The pan-genome of Lactobacillus reuteri strains originating from the pig gastrointestinal tract

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Wegmann, Udo ^a   MacKenzie, Donald A ^a   Zheng, Jinshui ^b   Goesmann, Alexander ^c   Roos, Stefan ^d   Swarbreck, David ^a   Walter, Jens ^e   Crossman, Lisa C ^f,g   Juge, Nathalie ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^e UNIVERSITY OF ALBERTA   (Canada)

^f UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^g NRP Innovation Centre   (United Kingdom)

Author keywords

Auxiliary secretion system; Clade specific genes; Comparative genomics; Host specificity; Lactobacillus reuteri; Pig; Serine rich repeat proteins; Surface adhesins

Indexed keywords

CELL SURFACE PROTEIN; BACTERIAL SECRETION SYSTEM; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL STRAIN; CLADISTICS; CONTROLLED STUDY; GASTROINTESTINAL TRACT; GENE CLUSTER; GENE SEQUENCE; GENOTYPE; HOST RANGE; HUMAN; INTESTINE; LACTOBACILLUS REUTERI; MOUSE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PIG; PLASMID; RAT; SMALL INTESTINE; ANIMAL; BACTERIAL SECRETION SYSTEM; BACTERIOPHAGE; BASAL METABOLIC RATE; GENE ORDER; GENE STRUCTURE; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PROCEDURES; PSEUDOGENE; VIROLOGY;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIOPHAGES; BASAL METABOLISM; CHROMOSOMES, BACTERIAL; GASTROINTESTINAL TRACT; GENE ORDER; GENE TRANSFER, HORIZONTAL; GENETIC STRUCTURES; GENOME, BACTERIAL; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PATHOGEN INTERACTIONS; LACTOBACILLUS REUTERI; MULTIGENE FAMILY; PHYLOGENY; PSEUDOGENES; SWINE;

EID: 84949255798     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2216-7     Document Type: Article

References (105)

1. Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009;136:65-80.
2. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90:859-904.
3. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science. 2012;336:1255-62.
4. Walter J, Ley R. The human gut microbiome: Ecology and recent evolutionary changes. Ann Rev Microbiol. 2011;65:411-29.
5. Walter J, Britton RA, Roos S. Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Nat Acad Sci USA. 2011;108:4645-52.
6. Walter J. Ecological role of lactobacilli in the gastrointestinal tract: Implications for fundamental and biomedical research. Appl Environ Microbiol. 2008;74:4985-96.
7. Fuller R, Brooker BE. Lactobacilli which attach to the crop epithelium of the fowl. Am J Clin Nutr. 1974;27:1305-12.
8. Fuller R, Barrow PA, Brooker BE. Bacteria associated with the gastric epithelium of neonatal pigs. Appl Environ Microbiol. 1978;35:582-91.
9. Tannock GW. The lactic microflora of pigs, mice and rats. In: Wood BJB, editor. The lactic acid bacteria, volume 1: The lactic acid bacteria in health and disease. London: Elsevier; 1992. p. 21-48.
10. Lin JH-C, Savage DC. Host specificity of the colonization of murine gastric epithelium by lactobacilli. FEMS Microbiol Lett. 1984;24:67-71.
11. Wesney E, Tannock GW. Association of rat, pig, and fowl biotypes of lactobacilli with the stomach of gnotobiotic mice. Microb Ecol. 1979;5:35-42.
12. Frese SA, MacKenzie DA, Peterson DA, Schmaltz R, Fangman T, Zhou Y, et al. Molecular characterization of host-specific biofilm formation in a vertebrate gut symbiont. PLoS Genet. 2013;9:e1004057.
13. Walter J, Schwab C, Loach DM, Gänzle MG, Tannock GW. Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology. 2008;154:72-80.
14. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN, Roos S, et al. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J. 2010;4:377-87.
15. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J, Zhang M, et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet. 2011;7:e1001314.
16. Etzold S, MacKenzie DA, Jeffers F, Walshaw J, Roos S, Hemmings AM, et al. Structural and molecular insights into novel surface-exposed mucus adhesins from Lactobacillus reuteri human strains. Mol Microbiol. 2014;92:543-56.
17. Jensen H, Roos S, Jonsson H, Rud I, Grimmer S, van Pijkeren J-P, et al. Role of Lactobacillus reuteri cell and mucus-binding protein A (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro. Microbiology. 2014;160:671-81.
18. Etzold S, Kober O, MacKenzie DA, Tailford LE, Gunning P, Walshaw J, et al. Structural basis for adaptation of lactobacilli to gastrointestinal mucus. Environ Microbiol. 2014;16:888-903.
19. MacKenzie DA, Tailford LE, Hemmings AM, Juge N. Crystal structure of a mucus binding protein repeat reveals an unexpected functional immunoglobulin binding activity. J Biol Chem. 2009;284:32444-53.
20. MacKenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ, Roos S, et al. Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology. 2010;156:3368-78.
21. Roos S, Jonsson H. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology. 2002;148:433-42.
22. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Møller K. Culture-independent analysis of gut bacteria: The pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol. 2002;68:673-90.
23. du Toit M, Franz CMAP, Dicks LMT, Schillinger U, Haberer P, Warlies B, et al. Characterisation and selection of probiotic lactobacilli for a preliminary minipig feeding trial and their effect on serum cholesterol levels, faeces pH and faeces moisture content. Int J Food Microbiol. 1998;40:93-104.
24. Hou C, Zeng X, Yang F, Liu H, Qiao S. Study and use of the probiotic Lactobacillus reuteri in pigs: A review. J Animal Sci Biotechnol. 2015;6:14.
25. Yang F, Wang A, Zeng X, Hou C, Liu H, Qiao S. Lactobacillus reuteri I5007 modulates tight junction protein expression in IPEC-J2 cells with LPS stimulation and in newborn piglets under normal conditions. BMC Microbiol. 2015;15:32.
26. Heavens D, Tailford LE, Crossman LC, Jeffers F, MacKenzie DA, Caccamo M, et al. Genome sequence of a vertebrate gut symbiont Lactobacillus reuteri ATCC 53608. J Bacteriol. 2011;193:4015-6.
27. Frank AC, Lobry JR. Oriloc: Prediction of replication boundaries in unannotated bacterial chromosomes. Bioinformatics. 2000;16:560-1.
28. The R Project for Statistical Computing. https://www.r-project.org/. Accessed 9 June 2014.
29. Axelsson LT, Ahrné SEI, Andersson MC, Ståhl SR. Identification and cloning of a plasmid-encoded erythromycin resistance determinant from Lactobacillus reuteri. Plasmid. 1988;20:171-4.
30. Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY, Sutormin RA, et al. RegPrecise 3.0-a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genomics. 2013;14:745.
31. Liu Y, Harrison P, Kunin V, Gerstein M. Comprehensive analysis of pseudogenes in prokaryotes: Widespread gene decay and failure of putative horizontally transferred genes. Genome Biol. 2004;5:R64.
32. Merkl R. SIGI: score-based identification of genomic islands. BMC Bioinformatics. 2004;5:22.
33. Crooks GE, Hon G, John-Marc Chandonia J-M, Brenner SE. WebLogo: A sequence logo generator. Genome Res. 2004;14:1188-90.
34. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: A fast phage search tool. Nucl Acids Res. 2011;39:W347-52.
35. Darling AE, Mau B, Perna NT. Progressivemauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5:e11147.
36. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12.
37. Zheng J, Ruan L, Sun M, Gänzle M. A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology. Appl Environ Microbiol. 2015;81:7233-43.
38. Hou C, Wang Q, Zeng X, Yang F, Zhang J, Liu H, et al. Complete genome sequence of Lactobacillus reuteri I5007, a probiotic strain isolated from healthy piglet. J Biotechnol. 2014;179:63-4.
39. Fischer S, Brunk BP, Chen F, Gao X, Harb OS, Iodice JB, et al. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr Prot Bioinformatics. 2011;6 Suppl 35:1-19. 12.
40. Laing C, Buchanan C, Taboada EN, Zhang Y, Kropinski A, Villegas A, et al. Pan-genome sequence analysis using Panseq: An online tool for the rapid analysis of core and accessory genomic regions. BMC Bioinformatics. 2010;11:461.
41. Grissa I, Vergnaud G, Pourcel C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics. 2007;8:172.
42. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucl Acids Res. 2007;35:W52-7.
43. Grissa I, Vergnaud G, Pourcel C. CRISPRcompar: A website to compare clustered regularly interspaced short palindromic repeats. Nucl Acids Res. 2008;36:W145-8.
44. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119.
45. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007;23:673-9.
46. Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E, Grechkin Y, et al. IMG: The integrated microbial genomes database and comparative analysis system. Nucl Acids Res. 2012;40:D115-22.
47. Artemis: genome browser and annotation tool. http://www.sanger.ac.uk/ science/tools/artemis. Accessed 20 June 2014.
48. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M-A, et al. Artemis: Sequence visualization and annotation. Bioinformatics. 2000;16:944-5.
49. Wadström T, Andersson K, Sydow M, Axelsson L, Lindgren S, Gullmar B. Surface properties of lactobacilli isolated from the small intestine of pigs. J Appl Bacteriol. 1987;62:513-20.
50. Gallotta M, Gancitano G, Pietrocola G, Mora M, Pezzicoli A, Tuscano G, et al. SpyAD, a moonlighting protein of Group A Streptococcus contributing to bacterial division and host cell adhesion. Infect Immun. 2014;82:2890-901.
51. Wästfelt M, Stâlhammar-Carlemalm M, Delisse AM, Cabezon T, Lindahl G. Identification of a family of streptococcal surface proteins with extremely repetitive structure. J Biol Chem. 1996;271:18892-7.
52. De Weirdt R, Crabbé A, Roos S, Vollenweider S, Lacroix C, van Pijkeren JP, et al. Glycerol supplementation enhances L. reuteri's protective effect against S. typhimurium colonization in a 3-D model of colonic epithelium. PLoS One. 2012;7:e37116.
53. Walter J, Chagnaud P, Tannock GW, Loach DM, Dal Bello F, Jenkinson HF, et al. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol. 2005;71:979-86.
54. Juge N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 2012;20:30-9.
55. Langmead B, Salzberg S. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9.
56. Li H, Durbin R. Fast and accurate long-read alignment with Burrows- Wheeler transform. Bioinformatics. 2010;26:589-95.
57. Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-2.
58. Wong JEMM, Midtgaard SR, Gysel K, Thygesen MB, Sørensen KK, Jensen KJ, et al. An intermolecular binding mechanism involving multiple LysM domains mediates carbohydrate recognition by an endopeptidase. Acta Cryst. 2015;D71:592-605.
59. Bendtsen JD, Kiemer L, Fausbøll A, Brunak S. Non-classical protein secretion in bacteria. BMC Microbiol. 2005;5:58.
60. Perea Vélez M, Petrova MI, Lebeer S, Verhoeven TLA, Claes I, Lambrichts I, et al. Characterization of MabA, a modulator of Lactobacillus rhamnosus GG adhesion and biofilm formation. FEMS Immunol Med Microbiol. 2010;59:386-98.
61. Pyburn TM, Bensing BA, Xiong YQ, Melancon BJ, Tomasiak TM, Ward NJ, et al. A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathog. 2011;7:e1002112.
62. Garnett JA, Simpson PJ, Taylor J, Benjamin SV, Tagliaferri C, Cota E, et al. Structural insight into the role of Streptococcus parasanguinis Fap1 within oral biofilm formation. Biochem Biophys Res Commun. 2012;417:421-6.
63. Li Y, Huang X, Li J, Zeng J, Zhu F, Fan W, et al. Both GtfA and GtfB are required for SraP glycosylation in Staphylococcus aureus. Curr Microbiol. 2014;69:121-6.
64. Feltcher ME, Braunstein M. Emerging themes in SecA2-mediated protein export. Nat Rev Microbiol. 2012;10:779-89.
65. Alien_hunter: predicts putative horizontal gene transfer events with the implementation of interpolated variable order motifs. http://www.sanger.ac. uk/science/tools/alien-hunter. Accessed 20 July 2014.
66. Vernikos GS, Parkhill J. Interpolated variable order motifs for identification of horizontally acquired DNA: Revisiting the Salmonella pathogenicity islands. Bioinformatics. 2006;22:2196-203.
67. Ozimek LK, Kralj S, van der Maarel MJEC, Dijkhuizen L. The levansucrase and inulosucrase enzymes of Lactobacillus reuteri 121 catalyse processive and non-processive transglycosylation reactions. Microbiology. 2006;152:1187-96.
68. Schwab C, Walter J, Tannock GW, Vogel RF, Gänzle MG. Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri. Syst Appl Microbiol. 2007;30:433-43.
69. Kralj S, van Geel-Schutten GH, Rahaoui H, Leer RJ, Faber EJ, van der Maarel MJEC, et al. Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with a-(1-4) and a-(1-6) glucosidic bonds. Appl Environ Microbiol. 2002;68:4283-91.
70. Dobruchowska JM, Meng X, Leemhuis H, Gerwig GJ, Dijkhuizen L, Kamerling JP. Gluco-oligomers initially formed by the reuteransucrase enzyme of Lactobacillus reuteri 121 incubated with sucrose and malto-oligosaccharides. Glycobiology. 2013;23:1084-96.
71. Kralj S, Stripling E, Sanders P, van Geel-Schutten GH, Dijkhuizen L. Highly hydrolytic reuteransucrase from probiotic Lactobacillus reuteri strain ATCC 55730 Appl Environ Microbiol. 2005;71:3942-50.
72. Sims IM, Frese SA, Walter J, Loach D, Wilson M, Appleyard K, et al. Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23. ISME J. 2011;5:1115-24.
73. Lebeer S, Verhoeven TLA, Francius G, Schoofs G, Lambrichts I, Dufrêne Y, et al. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol. 2009;75:3554-63.
74. Saulnier DM, Santos F, Roos S, Mistretta T-A, Spinler JK, Molenaar D, et al. Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PLoS One. 2011;6:e18783.
75. Ewing B, Green P. Base-calling of automated sequencer traces using Phred. II Error probabilities Genome Res. 1998;8:186-94.
76. Staden R, Beal KF, Bonfield JK. The Staden package, 1998. Methods Mol Biol. 2000;132:115-30.
77. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, et al. GenDB-an open source genome annotation system for prokaryote genomes. Nucl Acids Res. 2003;31:2187-95.
78. Lowe TM, Eddy SR. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res. 1997;25:955-64.
79. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: Rapid annotations using subsystems technology. BMC Genomics. 2008;9:75.
80. 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. Nucl Acids Res. 1997;25:3389-402.
81. Tatusova T, Ciufo S, Fedorov B, O'Neill K, Tolstoy I. RefSeq microbial genomes database: New representation and annotation strategy. Nucl Acids Res. 2014;42:D553-9.
82. Magrane M, UniProt Consortium. UniProt knowledgebase: A hub of integrated protein data. Database 2011:bar009. doi:10.1093/database/bar009.
83. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucl Acids Res. 2008;36:D480-4.
84. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. The Pfam protein families database. Nucl Acids Res. 2012;40:D290-301.
85. Haft DH, Loftus BJ, Richardson DL, Yang F, Eisen JA, Paulsen IT, et al. TIGRFAMs: A protein family resource for the functional identification of proteins. Nucl Acids Res. 2001;29:41-3.
86. SignalP 4.1 server: predicts the presence and location of signal peptide cleavage sites in amino acid sequences. http://www.cbs.dtu.dk/services/ SignalP/. Accessed 19 November 2014.
87. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785-6.
88. PRED-LIPO: a hidden Markov model method for the prediction of lipoprotein signal peptides of Gram-positive bacteria. http://bioinformatics. biol.uoa.gr/PRED-LIPO/. Accessed 21 November 2014.
89. Bagos PG, Tsirigos KD, Liakopoulos TD, Hamodrakas SJ. Prediction of lipoprotein signal peptides in Gram-positive bacteria with a hidden Markov model. J Proteome Res. 2008;7:5082-93.
90. LipoP 1.0 server: predicts lipoproteins and discriminates between lipoprotein signal peptides, other signal peptides and n-terminal membrane helices in Gram-negative (and Gram-positive) bacteria. http://www.cbs.dtu. dk/services/LipoP/. Accessed 21 November 2014.
91. Juncker AS, Willenbrock H, von Heijne G, Nielsen H, Brunak S, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003;12:1652-62.
92. Rahman O, Cummings SP, Harrington DJ, Sutcliffe IC. Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol. 2008;24:2377-82.
93. Sutcliffe IC, Harrington DJ. Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology. 2002;148:2065-77.
94. TMHMM Server v. 2.0: prediction of transmembrane helices in proteins. http://www.cbs.dtu.dk/services/TMHMM/. Accessed 9 June 2014.
95. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol. 2001;305:567-80.
96. CAZy: the Carbohydrate-Active enZYmes Database. http://www.cazy.org/. Accessed 20 May 2014.
97. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucl Acids Res. 2014;42:D490-5.
98. Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068-9.
99. JSpecies: a biologist-centric software for measuring the probability of two genomes belonging to the same species. http://imedea.uib-csic.es/jspecies/. Accessed 27 July 2015.
100. MySQL 5.7 reference manual :: 3 tutorial :: 3.3.1 creating and selecting a database. https://dev.mysql.com/doc/refman/5.7/en/creating-database.html. Accessed 25 July 2014.
101. Contreras-Moreira B, Vinuesa P. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol. 2013;79:7696-701.
102. Angiuoli SV, Salzberg SL. Mugsy: Fast multiple alignment of closely related whole genomes. Bioinformatics. 2011;27:334-42.
103. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972-3.
104. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat Methods. 2012;9:772.
105. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307-21.