Horizontal transmission and recombination maintain forever young bacterial symbiont genomes


Autoři: Shelbi L. Russell aff001;  Evan Pepper-Tunick aff002;  Jesper Svedberg aff002;  Ashley Byrne aff001;  Jennie Ruelas Castillo aff001;  Christopher Vollmers aff002;  Roxanne A. Beinart aff004;  Russell Corbett-Detig aff002
Působiště autorů: Department of Molecular Cellular and Developmental Biology. University of California Santa Cruz, Santa Cruz, California, United States of America aff001;  Department of Biomolecular Engineering. University of California Santa Cruz, Santa Cruz, California, United States of America aff002;  Genomics Institute, University of California, Santa Cruz, California, United States of America aff003;  Graduate School of Oceanography. University of Rhode Island, Narragansett, Rhode Island, United States of America aff004
Vyšlo v časopise: Horizontal transmission and recombination maintain forever young bacterial symbiont genomes. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008935
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008935

Souhrn

Bacterial symbionts bring a wealth of functions to the associations they participate in, but by doing so, they endanger the genes and genomes underlying these abilities. When bacterial symbionts become obligately associated with their hosts, their genomes are thought to decay towards an organelle-like fate due to decreased homologous recombination and inefficient selection. However, numerous associations exist that counter these expectations, especially in marine environments, possibly due to ongoing horizontal gene flow. Despite extensive theoretical treatment, no empirical study thus far has connected these underlying population genetic processes with long-term evolutionary outcomes. By sampling marine chemosynthetic bacterial-bivalve endosymbioses that range from primarily vertical to strictly horizontal transmission, we tested this canonical theory. We found that transmission mode strongly predicts homologous recombination rates, and that exceedingly low recombination rates are associated with moderate genome degradation in the marine symbionts with nearly strict vertical transmission. Nonetheless, even the most degraded marine endosymbiont genomes are occasionally horizontally transmitted and are much larger than their terrestrial insect symbiont counterparts. Therefore, horizontal transmission and recombination enable efficient natural selection to maintain intermediate symbiont genome sizes and substantial functional genetic variation.

Klíčová slova:

Bacterial genomics – DNA recombination – Genomics – Homologous recombination – Invertebrate genomics – Mitochondria – Population genetics – Sequence alignment


Zdroje

1. Moran NA, Bennett GM. The Tiniest Tiny Genomes. Annu Rev Microbiol. 2014;68: 195–215. doi: 10.1146/annurev-micro-091213-112901 24995872

2. Lo W-S, Huang Y-Y, Kuo C-H. Winding paths to simplicity: genome evolution in facultative insect symbionts. Lai E-M, editor. FEMS Microbiol Rev. 2016;40: 855–874. doi: 10.1093/femsre/fuw028 28204477

3. Giovannoni SJ, Cameron Thrash J, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8.

4. Meseguer AS, Manzano-Marín A, Coeur d’Acier A, Clamens A-L, Godefroid M, Jousselin E. Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Mol Ecol. 2017;26: 2363–2378. doi: 10.1111/mec.13910 27862540

5. McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 2011 [cited 3 Jan 2017]. doi: 10.1038/nrmicro2670 22064560

6. Toft C, Andersson SGE. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet. 2010;11: 465–475. doi: 10.1038/nrg2798 20517341

7. Lambert JD, Moran NA. Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci. 1998;95: 4458–4462. doi: 10.1073/pnas.95.8.4458 9539759

8. Kuwahara H, Takaki Y, Yoshida T, Shimamura S, Takishita K, Reimer JD, et al. Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams. Extremophiles. 2008;12: 365–374. doi: 10.1007/s00792-008-0141-2 18305898

9. Herbeck JT, Funk DJ, Degnan PH, Wernegreen JJ. A Conservative Test of Genetic Drift in the Endosymbiotic Bacterium Buchnera: Slightly Deleterious Mutations in the Chaperonin groEL. Genetics. 2003; 10.

10. Shapiro BJ, Alm E. The slow:fast substitution ratio reveals changing patterns of natural selection in γ-proteobacterial genomes. ISME J. 2009;3: 1180–1192. doi: 10.1038/ismej.2009.51 19458656

11. Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, et al. The Calyptogena magnifica Chemoautotrophic Symbiont Genome. Science. 2007;315: 998–1000. doi: 10.1126/science.1138438 17303757

12. Kuwahara H, Yoshida T, Takaki Y, Shimamura S, Nishi S, Harada M, et al. Reduced Genome of the Thioautotrophic Intracellular Symbiont in a Deep-Sea Clam, Calyptogena okutanii. Curr Biol. 2007;17: 881–886. doi: 10.1016/j.cub.2007.04.039 17493812

13. Dmytrenko O, Russell SL, Loo WT, Fontanez KM, Liao L, Roeselers G, et al. The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. BMC Genomics. 2014;15. doi: 10.1186/1471-2164-15-15

14. Miller IJ, Vanee N, Fong SS, Lim-Fong GE, Kwan JC. Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula.” Drake HL, editor. Appl Environ Microbiol. 2016;82: 6573–6583. doi: 10.1128/AEM.01800-16 27590822

15. Russell SL, Corbett-Detig RB, Cavanaugh CM. Mixed transmission modes and dynamic genome evolution in an obligate animal–bacterial symbiosis. ISME J. 2017; 1359–1371. doi: 10.1038/ismej.2017.10 28234348

16. Hendry TA, Freed LL, Fader D, Fenolio D, Sutton TT, Lopez JV. Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes. Moran NA, editor. mBio. 2018;9: e01033–18, /mbio/9/3/mBio.01033-18.atom. doi: 10.1128/mBio.01033-18 29946051

17. Jäckle O, Seah BKB, Tietjen M, Leisch N, Liebeke M, Kleiner M, et al. Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula. Proc Natl Acad Sci. 2019; 201818995. doi: 10.1073/pnas.1818995116 30962361

18. George EE, Husnik F, Tashyreva D, Prokopchuk G, Horák A, Kwong WK, et al. Highly Reduced Genomes of Protist Endosymbionts Show Evolutionary Convergence. Curr Biol. 2020;30: 925–933.e3. doi: 10.1016/j.cub.2019.12.070 31978335

19. Ran L, Larsson J, Vigil-Stenman T, Nylander JAA, Ininbergs K, Zheng W-W, et al. Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium. Ahmed N, editor. PLoS ONE. 2010;5: e11486. doi: 10.1371/journal.pone.0011486 20628610

20. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC, Hamil C, et al. Genome Degeneration and Adaptation in a Nascent Stage of Symbiosis. Genome Biol Evol. 2014;6: 76–93. doi: 10.1093/gbe/evt210 24407854

21. Johnson SB, Krylova EM, Audzijonyte A, Sahling H, Vrijenhoek RC. Phylogeny and origins of chemosynthetic vesicomyid clams. Syst Biodivers. 2017;15: 346–360. doi: 10.1080/14772000.2016.1252438

22. Sharma PP, Zardus JD, Boyle EE, González VL, Jennings RM, McIntyre E, et al. Into the deep: A phylogenetic approach to the bivalve subclass Protobranchia. Mol Phylogenet Evol. 2013;69: 188–204. doi: 10.1016/j.ympev.2013.05.018 23742885

23. Ozawa G, Shimamura S, Takaki Y, Takishita K, Ikuta T, Barry JP, et al. Ancient occasional host switching of maternally transmitted bacterial symbionts of chemosynthetic vesicomyid clams. Genome Biol Evol. 2017;9: 2226–2236. doi: 10.1093/gbe/evx166 28922872

24. Kuwahara H, Takaki Y, Shimamura S, Yoshida T, Maeda T, Kunieda T, et al. Loss of genes for DNA recombination and repair in the reductive genome evolution of thioautotrophic symbionts of Calyptogena clams. BMC Evol Biol. 2011;11: 285. doi: 10.1186/1471-2148-11-285 21966992

25. Russell SL. Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses: a systematic review and meta-analysis. FEMS Microbiol Lett. 2019; fnz013.

26. Wernegreen JJ. Endosymbiont evolution: predictions from theory and surprises from genomes: Endosymbiont genome evolution. Ann N Y Acad Sci. 2015;1360: 16–35. doi: 10.1111/nyas.12740 25866055

27. Fontanez KM, Cavanaugh CM. Evidence for horizontal transmission from multilocus phylogeny of deep-sea mussel (Mytilidae) symbionts: Horizontal transmission of mussel symbionts. Environ Microbiol. 2014;16: 3608–3621. doi: 10.1111/1462-2920.12379 24428587

28. Won Y-J, Hallam SJ, O’Mullan GD, Pan IL, Buck KR, Vrijenhoek RC. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl Environ Microbiol. 2003;69: 6785–6792. doi: 10.1128/aem.69.11.6785-6792.2003 14602641

29. Wentrup C, Wendeberg A, Huang JY, Borowski C, Dubilier N. Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deep-sea mussels. ISME J. 2013;7: 1244–1247. doi: 10.1038/ismej.2013.5 23389105

30. Gustafson RG, Reid RG. Association of bacteria with larvae of the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar Biol. 1988;97: 389–401.

31. Russell SL, McCartney E, Cavanaugh CM. Transmission strategies in a chemosynthetic symbiosis: detection and quantification of symbionts in host tissues and their environment. Proc R Soc B Biol Sci. 2018;285: 9.

32. Krueger DM, Gustafson RG, Cavanaugh CM. Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol Bull. 1996;190: 195–202. doi: 10.2307/1542539 8652730

33. Ikuta T, Igawa K, Tame A, Kuroiwa T, Kuroiwa H, Aoki Y, et al. Surfing the vegetal pole in a small population: extracellular vertical transmission of an “intracellular” deep-sea clam symbiont. R Soc Open Sci. 2016;3: 160130. doi: 10.1098/rsos.160130 27293794

34. Cary SC, Giovannoni SJ. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci. 1993;90: 5695–5699. doi: 10.1073/pnas.90.12.5695 8100068

35. Breusing C, Johnson SB, Vrijenhoek RC, Young CR. Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams. Mol Ecol. 2019; mec.15224. doi: 10.1111/mec.15224 31478269

36. Dubilier N, Bergin C, Lott C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol. 2008;6: 725–740. doi: 10.1038/nrmicro1992 18794911

37. Duperron S, Halary S, Lorion J, Sibuet M, Gaill F. Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ Microbiol. 2008;10: 433–445. doi: 10.1111/j.1462-2920.2007.01465.x 18093159

38. Noellette Conway, Judith McDowell Capuzzo, Brian Fry. The Role of Endosymbiotic Bacteria in the Nutrition of Solemya velum: Evidence from a Stable Isotope Analysis of Endosymbionts and Host. Limnol Oceanogr. 1989;34: 249–255.

39. Reid Robert G. B., Bernard Frank R. Gutless Bivalves. Sci New Ser. 1980;208: 609–610.

40. Decker C, Olu K, Arnaud-Haond S, Duperron S. Physical proximity may promote lateral acquisition of bacterial symbionts in vesicomyid clams. López-García P, editor. PLoS ONE. 2013;8: e64830. doi: 10.1371/journal.pone.0064830 23861734

41. Ponnudurai R, Kleiner M, Sayavedra L, Petersen JM, Moche M, Otto A, et al. Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis. ISME J. 2016 [cited 3 Jan 2017]. Available: http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2016124a.html

42. Ikuta T, Takaki Y, Nagai Y, Shimamura S, Tsuda M, Kawagucci S, et al. Heterogeneous composition of key metabolic gene clusters in a vent mussel symbiont population. ISME J. 2016;10: 990. doi: 10.1038/ismej.2015.176 26418631

43. Brandvain Y, Goodnight C, Wade MJ. Horizontal Transmission Rapidly Erodes Disequilibria Between Organelle and Symbiont Genomes. Genetics. 2011;189: 397–404. doi: 10.1534/genetics.111.130906 21750254

44. Stewart FJ, Cavanaugh CM. Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)—Model systems for studies of symbiont–host adaptation. Antonie Van Leeuwenhoek. 2006;90: 343–360. doi: 10.1007/s10482-006-9086-6 17028934

45. Cocks LRM, Torsvik TH. Earth geography from 500 to 400 million years ago: a faunal and palaeomagnetic review. J Geol Soc. 2002;159: 631–644. doi: 10.1144/0016-764901-118

46. Biari Y, Klingelhoefer F, Sahabi M, Funck T, Benabdellouahed M, Schnabel M, et al. Opening of the central Atlantic Ocean: Implications for geometric rifting and asymmetric initial seafloor spreading after continental breakup: Opening of the Central Atlantic Ocean. Tectonics. 2017;36: 1129–1150. doi: 10.1002/2017TC004596

47. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabo G, et al. Population Genomics of Early Events in the Ecological Differentiation of Bacteria. Science. 2012;336: 48–51. doi: 10.1126/science.1218198 22491847

48. Rosen MJ, Davison M, Bhaya D, Fisher DS. Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche. Science. 2015;348: 1019–1023. doi: 10.1126/science.aaa4456 26023139

49. Chong RA, Park H, Moran NA. Genome Evolution of the Obligate Endosymbiont Buchnera aphidicola. Agashe D, editor. Mol Biol Evol. 2019;36: 1481–1489. doi: 10.1093/molbev/msz082 30989224

50. Ansorge R, Romano S, Sayavedra L, Kupczok A, Tegetmeyer HE, Dubilier N, et al. Diversity matters: Deep-sea mussels harbor multiple symbiont strains. bioRxiv. 2019 [cited 24 Jul 2019]. doi: 10.1101/531459

51. Ansari MA, Didelot X. Inference of the Properties of the Recombination Process from Whole Bacterial Genomes. Genetics. 2014;196: 253–265. doi: 10.1534/genetics.113.157172 24172133

52. Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009;3: 199–208. doi: 10.1038/ismej.2008.93 18830278

53. Rocha EPC. An Appraisal of the Potential for Illegitimate Recombination in Bacterial Genomes and Its Consequences: From Duplications to Genome Reduction. Genome Res. 2003;13: 1123–1132. doi: 10.1101/gr.966203 12743022

54. Neher RA. Genetic Draft, Selective Interference, and Population Genetics of Rapid Adaptation. Annu Rev Ecol Evol Syst. 2013;44: 195–215. doi: 10.1146/annurev-ecolsys-110512-135920

55. Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974;23: 23–25. 4407212

56. Nilsson AI, Koskiniemi S, Eriksson S, Kugelberg E, Hinton JCD, Andersson DI. Bacterial genome size reduction by experimental evolution. Proc Natl Acad Sci U S A. 2005;102: 12112–12116. doi: 10.1073/pnas.0503654102 16099836

57. Clayton AL, Jackson DG, Weiss RB, Dale C. Adaptation by Deletogenic Replication Slippage in a Nascent Symbiont. Mol Biol Evol. 2016;33: 1957–1966. doi: 10.1093/molbev/msw071 27189544

58. Merrikh CN, Merrikh H. Gene inversion potentiates bacterial evolvability and virulence. Nat Commun. 2018;9: 4662. doi: 10.1038/s41467-018-07110-3 30405125

59. Newton ILG, Bordenstein SR. Correlations Between Bacterial Ecology and Mobile DNA. Curr Microbiol. 2011;62: 198–208. doi: 10.1007/s00284-010-9693-3 20577742

60. Glémin S, Galtier N. Genome Evolution in Outcrossing Versus Selfing Versus Asexual Species. In: Anisimova M, editor. Evolutionary Genomics. Totowa, NJ: Humana Press; 2012. pp. 311–335. doi: 10.1007/978-1-61779-582-4_11

61. Allen JM, Reed DL, Perotti MA, Braig HR. Evolutionary Relationships of “Candidatus Riesia spp.,” Endosymbiotic Enterobacteriaceae Living within Hematophagous Primate Lice. Appl Environ Microbiol. 2007;73: 1659–1664. doi: 10.1128/AEM.01877-06 17220259

62. Lefevre C. Endosymbiont Phylogenesis in the Dryophthoridae Weevils: Evidence for Bacterial Replacement. Mol Biol Evol. 2004;21: 965–973. doi: 10.1093/molbev/msh063 14739242

63. Degnan PH, Lazarus AB, Brock CD, Wernegreen JJ. Host–Symbiont Stability and Fast Evolutionary Rates in an Ant–Bacterium Association: Cospeciation of Camponotus Species and Their Endosymbionts, Candidatus Blochmannia. Johnson K, editor. Syst Biol. 2004;53: 95–110. doi: 10.1080/10635150490264842 14965905

64. Moran N, Wernegreen J. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol. 2000;15: 321–326. doi: 10.1016/s0169-5347(00)01902-9 10884696

65. Takiya DM, Tran PL, Dietrich CH, Moran NA. Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol Ecol. 2006;15: 4175–4191. doi: 10.1111/j.1365-294X.2006.03071.x 17054511

66. Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of Psyllids and Their Primary Prokaryotic Endosymbionts. Appl Environ Microbiol. 2000;66: 2898–2905. doi: 10.1128/aem.66.7.2898-2905.2000 10877784

67. Thao ML, Gullan PJ, Baumann P. Secondary (-Proteobacteria) Endosymbionts Infect the Primary (-Proteobacteria) Endosymbionts of Mealybugs Multiple Times and Coevolve with Their Hosts. Appl Environ Microbiol. 2002;68: 3190–3197. doi: 10.1128/aem.68.7.3190-3197.2002 12088994

68. Santos-Garcia D, Vargas-Chavez C, Moya A, Latorre A, Silva FJ. Genome Evolution in the Primary Endosymbiont of Whiteflies Sheds Light on Their Divergence. Genome Biol Evol. 2015;7: 873–888. doi: 10.1093/gbe/evv038 25716826

69. Ruan J, Li H. Fast and accurate long-read assembly with wtdbg2. Bioinformatics; 2019 Jan. doi: 10.1101/530972

70. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. Wang J, editor. PLoS ONE. 2014;9: e112963. doi: 10.1371/journal.pone.0112963 25409509

71. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. 2013; arXiv:1303.3997.

72. Peng Y, Leung HCM, Yiu SM, Chin FYL. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics. 2012;28: 1420–1428. doi: 10.1093/bioinformatics/bts174 22495754

73. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J Comput Biol. 2012;19: 455–477. doi: 10.1089/cmb.2012.0021 22506599

74. Hyatt D, LoCascio PF, Hauser LJ, Uberbacher EC. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics. 2012;28: 2223–2230. doi: 10.1093/bioinformatics/bts429 22796954

75. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10: 421. doi: 10.1186/1471-2105-10-421 20003500

76. Lagesen K, Hallin P, Rodland EA, Staerfeldt H-H, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35: 3100–3108. doi: 10.1093/nar/gkm160 17452365

77. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25: 955–964. doi: 10.1093/nar/25.5.955 9023104

78. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25: 1043–1055. doi: 10.1101/gr.186072.114 25977477

79. Wu M, Eisen JA. A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 2008;9: 1.

80. Kelley DR, Schatz MC, Salzberg SL. Quake: quality-aware detection and correction of sequencing errors. Genome Biol. 2010;11: 1.

81. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, et al. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol. 2013;69: 313–319. doi: 10.1016/j.ympev.2012.08.023 22982435

82. Liu H, Cai S, Zhang H, Vrijenhoek RC. Complete mitochondrial genome of hydrothermal vent clam Calyptogena magnifica. Mitochondrial DNA Part A. 2016;27: 4333–4335. doi: 10.3109/19401736.2015.1089488 26462964

83. Plazzi F, Ribani A, Passamonti M. The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with Conchifera. BMC Genomics. 2013;14: 1. doi: 10.1186/1471-2164-14-1

84. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

85. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43: 491–498. doi: 10.1038/ng.806 21478889

86. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

87. Russell SL, Cavanaugh CM. Intrahost Genetic Diversity of Bacterial Symbionts Exhibits Evidence of Mixed Infections and Recombinant Haplotypes. Mol Biol Evol. 2017;34: 2747–2761. doi: 10.1093/molbev/msx188 29106592

88. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

89. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975;7: 256–276. doi: 10.1016/0040-5809(75)90020-9 1145509

90. Nei M, Li W-H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci. 1979;76: 5269–5273. doi: 10.1073/pnas.76.10.5269 291943

91. 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: 1.

92. Ponnudurai R, Sayavedra L, Kleiner M, Heiden SE, Thürmer A, Felbeck H, et al. Genome sequence of the sulfur-oxidizing Bathymodiolus thermophilus gill endosymbiont. Stand Genomic Sci. 2017;12. doi: 10.1186/s40793-017-0232-8

93. Darling AE, Mau B, Perna NT. progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement. Stajich JE, editor. PLoS ONE. 2010;5: e11147. doi: 10.1371/journal.pone.0011147 20593022

94. Guy L, Roat Kultima J, Andersson SGE. genoPlotR: comparative gene and genome visualization in R. Bioinformatics. 2010;26: 2334–2335. doi: 10.1093/bioinformatics/btq413 20624783

95. Leplae R, Lima-Mendez G, Toussaint A. ACLAME: A CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 2010;38: D57–D61. doi: 10.1093/nar/gkp938 19933762

96. Bi D, Xu Z, Harrison EM, Tai C, Wei Y, He X, et al. ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria. Nucleic Acids Res. 2012;40: D621–D626. doi: 10.1093/nar/gkr846 22009673

97. Ranwez V, Harispe S, Delsuc F, Douzery EJP. MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons. Murphy WJ, editor. PLoS ONE. 2011;6: e22594. doi: 10.1371/journal.pone.0022594 21949676

98. Yang Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 2007;24: 1586–1591. doi: 10.1093/molbev/msm088 17483113

99. Plazzi F, Puccio G, Passamonti M. Comparative Large-Scale Mitogenomics Evidences Clade-Specific Evolutionary Trends in Mitochondrial DNAs of Bivalvia. Genome Biol Evol. 2016;8: 2544–2564. doi: 10.1093/gbe/evw187 27503296

100. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28: 1647–1649. doi: 10.1093/bioinformatics/bts199 22543367

101. Ankenbrand MJ, Keller A. bcgTree: automatized phylogenetic tree building from bacterial core genomes. Chain F, editor. Genome. 2016;59: 783–791. doi: 10.1139/gen-2015-0175 27603265

102. Wernersson R. RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 2003;31: 3537–3539. doi: 10.1093/nar/gkg609 12824361

103. Katoh K, Standley DM. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol Biol Evol. 2013;30: 772–780. doi: 10.1093/molbev/mst010 23329690

104. Hedge J, Wilson DJ. Bacterial Phylogenetic Reconstruction from Whole Genomes Is Robust to Recombination but Demographic Inference Is Not. Vidaver AK, editor. mBio. 2014;5: e02158–14. doi: 10.1128/mBio.02158-14 25425237

105. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, et al. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. Prlic A, editor. PLoS Comput Biol. 2014;10: e1003537. doi: 10.1371/journal.pcbi.1003537 24722319

106. Behrensmeyer A, Turner A. Taxonomic occurrences of Bivalvia recorded in the Paleobiology Database. In: Fossilworks [Internet]. 2013. Available: http://fossilworks.org

107. Pojeta J, Runnegar B, Kriz J. Fordilla troyensis Barrande: The Oldest Known Pelecypod. Science. 1973;180: 866–868. doi: 10.1126/science.180.4088.866 17789257

108. Brasier MD, Hewitt RA, Brasier CJ. On the Late Precambrian–Early Cambrian Hartshill Formation of Warwickshire. Geol Mag. 1978;115: 21–36. doi: 10.1017/S0016756800040954

109. Battistuzzi FU, Tao Q, Jones L, Tamura K, Kumar S. RelTime Relaxes the Strict Molecular Clock throughout the Phylogeny. Martin B, editor. Genome Biol Evol. 2018;10: 1631–1636. doi: 10.1093/gbe/evy118 29878203

110. Tamura K, Tao Q, Kumar S. Theoretical Foundation of the RelTime Method for Estimating Divergence Times from Variable Evolutionary Rates. Russo C, editor. Mol Biol Evol. 2018;35: 1770–1782. doi: 10.1093/molbev/msy044 29893954

111. Britton T, Anderson CL, Jacquet D, Lundqvist S, Bremer K. Estimating Divergence Times in Large Phylogenetic Trees. Anderson F, editor. Syst Biol. 2007;56: 741–752. doi: 10.1080/10635150701613783 17886144

112. Sheridan PP, Freeman KH, Brenchley JE. Estimated Minimal Divergence Times of the Major Bacterial and Archaeal Phyla. Geomicrobiol J. 2003;20: 1–14. doi: 10.1080/01490450303891

113. De Maio N, Wilson DJ. The Bacterial Sequential Markov Coalescent. Genetics. 2017;206: 333–343. doi: 10.1534/genetics.116.198796 28258183

114. Polimis K, Rokem A, Hazelton B. Confidence Intervals for Random Forests in Python. J Open Source Softw. 2017;2: 124. doi: 10.21105/joss.00124

115. Didelot X, Lawson D, Darling A, Falush D. Inference of Homologous Recombination in Bacteria Using Whole-Genome Sequences. Genetics. 2010;186: 1435–1449. doi: 10.1534/genetics.110.120121 20923983


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