Skip to main content

Methodologies for Microbial Ancestral Sequence Reconstruction

  • Protocol
  • First Online:
Environmental Microbial Evolution

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2569))

Abstract

The reconstruction of genetic material of ancestral organisms constitutes a powerful application of evolutionary biology. A fundamental step in this inference is the ancestral sequence reconstruction (ASR), which can be performed with diverse methodologies implemented in computer frameworks. However, most of these methodologies ignore evolutionary properties frequently observed in microbes, such as genetic recombination and complex selection processes, that can bias the traditional ASR. From a practical perspective, here I review methodologies for the reconstruction of ancestral DNA and protein sequences, with particular focus on microbes, and including biases, recommendations, and software implementations. I conclude that microbial ASR is a complex analysis that should be carefully performed and that there is a need for methods to infer more realistic ancestral microbial sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Chang BS, Donoghue MJ (2000) Recreating ancestral proteins. Trends Ecol Evol 15(3):109–114

    CAS  PubMed  Google Scholar 

  2. Liberles DA (2007) Ancestral Sequence Reconstruction. Oxford University Press

    Google Scholar 

  3. Merkl R, Sterner R (2016) Ancestral protein reconstruction: techniques and applications. Biol Chem 397(1):1–21. https://doi.org/10.1515/hsz-2015-0158

    Article  CAS  PubMed  Google Scholar 

  4. Pauling L, Zuckerkandl E (1963) Chemical paleogenetics: molecular “restoration studies” of extinct forms of life. Act Chem Scand 17:S9–S16

    CAS  Google Scholar 

  5. Malcom BA, Wilson KP, Matthews BW, Kirsch JF, Wilson AC (1990) Ancestral lysozymes reconstructed, neutrality tested, and thermostability linked to hydrocarbon packing. Nature 345:86–89

    Google Scholar 

  6. Stackhouse J, Presnell SR, McGeehan GM, Nambiar KP, Benner SA (1990) The ribonuclease from an extinct bovid ruminant. FEBS Lett 262(1):104–106

    CAS  PubMed  Google Scholar 

  7. Jermann TM, Opitz JG, Stackhouse J, Benner SA (1995) Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374(6517):57–59

    CAS  PubMed  Google Scholar 

  8. Gao F, Bhattacharya T, Gaschen B, Taylor J, Moore JP, Novitsky V, Yusim K, Lang D, Foley B, Beddows S, Alam M, Haynes B, Hahn BH, Korber B (2003) Consensus and ancestral state HIV vaccines. Science 299(5612):1515–1518

    Google Scholar 

  9. Doria-Rose NA, Learn GH, Rodrigo AG, Nickle DC, Li F, Mahalanabis M, Hensel MT, McLaughlin S, Edmonson PF, Montefiori D, Barnett SW, Haigwood NL, Mullins JI (2005) Human immunodeficiency virus type 1 subtype B ancestral envelope protein is functional and elicits neutralizing antibodies in rabbits similar to those elicited by a circulating subtype B envelope. J Virol 79(17):11214–11224

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Kothe DL, Li Y, Decker JM, Bibollet-Ruche F, Zammit KP, Salazar MG, Chen Y, Weng Z, Weaver EA, Gao F, Haynes BF, Shaw GM, Korber BT, Hahn BH (2006) Ancestral and consensus envelope immunogens for HIV-1 subtype C. Virology 352(2):438–449

    CAS  PubMed  Google Scholar 

  11. Gaschen B, Taylor J, Yusim K, Foley B, Gao F, Lang D, Novitsky V, Haynes B, Hahn BH, Bhattacharya T, Korber B (2002) Diversity considerations in HIV-1 vaccine selection. Science 296(5577):2354–2360

    CAS  PubMed  Google Scholar 

  12. Kothe DL, Decker JM, Li Y, Weng Z, Bibollet-Ruche F, Zammit KP, Salazar MG, Chen Y, Salazar-Gonzalez JF, Moldoveanu Z, Mestecky J, Gao F, Haynes BF, Shaw GM, Muldoon M, Korber BT, Hahn BH (2007) Antigenicity and immunogenicity of HIV-1 consensus subtype B envelope glycoproteins. Virology 360(1):218–234

    CAS  PubMed  Google Scholar 

  13. Arenas M, Posada D (2010) Computational Design of Centralized HIV-1 genes. Curr HIV Res 8(8):613–621

    CAS  PubMed  Google Scholar 

  14. Guyeux C, Al-Nuaimi B, AlKindy B, Couchot J-F, Salomon M (2018) On the reconstruction of the ancestral bacterial genomes in genus mycobacterium and Brucella. BMC Syst Biol 12(5):100. https://doi.org/10.1186/s12918-018-0618-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Harms MJ, Thornton JW (2013) Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nat Rev Genet 14(8):559–571. https://doi.org/10.1038/nrg3540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Garcia AK, Kaçar B (2019) How to resurrect ancestral proteins as proxies for ancient biogeochemistry. Free Radic Biol Med 140:260–269. https://doi.org/10.1016/j.freeradbiomed.2019.03.033

    Article  CAS  PubMed  Google Scholar 

  17. Yamashiro K, Yokobori S, Koikeda S, Yamagishi A (2010) Improvement of Bacillus circulans beta-amylase activity attained using the ancestral mutation method. Protein Eng Des Sel 23(7):519–528. https://doi.org/10.1093/protein/gzq021

    Article  CAS  PubMed  Google Scholar 

  18. Gaucher EA, Thomson JM, Burgan MF, Benner SA (2003) Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425(6955):285–288

    CAS  PubMed  Google Scholar 

  19. Miyazaki J, Nakaya S, Suzuki T, Tamakoshi M, Oshima T, Yamagishi A (2001) Ancestral residues stabilizing 3-isopropylmalate dehydrogenase of an extreme thermophile: experimental evidence supporting the thermophilic common ancestor hypothesis. J Biochem 129(5):777–782. https://doi.org/10.1093/oxfordjournals.jbchem.a002919

    Article  CAS  PubMed  Google Scholar 

  20. Iwabata H, Watanabe K, Ohkuri T, Yokobori S-i, Yamagishi A (2005) Thermostability of ancestral mutants of Caldococcus noboribetus isocitrate dehydrogenase. FEMS Microbiol Lett 243(2):393–398. https://doi.org/10.1016/j.femsle.2004.12.030

    Article  CAS  PubMed  Google Scholar 

  21. Perez-Jimenez R, Ingles-Prieto A, Zhao ZM, Sanchez-Romero I, Alegre-Cebollada J, Kosuri P, Garcia-Manyes S, Kappock TJ, Tanokura M, Holmgren A, Sanchez-Ruiz JM, Gaucher EA, Fernandez JM (2011) Single-molecule paleoenzymology probes the chemistry of resurrected enzymes. Nat Struct Mol Biol 18(5):592–596

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Risso VA, Gavira JA, Mejia-Carmona DF, Gaucher EA, Sanchez-Ruiz JM (2013) Hyperstability and substrate promiscuity in laboratory resurrections of Precambrian beta-lactamases. J Am Chem Soc 135(8):2899–2902. https://doi.org/10.1021/ja311630a

    Article  CAS  PubMed  Google Scholar 

  23. Shih PM, Occhialini A, Cameron JC, Andralojc PJ, Parry MA, Kerfeld CA (2016) Biochemical characterization of predicted Precambrian RuBisCO. Nat Commun 7:10382. https://doi.org/10.1038/ncomms10382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP, Benner SA (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37(6):630–635. https://doi.org/10.1038/ng1553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Alcalde M (2015) Engineering the ligninolytic enzyme consortium. Trends Biotechnol 33(3):155–162. https://doi.org/10.1016/j.tibtech.2014.12.007

    Article  CAS  PubMed  Google Scholar 

  26. Trudeau DL, Kaltenbach M, Tawfik DS (2016) On the potential origins of the high stability of reconstructed ancestral proteins. Mol Biol Evol 33(10):2633–2641. https://doi.org/10.1093/molbev/msw138

    Article  CAS  PubMed  Google Scholar 

  27. Schmitt AO, Schuchhardt J, Ludwig A, Brockmann GA (2007) Protein evolution within and between species. J Theor Biol 249(2):376–383. https://doi.org/10.1016/j.jtbi.2007.08.001

    Article  CAS  PubMed  Google Scholar 

  28. Wilson C, Agafonov RV, Hoemberger M, Kutter S, Zorba A, Halpin J, Buosi V, Otten R, Waterman D, Theobald DL, Kern D (2015) Kinase dynamics. Using ancient protein kinases to unravel a modern cancer drug’s mechanism. Science 347(6224):882–886. https://doi.org/10.1126/science.aaa1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gaucher EA (2007) Experimental resurrection of ancient biomolecules: gene synthesis, heterologous protein expression, and functional assays. In: Liberles DA (ed) Ancestral Sequence Reconstruction. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199299188.003.0014

    Chapter  Google Scholar 

  30. Felsenstein J (2004) Inferring phylogenies. Sinauer Associates, Sunderland, MA

    Google Scholar 

  31. Joy JB, Liang RH, McCloskey RM, Nguyen T, Poon AFY (2016) Ancestral reconstruction. PLoS Comput Biol 12(7):e1004763. https://doi.org/10.1371/journal.pcbi.1004763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bull JJ, Cunningham CW, Molineux IJ, Badgett MR, Hillis DM (1993) Experimental molecular evolution of bacteriophage T7. Evolution 47(4):993–1007

    CAS  PubMed  Google Scholar 

  33. Zhang J, Nei M (1997) Accuracies of ancestral amino acid sequences inferred by the parsimony, likelihood, and distance methods. J Mol Evol 44(Suppl 1):S139–S146

    CAS  PubMed  Google Scholar 

  34. Randall RN, Radford CE, Roof KA, Natarajan DK, Gaucher EA (2016) An experimental phylogeny to benchmark ancestral sequence reconstruction. Nat Commun 7:12847. https://doi.org/10.1038/ncomms12847

    Article  PubMed  PubMed Central  Google Scholar 

  35. Williams PD, Pollock DD, Blackburne BP, Goldstein RA (2006) Assessing the accuracy of ancestral protein reconstruction methods. PLoS Comput Biol 2(6):e69

    PubMed  PubMed Central  Google Scholar 

  36. Fitch W (1971) Toward defining the course of evolution: minimal change for a specific tree topology. Syst Zool 20:406–416

    Google Scholar 

  37. Sankoff D (1975) Minimal mutation trees of sequences. SIAM J Appl Math 28:35–42

    Google Scholar 

  38. Maddison WP, Donoghue MJ, Maddison DR (1984) Outgroup analysis and parsimony. Syst Zool 33:83–103

    Google Scholar 

  39. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford series in ecology and evolution. Oxford University Press, New York

    Google Scholar 

  40. Swofford DL, Maddison WP (1987) Reconstructing ancestral character states under Wagner parsimony. Math Biosci 87:199–229

    Google Scholar 

  41. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17(1):32–43

    CAS  PubMed  Google Scholar 

  42. Holder M, Lewis PO (2003) Phylogeny estimation: traditional and Bayesian approaches. Nat Rev Genet 4(4):275–284

    CAS  PubMed  Google Scholar 

  43. Eyre-Walker A (1998) Problems with parsimony in sequences of Biased Base composition. J Mol Evol 47(6):686–690. https://doi.org/10.1007/PL00006427

    Article  CAS  PubMed  Google Scholar 

  44. Arenas M (2015) Trends in substitution models of molecular evolution. Front Genet 6:319. https://doi.org/10.3389/fgene.2015.00319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schluter D (1995) Uncertainty in ancient phylogenies. Nature 377:108–109

    CAS  PubMed  Google Scholar 

  46. Yang Z, Kumar S, Nei M (1995) A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641–1650

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Koshi JM, Goldstein RA (1996) Probabilistic reconstruction of ancestral protein sequences. J Mol Evol 42(2):313–320

    CAS  PubMed  Google Scholar 

  48. Pupko T, Pe’er I, Shamir R, Graur D (2000) A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol Biol Evol 17(6):890–896

    CAS  PubMed  Google Scholar 

  49. Arenas M, Bastolla U (2020) ProtASR2: ancestral reconstruction of protein sequences accounting for folding stability. Methods Ecol Evol 11(2):248–257. https://doi.org/10.1111/2041-210X.13341

    Article  Google Scholar 

  50. Arenas M, Weber CC, Liberles DA, Bastolla U (2017) ProtASR: an evolutionary framework for ancestral protein reconstruction with selection on folding stability. Syst Biol 66(6):1054–1064. https://doi.org/10.1093/sysbio/syw121

    Article  CAS  PubMed  Google Scholar 

  51. Pupko T, Pe’er I, Hasegawa M, Graur D, Friedman N (2002) A branch-and-bound algorithm for the inference of ancestral amino-acid sequences when the replacement rate varies among sites: application to the evolution of five gene families. Bioinformatics 18(8):1116–1123

    CAS  PubMed  Google Scholar 

  52. Galtier N (2001) Maximum-likelihood phylogenetic analysis under a covarion-like model. Mol Biol Evol 18(5):866–873

    CAS  PubMed  Google Scholar 

  53. Yang Z (2006) Computational Molecular Evolution. Oxford University Press, Oxford

    Google Scholar 

  54. Liò P, Goldman N (1998) Models of molecular evolution and phylogeny. Genome Res 8(12):1233–1244

    PubMed  Google Scholar 

  55. Yang Z (1995) PAML, phylogenetic analysis by maximum likelihood. 1.1 edn. In: Institute of Molecular Evolutionary Genetics. The Pennsylvania State University, University Park, PA

    Google Scholar 

  56. Arenas M, Posada D (2010) The effect of recombination on the reconstruction of ancestral sequences. Genetics 184(4):1133–1139

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Schultz TR, Churchill GA (1999) The role of subjectivity in reconstructing ancestral character states: a Bayesian approach to unknown rates, states, and transformation asymmetries. Syst Biol 48(3):651–664. https://doi.org/10.1080/106351599260229

    Article  Google Scholar 

  58. Huelsenbeck JP, Bollback JP (2001) Empirical and hierarchical Bayesian estimation of ancestral states. Syst Biol 50(3):351–366

    CAS  PubMed  Google Scholar 

  59. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591

    CAS  PubMed  Google Scholar 

  60. Hanson-Smith V, Kolaczkowski B, Thornton JW (2010) Robustness of ancestral sequence reconstruction to phylogenetic uncertainty. Mol Biol Evol 27(9):1988–1999. https://doi.org/10.1093/molbev/msq081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Merkl R, Sterner R (2016) Reconstruction of ancestral enzymes. Perspect Sci 9:17–23. https://doi.org/10.1016/j.pisc.2016.08.002

    Article  Google Scholar 

  62. Perez-Losada M, Arenas M, Galan JC, Palero F, Gonzalez-Candelas F (2015) Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect Genet Evol 30C:296–307. https://doi.org/10.1016/j.meegid.2014.12.022

    Article  CAS  Google Scholar 

  63. Didelot X, Maiden MC (2010) Impact of recombination on bacterial evolution. Trends Microbiol 18(7):315–322. https://doi.org/10.1016/j.tim.2010.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Arenas M, Araujo NM, Branco C, Castelhano N, Castro-Nallar E, Perez-Losada M (2018) Mutation and recombination in pathogen evolution: relevance, methods and controversies. Infect Genet Evol 63:295–306. https://doi.org/10.1016/j.meegid.2017.09.029

    Article  CAS  PubMed  Google Scholar 

  65. Castelhano N, Araujo NM, Arenas M (2017) Heterogeneous recombination among hepatitis B virus genotypes. Infect Genet Evol 54:486–490. https://doi.org/10.1016/j.meegid.2017.08.015

    Article  CAS  PubMed  Google Scholar 

  66. Arenas M, Lorenzo-Redondo R, Lopez-Galindez C (2016) Influence of mutation and recombination on HIV-1 in vitro fitness recovery. Mol Phylogenet Evol 94(Pt A):264–270. https://doi.org/10.1016/j.ympev.2015.09.001

    Article  CAS  PubMed  Google Scholar 

  67. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879–891

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Arenas M (2013) The importance and application of the ancestral recombination graph. Front Genet 4:206

    PubMed  PubMed Central  Google Scholar 

  69. Griffiths RC, Marjoram P (1997) An ancestral recombination graph. In: Donelly P, Tavaré S (eds) Progress in population genetics and human evolution, IMA volume in mathematics and its applications, vol 87. Springer-Verlag, Berlin, pp 257–270

    Google Scholar 

  70. Martin DP, Lemey P, Posada D (2011) Analysing recombination in nucleotide sequences. Mol Ecol Resour 11(6):943–955

    PubMed  Google Scholar 

  71. Arenas M (2021) Computational analysis of recombination in viral nucleotide sequences. In: Bamford D, Zuckerman M (eds) Encyclopedia of virology, 4th edn. Academic Press (Elsevier), p In press

    Google Scholar 

  72. Mallo D, Sánchez-Cobos A, Arenas M (2016) Diverse considerations for successful phylogenetic tree reconstruction: impacts from model misspecification, recombination, homoplasy, and pattern recognition. In: Elloumi M, Iliopoulos C, Wang J, Zomaya A (eds) Pattern recognition in computational molecular biology. Wiley, pp 439–456. https://doi.org/10.1002/9781119078845.ch23

    Chapter  Google Scholar 

  73. Kosakovsky Pond SL, Frost SD, Muse SV (2005) HYPHY: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Google Scholar 

  74. Hubisz M, Siepel A (2020) In: Dutheil JY (ed) Inference of ancestral recombination graphs using ARGweaver. Statistical Population Genomics. Springer, US, New York, NY, pp 231–266. https://doi.org/10.1007/978-1-0716-0199-0_10

    Chapter  Google Scholar 

  75. Rasmussen MD, Siepel A (2013) Genome-wide inference of ancestral recombination graphs. arXiv:1306.5110v2

    Google Scholar 

  76. Cámara PG, Levine AJ, Rabadán R (2016) Inference of ancestral recombination graphs through topological data analysis. PLoS Comput Biol 12(8):e1005071. https://doi.org/10.1371/journal.pcbi.1005071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Heine K, Beskos A, Jasra A, Balding D, De Iorio M (2018) Bridging trees for posterior inference on ancestral recombination graphs. Proc Math Phys Eng Sci 474(2220):20180568. https://doi.org/10.1098/rspa.2018.0568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Vaughan TG, Welch D, Drummond AJ, Biggs PJ, George T, French NP (2017) Inferring ancestral recombination graphs from bacterial genomic data. Genetics 205(2):857. https://doi.org/10.1534/genetics.116.193425

    Article  PubMed  Google Scholar 

  79. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22(24):3096–3098

    PubMed  Google Scholar 

  80. Lemmon AR, Moriarty EC (2004) The importance of proper model assumption in bayesian phylogenetics. Syst Biol 53(2):265–277

    PubMed  Google Scholar 

  81. Spielman SJ, Kosakovsky Pond SL (2018) Relative evolutionary rates in proteins are largely insensitive to the substitution model. Mol Biol Evol 35(9):2307–2317. https://doi.org/10.1093/molbev/msy127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Abadi S, Azouri D, Pupko T, Mayrose I (2019) Model selection may not be a mandatory step for phylogeny reconstruction. Nat Commun 10(1):934. https://doi.org/10.1038/s41467-019-08822-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Spielman SJ (2020) Relative model fit does not predict topological accuracy in single-gene protein Phylogenetics. Mol Biol Evol 37(7):2110–2123. https://doi.org/10.1093/molbev/msaa075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Duchene S, Di Giallonardo F, Holmes EC (2016) Substitution model adequacy and assessing the reliability of estimates of virus evolutionary rates and time scales. Mol Biol Evol 33(1):255–267. https://doi.org/10.1093/molbev/msv207

    Article  CAS  PubMed  Google Scholar 

  85. Tao Q, Barba-Montoya J, Huuki LA, Durnan MK, Kumar S (2020) Relative efficiencies of simple and complex substitution models in estimating divergence times in Phylogenomics. Mol Biol Evol 37(6):1819–1831. https://doi.org/10.1093/molbev/msaa049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Chang BS, Jonsson K, Kazmi MA, Donoghue MJ, Sakmar TP (2002) Recreating a functional ancestral archosaur visual pigment. Mol Biol Evol 19(9):1483–1489

    CAS  PubMed  Google Scholar 

  87. Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301(5640):1714–1717

    CAS  PubMed  Google Scholar 

  88. Goldstein RA (2011) The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins 79(5):1396–1407

    CAS  PubMed  Google Scholar 

  89. Serohijos AW, Shakhnovich EI (2014) Merging molecular mechanism and evolution: theory and computation at the interface of biophysics and evolutionary population genetics. Curr Opin Struct Biol 26:84–91. https://doi.org/10.1016/j.sbi.2014.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bastolla U, Dehouck Y, Echave J (2017) What evolution tells us about protein physics, and protein physics tells us about evolution. Curr Opin Struct Biol 42:59–66. https://doi.org/10.1016/j.sbi.2016.10.020

    Article  CAS  PubMed  Google Scholar 

  91. Taverna DM, Goldstein RA (2002) Why are proteins so robust to site mutations? J Mol Biol 315(3):479–484

    CAS  PubMed  Google Scholar 

  92. DePristo MA, Weinreich DM, Hartl DL (2005) Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6(9):678–687

    CAS  PubMed  Google Scholar 

  93. Liberles DA, Teichmann SA, Bahar I, Bastolla U, Bloom J, Bornberg-Bauer E, Colwell LJ, de Koning AP, Dokholyan NV, Echave J, Elofsson A, Gerloff DL, Goldstein RA, Grahnen JA, Holder MT, Lakner C, Lartillot N, Lovell SC, Naylor G, Perica T, Pollock DD, Pupko T, Regan L, Roger A, Rubinstein N, Shakhnovich E, Sjolander K, Sunyaev S, Teufel AI, Thorne JL, Thornton JW, Weinreich DM, Whelan S (2012) The interface of protein structure, protein biophysics, and molecular evolution. Protein Sci 21(6):769–785

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Arenas M, Sanchez-Cobos A, Bastolla U (2015) Maximum likelihood phylogenetic inference with selection on protein folding stability. Mol Biol Evol 32(8):2195–2207. https://doi.org/10.1093/molbev/msv085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Arenas M, Dos Santos HG, Posada D, Bastolla U (2013) Protein evolution along phylogenetic histories under structurally constrained substitution models. Bioinformatics 29(23):3020–3028

    CAS  PubMed  Google Scholar 

  96. Jiménez-Santos MJ, Arenas M, Bastolla U (2018) Influence of mutation bias and hydrophobicity on the substitution rates and sequence entropies of protein evolution. Peer J 6:e5549. https://doi.org/10.7717/peerj.5549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Jimenez MJ, Arenas M, Bastolla U (2018) Substitution rates predicted by stability-constrained models of protein evolution are not consistent with empirical data. Mol Biol Evol 35(3):743–755. https://doi.org/10.1093/molbev/msx327

    Article  CAS  PubMed  Google Scholar 

  98. Echave J, Wilke CO (2017) Biophysical models of protein evolution: understanding the patterns of evolutionary sequence divergence. Annu Rev Biophys 46:85–103. https://doi.org/10.1146/annurev-biophys-070816-033819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Bastolla U, Arenas M (2019) The influence of protein stability on sequence evolution: applications to phylogenetic inference. In: Sikosek T (ed) Computational methods in protein evolution. Springer, New York, New York, NY, pp 215–231. https://doi.org/10.1007/978-1-4939-8736-8_11

    Chapter  Google Scholar 

  100. Wilke CO (2012) Bringing molecules back into molecular evolution. PLoS Comput Biol 8(6):e1002572

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Bordner AJ, Mittelmann HD (2013) A new formulation of protein evolutionary models that account for structural constraints. Mol Biol Evol 31(3):736–749

    PubMed  Google Scholar 

  102. Echave J (2019) Beyond stability constraints: a biophysical model of enzyme evolution with selection on stability and activity. Mol Biol Evol 36(3):613–620. https://doi.org/10.1093/molbev/msy244

    Article  CAS  PubMed  Google Scholar 

  103. Rodrigue N, Lartillot N, Bryant D, Philippe H (2005) Site interdependence attributed to tertiary structure in amino acid sequence evolution. Gene 347(2):207–217

    CAS  PubMed  Google Scholar 

  104. Bastolla U, Porto M, Roman HE, Vendruscolo M (2006) A protein evolution model with independent sites that reproduces site-specific amino acid distributions from the protein data Bank. BMC Evol Biol 6:43

    PubMed  PubMed Central  Google Scholar 

  105. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27(8):1164–1165. https://doi.org/10.1093/bioinformatics/btr088

    Article  CAS  PubMed  Google Scholar 

  108. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35(21):4453–4455. https://doi.org/10.1093/bioinformatics/btz305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Minning J, Porto M, Bastolla U (2013) Detecting selection for negative design in proteins through an improved model of the misfolded state. Proteins 81(7):1102–1112. https://doi.org/10.1002/prot.24244

    Article  CAS  PubMed  Google Scholar 

  110. Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21(6):1095–1109

    CAS  PubMed  Google Scholar 

  111. Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25(17):2286–2288. https://doi.org/10.1093/bioinformatics/btp368

    Article  CAS  PubMed  Google Scholar 

  112. Bastolla U, Moya A, Viguera E, van Ham RC (2004) Genomic determinants of protein folding thermodynamics in prokaryotic organisms. J Mol Biol 343(5):1451–1466

    CAS  PubMed  Google Scholar 

  113. Carletti MS, Monzon AM, Garcia-Rios E, Benitez G, Hirsh L, Fornasari MS, Parisi G (2020) Revenant: a database of resurrected proteins. Database 2020. https://doi.org/10.1093/database/baaa031

  114. Arenas J, Paganelli FL, Rodriguez-Castano P, Cano-Crespo S, van der Ende A, van Putten JP, Tommassen J (2016) Expression of the gene for autotransporter AutB of Neisseria meningitidis affects biofilm formation and epithelial transmigration. Front Cell Infect Microbiol 6:162. https://doi.org/10.3389/fcimb.2016.00162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Arenas M (2015) Genetic consequences of antiviral therapy on HIV-1. Comput Math Method M 2015:9. https://doi.org/10.1155/2015/395826

    Article  Google Scholar 

  116. Arenas M (2020) Protein evolution in the Flaviviruses. J Mol Evol 88(6):473–476. https://doi.org/10.1007/s00239-020-09953-1

    Article  CAS  PubMed  Google Scholar 

  117. Lopes JS, Arenas M, Posada D, Beaumont MA (2014) Coestimation of recombination, substitution and molecular adaptation rates by approximate Bayesian computation. Heredity 112(3):255–264

    CAS  PubMed  Google Scholar 

  118. Poon AF, Kosakovsky Pond SL, Richman DD, Frost SD (2007) Mapping protease inhibitor resistance to human immunodeficiency virus type 1 sequence polymorphisms within patients. J Virol 81(24):13598–13607

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Perez-Losada M, Jobes DV, Sinangil F, Crandall KA, Arenas M, Posada D, Berman PW (2011) Phylodynamics of HIV-1 from a phase III AIDS vaccine trial in Bangkok, Thailand. PLoS One 6(3):e16902

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Perez-Losada M, Posada D, Arenas M, Jobes DV, Sinangil F, Berman PW, Crandall KA (2009) Ethnic differences in the adaptation rate of HIV gp120 from a vaccine trial. Retrovirology 6:67

    PubMed  PubMed Central  Google Scholar 

  121. Didelot X, Walker AS, Peto TE, Crook DW, Wilson DJ (2016) Within-host evolution of bacterial pathogens. Nat Rev Microbiol 14(3):150–162. https://doi.org/10.1038/nrmicro.2015.13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Wang H-C, Spencer M, Susko E, Roger AJ (2007) Testing for Covarion-like evolution in protein sequences. Mol Biol Evol 24(1):294–305. https://doi.org/10.1093/molbev/msl155

    Article  CAS  PubMed  Google Scholar 

  123. Neuhauser C, Krone SM (1997) The genealogy of samples in models with selection. Genetics 145(2):519–534

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  125. Maddison WP, Maddison DR (2019) Mesquite: a modular system for evolutionary analysis. 3.61 edn.,

    Google Scholar 

  126. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Xu B, Yang Z (2013) PAMLX: a graphical user interface for PAML. Mol Biol Evol 30(12):2723–2724. https://doi.org/10.1093/molbev/mst179

    Article  CAS  PubMed  Google Scholar 

  128. Moshe A, Pupko T (2019) Ancestral sequence reconstruction: accounting for structural information by averaging over replacement matrices. Bioinformatics 35(15):2562–2568. https://doi.org/10.1093/bioinformatics/bty1031

    Article  CAS  PubMed  Google Scholar 

  129. Guindon S, Dufayard JF, 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 (3):307-321

    Google Scholar 

  130. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    CAS  PubMed  Google Scholar 

  131. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchene S, Fourment M, Gavryushkina A, Heled J, Jones G, Kuhnert D, De Maio N, Matschiner M, Mendes FK, Muller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu CH, Xie D, Zhang C, Stadler T, Drummond AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15(4):e1006650. https://doi.org/10.1371/journal.pcbi.1006650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Martin DP, Varsani A, Roumagnac P, Botha G, Maslamoney S, Schwab T, Kelz Z, Kumar V, Murrell B (2020) RDP5: a computer program for analysing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. https://doi.org/10.1093/ve/veaa087

  133. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61 (3):539-542

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Spanish Ministry of Economy and Competitiveness [RYC-2015-18241] and by Xunta de Galicia [ED431F 2018/08].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miguel Arenas .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Arenas, M. (2022). Methodologies for Microbial Ancestral Sequence Reconstruction. In: Luo, H. (eds) Environmental Microbial Evolution. Methods in Molecular Biology, vol 2569. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2691-7_14

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2691-7_14

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2690-0

  • Online ISBN: 978-1-0716-2691-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics