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Journal of Molecular Evolution

, Volume 87, Issue 1, pp 7–15 | Cite as

Genomic Signatures Among Acanthamoeba polyphaga Entoorganisms Unveil Evidence of Coevolution

  • Víctor Serrano-SolísEmail author
  • Paulo Eduardo Toscano Soares
  • Sávio T. de Farías
Original Article
  • 74 Downloads

Abstract

The definition of a genomic signature (GS) is “the total net response to selective pressure”. Recent isolation and sequencing of naturally occurring organisms, hereby named entoorganisms, within Acanthamoeba polyphaga, raised the hypothesis of a common genomic signature despite their diverse and unrelated evolutionary origin. Widely accepted and implemented tests for GS detection are oligonucleotide relative frequencies (OnRF) and relative codon usage (RCU) surveys. A common pattern and strong correlations were unveiled from OnRFs among A. polyphaga's Mimivirus and virophage Sputnik. RCU showed a common A-T bias at third codon position. We expanded tests to the amoebal mitochondrial genome and amoeba-resistant bacteria, achieving strikingly coherent results to the aforementioned viral analyses. The GSs in these entoorganisms of diverse evolutionary origin are coevolutionarily conserved within an intracellular environment that provides sanctuary for species of ecological and biomedical relevance.

Keywords

Entoorganism Genomic Signature Virophage Mimivrus Acanthamoeba polyphaga Coevolution 

Notes

Acknowledgements

The authors thank Dr. Jonathas Abrahão for his valuable comments. This work was supported by a postdoctoral grant from PNPD/CAPES to VSS.

Author Contributions

VSS and STF conceived the project. VSS designed the experiments. VSS and PETS performed the experiments. VSS, STF and PETS analyzed the data. VSS and PETS wrote the paper.

Compliance with Ethical Standards

Competing interests

The authors declare no competing interests.

References

  1. Abe T, Kanaya S, Kinouchi M, Ichiba Y, Kozuki T, Ikemura T (2003) Informatics for unveiling hidden genome signatures. Genome Res 13(4):693–702Google Scholar
  2. Abergel C, Rudinger-Thirion J, Giegé R, Claverie JM (2007) Virus-encoded aminoacyl-tRNA synthetases: structural and functional characterization of mimivirus TyrRS and MetRS. J Virol 81(22):12406–12417Google Scholar
  3. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA 108:17486–17491.  https://doi.org/10.1073/pnas.1110889108 Google Scholar
  4. Benson DA, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) GenBank. Nucleic Acids Res 42:D32–D37.  https://doi.org/10.1093/nar/gkt1030 Google Scholar
  5. Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–792Google Scholar
  6. Berdal BP, Mehl R, Meidell NK, Lorentzen-Styr A-M, Scheel O (1996) Field investigations of tularemia in Norway. FEMS Immunol Med Microbiol 13:191–195Google Scholar
  7. Blaisdell BE, Campbell AM, Karlin S (1996) Similarities and dissimilarities of phage genomes. Proc Natl Acad Sci USA 93(12):5854–5859Google Scholar
  8. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, Robert C, Azza S, Sun S, Rossmann MG, Suzan-Monti M, La Scola B, Koonin EV, Raoult D (2009) Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci USA 106(51):21848–21853.  https://doi.org/10.1073/pnas.0911354106 Google Scholar
  9. Brister JR, Ako-Adjei D, Bao Y, Blinkova O (2015) NCBI viral genomes resource. Nucleic Acids Res 43:D571–577.  https://doi.org/10.1093/nar/gku1207 Google Scholar
  10. Burge C, Campbell AM, Karlin S (1992) Over- and under-representation of short oligonucleotides in DNA sequences. Proc Natl Acad Sci USA 89(4):1358–1362Google Scholar
  11. Campbell A, Mrázek J, Karlin S (1999) Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc Natl Acad Sci USA 96(16):9184–9189Google Scholar
  12. Deschavanne P, Giron A, Vilain J, Dufraigne C, Fertil B (2000) Genomic signature is preserved in short DNA fragments. In: Bio-Informatics and Biomedical Engineering, Proceedings. IEEE International Symposium on. IEEE, 2000. pp 161–167.  https://doi.org/10.1109/BIBE.2000.889603
  13. Desnues C, La Scola B, Yutin N, Fournous G, Robert C, Azza S, Jardot P, Monteil S, Campocasso A, Koonin EV, Raoult D (2012) Provirophages and transpovirons as the diverse mobilome of giant viruses. Proc Natl Acad Sci USA 109(44):18078–18083.  https://doi.org/10.1073/pnas.1208835109 Google Scholar
  14. Duan J, Antezana MA (2003) Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J Mol Evol 57(6):694–701Google Scholar
  15. Filée J (2015) Genomic comparison of closely related Giant Viruses supports an accordion-like model of evolution. Front Microbiol 6:593.  https://doi.org/10.3389/fmicb.2015.00593 Google Scholar
  16. Foerstner KU, von Mering C, Hooper SD, Bork P (2005) Environments shape the nucleotide composition of genomes. EMBO Rep 6(12):1208–1213Google Scholar
  17. Forterre P (2010) Defining life: the virus viewpoint. Orig Life Evol Biosph 40(2):151–60.  https://doi.org/10.1007/s11084-010-9194-1 Google Scholar
  18. Frick DN, Richardson CC (2001) DNA primases. Annu Rev Biochem 70:39–80Google Scholar
  19. Gentles AJ, Karlin S (2001 Apr) Genome-scale compositional comparisons in eukaryotes. Genome Res 11(4):540–546Google Scholar
  20. Glass JI, Lefkowitz EJ, Glass JS, Heiner CR, Chen EY, Cassell GH (2000) The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature 407(6805):757–762Google Scholar
  21. Greub G, Raoult D (2004 Apr) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17(2):413–433Google Scholar
  22. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9Google Scholar
  23. Jernigan RW, Baran RH (2002) Pervasive properties of the genomic signature. BMC Genom 3(1):23Google Scholar
  24. Karlin S (1996) Genomic Signature and Bacterial Phylogeny. In: Bacterial genomes: physical structures and analysis, De Bruijn FJ, Lupski JR, Weinstock G (eds.). Chapman & Hall, New YorkGoogle Scholar
  25. Karlin S (1998 Oct) Global dinucleotide signatures and analysis of genomic heterogeneity. Curr Opin Microbiol 1(5):598–610Google Scholar
  26. Karlin S, Burge C (1995 Jul) Dinucleotide relative abundance extremes: a genomic signature. Trends Genet 11(7):283–290Google Scholar
  27. Karlin S, Cardon LR (1994) Computational DNA sequence analysis. Annu Rev Microbiol 48:619–654Google Scholar
  28. Karlin S, Ladunga I, Blaisdell BE (1994) Heterogeneity of genomes: measures and values. Proc Natl Acad Sci USA 91(26):12837–12841Google Scholar
  29. Khan NA, Siddiqui R (2014) Predator vs aliens: bacteria interactions with Acanthamoeba. Parasitology 141(7):869–874.  https://doi.org/10.1017/S003118201300231X Google Scholar
  30. Kirzhner V, Paz A, Volkovich Z, Nevo E, Korol A (2007) Different clustering of genomes across life using the A-T-C-G and degenerate R-Y alphabets: early and late signaling on genome evolution? J Mol Evol 64(4):448–456Google Scholar
  31. Kozobay-Avraham L, Hosid S, Bolshoy A (2006 May) Involvement of DNA curvature in intergenic regions of prokaryotes. Nucleic Acids Res 5(8):2316–2327Google Scholar
  32. Kumar S, Kumari R, Sharma V (2016) Coevolution mechanisms that adapt viruses to genetic code variations implemented in their hosts. J Genet 95(1):3–12Google Scholar
  33. Kunec D, Osterrieder N (2016) Codon pair bias is a direct consequence of dinucleotide bias. Cell Rep 14(1):55–67.  https://doi.org/10.1016/j.celrep.2015.12.011 Google Scholar
  34. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D (2003) A giant virus in amoebae. Science 299(5615):2033Google Scholar
  35. La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D (2008) The virophage as a unique parasite of the giant mimivirus. Nature 455(7209):100–104.  https://doi.org/10.1038/nature07218 Google Scholar
  36. Legendre M, Santini S, Rico A, Abergel C, Claverie JM (2011) Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J 8:99.  https://doi.org/10.1186/1743-422X-8-99 Google Scholar
  37. Lerat E, Capy P, Biémont C (2002) The relative abundance of dinucleotides in transposable elements in five species. Mol Biol Evol 19(6):964–967Google Scholar
  38. McDowall KJ, Lin-Chao S, Cohen SN (1994) A + U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269(14):10790–10796Google Scholar
  39. Moliner C, Fournier PE, Raoult D (2010) Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev 34(3):281–294.  https://doi.org/10.1111/j.1574-6976.2010.00209.x Google Scholar
  40. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108(5):583–586Google Scholar
  41. Mrázek J (2009) Phylogenetic signals in DNA composition: limitations and prospects. Mol Biol Evol 26(5):1163–1169.  https://doi.org/10.1093/molbev/msp032.Google Scholar
  42. Mrázek J, Karlin S (2007) Distinctive features of large complex virus genomes and proteomes. Proc Natl Acad Sci USA 104(12):5127–5132Google Scholar
  43. Nussinov R (1987) Theoretical molecular biology: prospectives and perspectives. J Theor Biol 125(2):219–235Google Scholar
  44. Pagnier I, Yutin N, Croce O, Makarova KS, Wolf YI, Benamar S, Raoult D, Koonin EV, La Scola B (2015) Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae. Biol Direct 10:13.  https://doi.org/10.1186/s13062-015-0043-z Google Scholar
  45. Paz A, Kirzhner V, Nevo E, Korol A (2006 Jan) Coevolution of DNA-interacting proteins and genome “dialect”. Mol Biol Evol 23(1):56–64Google Scholar
  46. Plotkin JB, Kudla G (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12(1):32–42  https://doi.org/10.1038/nrg2899 Google Scholar
  47. Prabha R, Singh DP (2014) Analysis of dinucleotide bias and genomic signatures across cyanobacterial genomes. J Adv Biotechnol 3(3):2348–6201Google Scholar
  48. Prasaot BVLS, Vemuri MC (2007) Genome analysis for nucleotide interactions in fully sequenced genomes of selective prokaryotes. J Biosci 23(3):255–263Google Scholar
  49. Pride DT, Wassenaar TM, Ghose C, Blaser MJ (2006) Evidence of host-virus co-evolution in tetranucleotide usage patterns of bacteriophages and eukaryotic viruses. BMC Genom 7:8Google Scholar
  50. Raoult D, Forterre P (2008) Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 6(4):315–319.  https://doi.org/10.1038/nrmicro1858 Google Scholar
  51. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306(5700):1344–1350Google Scholar
  52. Ravenhall M, Škunca N, Lassalle F, Dessimoz C (2015) Inferring horizontal gene transfer. PLoS Comput Biol 11(5):e1004095.  https://doi.org/10.1371/journal.pcbi.1004095 Google Scholar
  53. Robins H, Krasnitz M, Barak H, Levine AJ (2005 Dec) A relative-entropy algorithm for genomic fingerprinting captures host-phage similarities. J Bacteriol 187(24):8370–8374.Google Scholar
  54. Rossum van G, Drake JR, Fred L (2010) Python tutorial. HistoryGoogle Scholar
  55. Serrano-Solís V, Cocho G, José MV (2016) Genomic signatures in viral sequences by in-frame and out-frame mutual information. J Theor Biol 403:1–9.  https://doi.org/10.1016/j.jtbi.2016.05.014 Google Scholar
  56. Sharp PM, Li WH (1987) The codon Adaptation Index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295Google Scholar
  57. Sharp PM, Tuohy TM, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 14(13):5125–5143Google Scholar
  58. Silva LC, Almeida GM, Assis FL, Albarnaz JD, Boratto PV, Dornas FP, Andrade KR, La Scola B, Kroon EG, da Fonseca FG, Abrahão JS (2015) Modulation of the expression of mimivirus-encoded translation-related genes in response to nutrient availability during Acanthamoeba castellanii infection. Front Microbiol 6:539.  https://doi.org/10.3389/fmicb.2015.00539 Google Scholar
  59. Sinden RR (1994) DNA structure and function. Academic Press, San DiegoGoogle Scholar
  60. Suzuki H, Sota M, Brown CJ, Top EM (2008) Using Mahalanobis distance to compare genomic signatures between bacterial plasmids and chromosomes. Nucleic Acids Res 36(22):e147.  https://doi.org/10.1093/nar/gkn753 Google Scholar
  61. van Passel MW, Kuramae EE, Luyf AC, Bart A, Boekhout T (2006) The reach of the genome signature in prokaryotes. BMC Evol Biol 6:84Google Scholar
  62. Xia X, Wei T, Xie Z, Danchin A (2002) Genomic changes in nucleotide and dinucleotide frequencies in Pasteurella multocida cultured under high temperature. Genetics 161(4):1385–1394Google Scholar
  63. Yoosuf N, Yutin N, Colson P et al (2012) Related giant viruses in distant locations and different habitats: acanthamoeba polyphaga moumouvirus represents a third lineage of the mimiviridae that is close to the megavirus lineage. Genome Biol Evolut 4(12):1324–1330.  https://doi.org/10.1093/gbe/evs109 Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratório de Genética Evolutiva Paulo Leminsk, Departamento de Biologia Molecular, Centro de Ciencias Exatas e da NaturezaUniversidade Federal da ParaíbaJoão PessoaBrazil

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