1887

Abstract

The genomic architecture of organisms, including nucleotide composition, can be highly variable, even among closely-related species. To better understand the causes leading to structural variation in genomes, information on distinct and diverse genomic features is needed. Malaria parasites are known for encompassing a wide range of genomic GC-content and it has long been thought that Plasmodium falciparum, the virulent malaria parasite of humans, has the most AT-biased eukaryotic genome. Here, I perform comparative genomic analyses of the most AT-rich eukaryotes sequenced to date, and show that the avian malaria parasites Plasmodium gallinaceum, P. ashfordi, and P. relictum have the most extreme coding sequences in terms of AT-bias. Their mean GC-content is 21.21, 21.22 and 21.60 %, respectively, which is considerably lower than the transcriptome of P. falciparum (23.79 %) and other eukaryotes. This information enables a better understanding of genome evolution and raises the question of how certain organisms are able to prosper despite severe compositional constraints.

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2018-01-23
2024-04-23
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References

  1. Jabbari K, Bernardi G. CpG doublets, CpG islands and Alu repeats in long human DNA sequences from different isochore families. Gene 1998; 224:123–128 [View Article][PubMed]
    [Google Scholar]
  2. Mouchiroud D, D'Onofrio G, Aïssani B, Macaya G, Gautier C et al. The distribution of genes in the human genome. Gene 1991; 100:181–187 [View Article][PubMed]
    [Google Scholar]
  3. Massey SE. The proteomic constraint and its role in molecular evolution. Mol Biol Evol 2008; 25:2557–2565 [View Article][PubMed]
    [Google Scholar]
  4. Musto H, Romero H, Zavala A, Jabbari K, Bernardi G. Synonymous codon choices in the extremely GC-poor genome of Plasmodium falciparum: compositional constraints and translational selection. J Mol Evol 1999; 49:27–35 [View Article][PubMed]
    [Google Scholar]
  5. Birdsell JA. Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 2002; 19:1181–1197 [View Article][PubMed]
    [Google Scholar]
  6. Pessia E, Popa A, Mousset S, Rezvoy C, Duret L et al. Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biol Evol 2012; 4:675–682 [View Article][PubMed]
    [Google Scholar]
  7. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J et al. The mosaic genome of warm-blooded vertebrates. Science 1985; 228:953–958 [View Article][PubMed]
    [Google Scholar]
  8. Galtier N, Lobry JR. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 1997; 44:632–636 [View Article][PubMed]
    [Google Scholar]
  9. Hurst LD, Merchant AR. High guanine-cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proc R Soc B Biol Sci 2001; 268:493–497 [View Article]
    [Google Scholar]
  10. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921 [View Article][PubMed]
    [Google Scholar]
  11. Bernardi G, Bernardi G. Compositional constraints and genome evolution. J Mol Evol 1986; 24:1–11 [View Article][PubMed]
    [Google Scholar]
  12. Xue HY, Forsdyke DR. Low-complexity segments in Plasmodium falciparum proteins are primarily nucleic acid level adaptations. Mol Biochem Parasitol 2003; 128:21–32 [View Article][PubMed]
    [Google Scholar]
  13. Zilversmit MM, Volkman SK, Depristo MA, Wirth DF, Awadalla P et al. Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Mol Biol Evol 2010; 27:2198–2209 [View Article][PubMed]
    [Google Scholar]
  14. Sueoka N. Correlation between base composition of deoxyribonucleic acid and amino acid composition of protein. Proc Natl Acad Sci USA 1961; 47:1141–1149 [View Article][PubMed]
    [Google Scholar]
  15. Galtier N, Piganeau G, Mouchiroud D, Duret L. GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 2001; 159:907–911[PubMed]
    [Google Scholar]
  16. Acosta S, Carela M, Garcia-Gonzalez A, Gines M, Vicens L et al. DNA repair is associated with information content in bacteria, archaea, and DNA viruses. J Hered 2015; 106:644–659 [View Article][PubMed]
    [Google Scholar]
  17. Garcia-Gonzalez A, Rivera-Rivera RJ, Massey SE. The presence of the DNA repair genes mutM, mutY, mutL, and mutS is related to proteome size in bacterial genomes. Front Genet 2012; 3:1–11 [View Article][PubMed]
    [Google Scholar]
  18. Wernegreen JJ, Funk DJ. Mutation exposed: a neutral explanation for extreme base composition of an endosymbiont genome. J Mol Evol 2004; 59:849–858 [View Article][PubMed]
    [Google Scholar]
  19. Hamilton WL, Claessens A, Otto TD, Kekre M, Fairhurst RM et al. Extreme mutation bias and high AT content in Plasmodium falciparum . Nucleic Acids Res 2017; 45:1889–1901 [View Article][PubMed]
    [Google Scholar]
  20. Hildebrand F, Meyer A, Eyre-Walker A. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 2010; 6:e1001107 [View Article][PubMed]
    [Google Scholar]
  21. Hershberg R, Petrov DA. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 2010; 6:e1001115 [View Article][PubMed]
    [Google Scholar]
  22. Gardner MJ, Hall N, Fung E, White O, Berriman M et al. Genome sequence of the human malaria parasite Plasmodium falciparum . Nature 2002; 419:498–511 [View Article][PubMed]
    [Google Scholar]
  23. Pollack Y, Katzen AL, Spira DT, Golenser J. The genome of Plasmodium falciparum. I: DNA base composition. Nucleic Acids Res 1982; 10:539–546 [View Article][PubMed]
    [Google Scholar]
  24. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax . Nature 2008; 455:757–763 [View Article][PubMed]
    [Google Scholar]
  25. Dávalos LM, Perkins SL. Saturation and base composition bias explain phylogenomic conflict in Plasmodium . Genomics 2008; 91:433–442 [View Article][PubMed]
    [Google Scholar]
  26. McCutchan TF, Dame JB, Miller LH, Barnwell J. Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science 1984; 225:808–811 [View Article][PubMed]
    [Google Scholar]
  27. Nikbakht H, Xia X, Hickey DA, Golding B. The evolution of genomic GC content undergoes a rapid reversal within the genus Plasmodium . Genome 2014; 57:507–511 [View Article][PubMed]
    [Google Scholar]
  28. Bensch S, Canbäck B, DeBarry JD, Johansson T, Hellgren O et al. The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biol Evol 2016; 8:1361–1373 [View Article][PubMed]
    [Google Scholar]
  29. Kissinger JC, DeBarry J. Genome cartography: charting the apicomplexan genome. Trends Parasitol 2011; 27:345–354 [View Article][PubMed]
    [Google Scholar]
  30. Videvall E, Cornwallis CK, Ahrén D, Palinauskas V, Valkiūnas G et al. The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Mol Ecol 2017; 26:2939–2958 [View Article][PubMed]
    [Google Scholar]
  31. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009; 37:D539–D543 [View Article][PubMed]
    [Google Scholar]
  32. Böhme U, Otto TD, Cotton J, Steinbiss S, Sanders M et al. Complete avian malaria parasite genomes reveal host-specific parasite evolution in birds and mammals. bioRxiv 20161–32
    [Google Scholar]
  33. Otto TD, Rayner JC, Böhme U, Pain A, Spottiswoode N et al. Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat Commun 2014; 5:4754 [View Article][PubMed]
    [Google Scholar]
  34. Otto TD, Böhme U, Jackson AP, Hunt M, Franke-Fayard B et al. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol 2014; 12:86 [View Article][PubMed]
    [Google Scholar]
  35. Valkiūnas G, Ashford RW, Bensch S, Killick-Kendrick R, Perkins S. A cautionary note concerning Plasmodium in apes. Trends Parasitol 2011; 27:231–232 [View Article][PubMed]
    [Google Scholar]
  36. Aurrecoechea C, Barreto A, Brestelli J, Brunk BP, Caler EV et al. AmoebaDB and MicrosporidiaDB: functional genomic resources for Amoebozoa and Microsporidia species. Nucleic Acids Res 2011; 39:D612–D619 [View Article][PubMed]
    [Google Scholar]
  37. Williams BA, Lee RC, Becnel JJ, Weiss LM, Fast NM et al. Genome sequence surveys of Brachiola algerae and Edhazardia aedis reveal microsporidia with low gene densities. BMC Genomics 2008; 9:200 [View Article][PubMed]
    [Google Scholar]
  38. Cornman RS, Chen YP, Schatz MC, Street C, Zhao Y et al. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 2009; 5:e1000466 [View Article][PubMed]
    [Google Scholar]
  39. Stover NA, Punia RS, Bowen MS, Dolins SB, Clark TG. Tetrahymena genome database Wiki: a community-maintained model organism database. Database 2012; 2012:bas007 [View Article][PubMed]
    [Google Scholar]
  40. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M et al. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 2006; 4:e286 [View Article][PubMed]
    [Google Scholar]
  41. Wiredu Boakye D, Jaroenlak P, Prachumwat A, Williams TA, Bateman KS et al. Decay of the glycolytic pathway and adaptation to intranuclear parasitism within Enterocytozoonidae microsporidia . Environ Microbiol 2017; 19:2077–2089 [View Article][PubMed]
    [Google Scholar]
  42. Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R et al. The genome of the social amoeba Dictyostelium discoideum . Nature 2005; 435:43–57 [View Article][PubMed]
    [Google Scholar]
  43. Youssef NH, Couger MB, Struchtemeyer CG, Liggenstoffer AS, Prade RA et al. The genome of the anaerobic fungus Orpinomyces sp. strain C1A reveals the unique evolutionary history of a remarkable plant biomass degrader. Appl Environ Microbiol 2013; 79:4620–4634 [View Article][PubMed]
    [Google Scholar]
  44. Chen Y, Pettis JS, Zhao Y, Liu X, Tallon LJ et al. Genome sequencing and comparative genomics of honey bee microsporidia, Nosema apis reveal novel insights into host-parasite interactions. BMC Genomics 2013; 14:451 [View Article][PubMed]
    [Google Scholar]
  45. Hunt VL, Tsai IJ, Coghlan A, Reid AJ, Holroyd N et al. The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat Genet 2016; 48:299–307 [View Article][PubMed]
    [Google Scholar]
  46. Coyne RS, Hannick L, Shanmugam D, Hostetler JB, Brami D et al. Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control. Genome Biol 2011; 12:R100 [View Article][PubMed]
    [Google Scholar]
  47. Xiong J, Wang G, Cheng J, Tian M, Pan X et al. Genome of the facultative scuticociliatosis pathogen Pseudocohnilembus persalinus provides insight into its virulence through horizontal gene transfer. Sci Rep 2015; 5:15470 [View Article][PubMed]
    [Google Scholar]
  48. Brownlee AG. Remarkably AT-rich genomic DNA from the anaerobic fungus Neocallimastix . Nucleic Acids Res 1989; 17:1327–1335 [View Article][PubMed]
    [Google Scholar]
  49. Wang TY, Chen HL, Lu MJ, Chen YC, Sung HM et al. Functional characterization of cellulases identified from the cow rumen fungus Neocallimastix patriciarum W5 by transcriptomic and secretomic analyses. Biotechnol Biofuels 2011; 4:24 [View Article][PubMed]
    [Google Scholar]
  50. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article][PubMed]
    [Google Scholar]
  51. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR et al. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 2010; 76:12–24 [View Article][PubMed]
    [Google Scholar]
  52. Wickham H. ggplot2: elegant graphics for data analysis New York: Springer: 2009
    [Google Scholar]
  53. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article][PubMed]
    [Google Scholar]
  54. R Core Team 2017; R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria www.r-project.org/
  55. Hansen KD, Brenner SE, Dudoit S. Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 2010; 38:e131 [View Article][PubMed]
    [Google Scholar]
  56. Benjamini Y, Speed TP. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res 2012; 40:e72 [View Article][PubMed]
    [Google Scholar]
  57. Hanafy RA, Elshahed MS, Liggenstoffer AS, Griffith GW, Youssef NH. Pecoramyces ruminantium, gen. nov., sp. nov., an anaerobic gut fungus from the feces of cattle and sheep. Mycologia 2017; 109:231–243 [View Article][PubMed]
    [Google Scholar]
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