1104
45. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE: Flagellin-deficient Legionella mutants evade caspase-1-and Naip5-mediated macrophage immunity. PLoS Pathog 2006, 2:e18
46. Gomez Valero L, Runsiok C, Cazalet C, Buchrieser C: Comparative and functional genomics of Legionella identified eukaryotic like proteins as key players in host-pathogen interactions. Front Microbiol 2011, 2:208
47. Gomez-Valero L, Buchrieser C: Genome dynamics in Legionella: the basis of versatility and adaptation to intracellular replication. Cold Spring Harb Perspect Med 2013, 3:a009993
48. Lautner M, Schunder E, Herrmann V, Heuner K: Regulation, integrase-dependent excision, and horizontal transfer of genomic islands in Legionella pneumophila. J Bacteriol 2013, 195:1583-1597
49. Bandyopadhyay P, Liu S, Gabbai CB, Venitelli Z, Steinman HM: Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect Immun 2007, 75:723-735
50. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM, Ferguson DJ, Hood DW: Novel type IV secretion system involved in propagation of genomic islands. J Bacteriol 2007, 189:761-771
51. Wee BA, Woolfit M, Beatson SA, Petty NK: A distinct and divergent lineage of genomic island-associated type IV Secretion Systems in Legionella. PLoS One 2013, 8:e82221
52. Shohdy N, Efe JA, Emr SD, Shuman HA: Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci U S A 2005, 102:4866-4871
53. Habyarimana F, Al-Khodor S, Kalia A, Graham JE, Price CT, Garcia MT, Kwaik YA: Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages. Environ Microbiol 2008, 10:1460-1474
54. Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ, O'Connor TJ, Chen C, Machner M, Montminy T, Isberg RR: The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 2011, 13:227-245
55. Harding CR, Schroeder GN, Reynolds S, Kosta A, Collins JW, Mousnier A, Frankel G: Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun 2012, 80:2780-2790
56. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR: A Legionella pneumophilatranslocated substrate that is required for growth within macrophages and protection from host cell deat. Proc Natl Acad Sci U S A 2006, 103:18745-18750
57. Liu Y, Luo ZQ: The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 2007, 75:592-603
58. Eiserich JP, Estévez AG, Bamberg TV, Ye YZ, Chumley PH, Beckman JS, Freeman BA: Microtubule dysfunction by posttranslational nitrotyrosination of alpha-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc Natl Acad Sci U S A 1999, 96:6365-6370
59. Acharya K, Pal AK, Gulati A, Kumar S, Singh AK, Ahuja PS: Overexpression of Camellia sinensis thaumatin-like protein, CsTLP in potato confers enhanced resistance to Macrophomina phaseolina and Phytophthora infestans infection. Mol Biotechnol 2013, 54:609-622
60. Monteiro S, Barakat M, Picarra-Pereira MA, Teixeira AR, Ferreira RB: Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. Phytopathology 2003, 93:1505-1512
61. Vodovar N, Vinals M, Liehl P, Basset A, Degrouard J, Spellman P, Boccard F, Lemaitre B: Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci U S A 2005, 102:11414-11419
62. Sudhof TC, Baumert M, Perin MS, Jahn R: A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 1989, 2:1475-1481
63. McMahon HT, Mills IG: COP and clathrin-coated vesicle budding: different pathways, common approaches. Curr Opin Cell Biol 2004, 16:379-391
64. Degtyar E, Zusman T, Ehrlich M, Segal G: A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria. Cell Microbiol 2009, 11:1219-1235
65. Lurie-Weinberger MN, Gomez-Valero L, Merault N, Glockner G, Buchrieser C, Gophna U: The origins of eukaryotic-like proteins in Legionella pneumophila. Int J Med Microbiol 2010, 300:470-481
66. Herrmann V, Eidner A, Rydzewski K, Bladel I, Jules M, Buchrieser C, Eisenreich W, Heuner K: GamA is a eukaryotic-like glucoamylase responsible for glycogen-and starch-degrading activity of Legionella pneumophila. Int J Med Microbiol 2011, 301:133-139
67. Szyk A, Piszczek G, Roll-Mecak A: Tubulin tyrosine ligase and stathmin compete for tubulin binding in vitro. J Mol Biol 2013, 425:2412-2414
68. Tripathi LP, Sowdhamini R: Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 2006, 7:200
69. Jacobi A, Rossmann R, Bock A: The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in Escherichia coli. Arch Microbiol 1992, 158:444-451
70. Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M: Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 2002, 277:871-874
71. Ouellet H, Ouellet Y, Richard C, Labarre M, Wittenberg B, Wittenberg J, Guertin M: Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci U S A 2002, 99:5902-5907
72. Pawaria S, Lama A, Raje M, Dikshit KL: Responses of Mycobacterium tuberculosis hemoglobin promoters to in vitro and in vivo growth conditions. Appl Environ Microbiol 2008, 74:3512-3522
73. Vuletich DA, Lecomte JT: A phylogenetic and structural analysis of truncated hemoglobins. J Mol Evol 2006, 62:196-210
74. Wiens JR, Vasil AI, Schurr MJ, Vasil ML: Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa. MBio 2014, 5:e01010-e01013
75. Hindre T, Bruggemann H, Buchrieser C, Hechard Y: Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology 2008, 154:30-41
76. Bou-Abdallah F, Lewin AC, Le Brun NE, Moore GR, Chasteen ND: Iron detoxification properties of Escherichia coli bacterioferritin. Attenuation of oxyradical chemistry. J Biol Chem 2002, 277:37064-37069
77. Carrondo MA: Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J 2003, 22:1959-1968
78. Jarvinen HM, Laakkonen L, Haiko J, Johansson T, Juuti K, Suomalainen M, Buchrieser C, Kalkkinen N, Korhonen TK: Human single-chain urokinase is activated by the omptins PgtE of Salmonella enterica and Pla of Yersinia pestis despite mutations of active site residues. Mol Microbiol 2013, 89:507-517
79. Aurass P, Schlegel M, Metwally O, Harding CR, Schroeder GN, Frankel G, Flieger A: The Legionella pneumophila Dot/Icm-secreted effector PlcC/CegC1 together with PlcA and PlcB promotes virulence and belongs to a novel zinc metallophospholipase C family present in bacteria and fungi. J Biol Chem 2013, 288:11080-11092
80. Otto TD, Sanders M, Berriman M, Newbold C: Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 2010, 26:1704-1707
81. Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, Le Fevre F, Longin C, Mornico D, Roche D, Rouy Z, Salvignol G, Scarpelli C, Thil Smith AA, Weiman M, Médigue C: MicroScope-an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res 2013, 41:D636-D647
82. MicroScope Microbial Genome Annotation and Analysis Platform. [https://www.genoscope.cns.fr/agc/microscope/home/index.php]
83. Fouts DE, Brinkac L, Beck E, Inman J, Sutton G: PanOCT: automated clustering of orthologs using conserved gene neighborhood for pan-genomic analysis of bacterial strains and closely related species. Nucleic Acids Res 2012, 40:e172
84. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA: BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011, 12:402
85. Sullivan MJ, Petty NK, Beatson SA: Easyfig: a genome comparison visualizer. Bioinformatics 2011, 27:1009-1010
86. Darling AC, Mau B, Blattner FR, Perna NT: Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004, 14:1394-1403
87. Newton HJ, Sansom FM, Dao J, McAlister AD, Sloan J, Cianciotto NP, Hartland EL: Sel1 repeat protein LpnE is a Legionella pneumophila virulence determinant that influences vacuolar trafficking. Infect Immun 2007, 75:5575-5585
88. Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113
89. Criscuolo A, Gribaldo S: BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010, 10:210
90. Price MN, Dehal PS, Arkin AP: FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 2010, 5:e9490
91. Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552
92. 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, 28:2731-2739
93. Stamatakis A, Aberer AJ, Goll C, Smith SA, Berger SA, Izquierdo-Carrasco F: RAxML-Light: a tool for computing terabyte phylogenies. Bioinformatics 2012, 28:2064-2066