A complete logical approach to resolve the evolution and dynamics of mitochondrial genome in bilaterians

Investigating how recombination might modify gene order during the evolution has become a routine part of mitochondrial genome analysis. A new method of genomic maps analysis based on formal logic is described. The purpose of this method is to 1) use mitochondrial gene order of current taxa as datasets 2) calculate rearrangements between all mitochondrial gene orders and 3) reconstruct phylogenetic relationships according to these calculated rearrangements within a tree under the assumption of maximum parsimony. Unlike existing methods mainly based on the probabilistic approach, the main strength of this new approach is that it calculates all the exact tree solutions with completeness and provides logical consequences as highly robust results. Moreover, this method infers all possible hypothetical ancestors and reconstructs character states for all internal nodes of the trees. We started by testing our method using the deuterostomes as a study case. Then, with sponges as an outgroup, we investigated the evolutionary history of mitochondrial genomes of 47 bilaterian phyla and emphasised the peculiar case of chaetognaths. This pilot work showed that the use of formal logic in a hypothetico-deductive background such as phylogeny (where experimental testing of hypotheses is impossible) is very promising to explore mitochondrial gene order in deuterostomes and should be applied to many other bilaterian clades.

[1]  J. Boore,et al.  Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. , 2002, Molecular biology and evolution.

[2]  Timothy M. Collins,et al.  Deducing the pattern of arthropod phytogeny from mitochondrial DNA rearrangements , 1995, Nature.

[3]  Sarah J. Bourlat,et al.  The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes , 2009, BMC Evolutionary Biology.

[4]  M. Dowton,et al.  Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. , 2003, Molecular biology and evolution.

[5]  Vineet Bafna,et al.  Sorting by Transpositions , 1998, SIAM J. Discret. Math..

[6]  R. Copley,et al.  Acoelomorph flatworms are deuterostomes related to Xenoturbella , 2011, Nature.

[7]  P. Higgs,et al.  The Relationship Between the Rate of Molecular Evolution and the Rate of Genome Rearrangement in Animal Mitochondrial Genomes , 2006, Journal of Molecular Evolution.

[8]  W. Brown,et al.  EVOLUTION OF ANIMAL MITOCHONDRIAL DNA: RELEVANCE FOR POPULATION BIOLOGY AND SYSTEMATICS , 1987 .

[9]  L. Podsiadlowski,et al.  19 Mitochondrial gene order in Metazoa – theme and variations , 2014 .

[10]  Matthias Bernt,et al.  A method for computing an inventory of metazoan mitochondrial gene order rearrangements , 2011, BMC Bioinformatics.

[11]  Balakrishnan Krishnamurthy Short proofs for tricky formulas , 2004, Acta Informatica.

[12]  Sarah J. Bourlat,et al.  Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. , 2008, Molecular phylogenetics and evolution.

[13]  S. Harzsch,et al.  4 The Chaetognatha : An anarchistic taxon between Protostomia and Deuterostomia , 2014 .

[14]  D. Sankoff,et al.  Gene order comparisons for phylogenetic inference: evolution of the mitochondrial genome. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  C. Gissi,et al.  Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species , 2008, Heredity.

[16]  M. Smith,et al.  A novel mitochondrial gene order in the crinoid echinoderm Florometra serratissima. , 2001, Molecular biology and evolution.

[17]  K. Peterson,et al.  Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships. , 2012, Molecular phylogenetics and evolution.

[18]  G. Rouse,et al.  New deep-sea species of Xenoturbella and the position of Xenacoelomorpha , 2016, Nature.

[19]  Matthias Bernt,et al.  An Algorithm for Inferring Mitogenome Rearrangements in a Phylogenetic Tree , 2008, RECOMB-CG.

[20]  P. Holland,et al.  Rare genomic changes as a tool for phylogenetics. , 2000, Trends in ecology & evolution.

[21]  Richard Friedberg,et al.  Efficient sorting of genomic permutations by translocation, inversion and block interchange , 2005, Bioinform..

[22]  B. Lang,et al.  Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. , 2005, Systematic biology.

[23]  Jotun Hein,et al.  A Large Version of the Small Parsimony Problem , 2003, WABI.

[24]  Ian P. Gent,et al.  Symmetry Breaking in Constraint Programming , 2000, ECAI.

[25]  Michael J. Smith,et al.  The complete mitochondrial genomes of the sea lily Gymnocrinus richeri and the feather star Phanogenia gracilis: signature nucleotide bias and unique nad4L gene rearrangement within crinoids. , 2006, Molecular phylogenetics and evolution.

[26]  Donald W. Loveland,et al.  A machine program for theorem-proving , 2011, CACM.

[27]  M. Rattray,et al.  The Evolution of tRNA-Leu Genes in Animal Mitochondrial Genomes , 2003, Journal of Molecular Evolution.

[28]  Roded Sharan,et al.  Genome Rearrangement with ILP , 2018, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[29]  F. Ronquist,et al.  Xenacoelomorpha is the sister group to Nephrozoa , 2016, Nature.

[30]  David Sankoff,et al.  Multiple Genome Rearrangement and Breakpoint Phylogeny , 1998, J. Comput. Biol..

[31]  Jeffrey L. Boore,et al.  Gene translocation links insects and crustaceans , 1998, Nature.

[32]  R. Belshaw,et al.  Simultaneous Molecular and Morphological Analysis of Braconid Relationships (Insecta: Hymenoptera: Braconidae) Indicates Independent mt-tRNA Gene Inversions Within a Single Wasp Family , 2002, Journal of Molecular Evolution.

[33]  Matthias Bernt,et al.  Bioinformatics methods for the comparative analysis of metazoan mitochondrial genome sequences. , 2013, Molecular phylogenetics and evolution.

[34]  Giuseppe Lancia,et al.  A Unified Integer Programming Model for Genome Rearrangement Problems , 2015, IWBBIO.

[35]  P. Stadler,et al.  Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: insights in phylogenetic relationships of Echinodermata. , 2010, Molecular phylogenetics and evolution.

[36]  João Meidanis,et al.  SCJ: A Breakpoint-Like Distance that Simplifies Several Rearrangement Problems , 2011, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[37]  Guillaume Fertin,et al.  Combinatorics of Genome Rearrangements , 2009, Computational molecular biology.

[38]  J. Boore,et al.  Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. , 1998, Current opinion in genetics & development.

[39]  B F Lang,et al.  Mitochondrial genome evolution and the origin of eukaryotes. , 1999, Annual review of genetics.

[40]  Hilary Putnam,et al.  A Computing Procedure for Quantification Theory , 1960, JACM.

[41]  A. Braband,et al.  Phylogeny and mitochondrial gene order variation in Lophotrochozoa in the light of new mitogenomic data from Nemertea , 2009, BMC Genomics.

[42]  Sarah J. Bourlat,et al.  The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis , 2010, BMC Evolutionary Biology.

[43]  Sarah J. Bourlat,et al.  Mitogenomics and phylogenomics reveal priapulid worms as extant models of the ancestral Ecdysozoan , 2006, Evolution & development.

[44]  A. Arndt,et al.  Mitochondrial gene rearrangement in the sea cucumber genus Cucumaria. , 1998, Molecular biology and evolution.

[45]  P. Stadler,et al.  Genetic aspects of mitochondrial genome evolution. , 2013, Molecular phylogenetics and evolution.

[46]  Tandy J. Warnow,et al.  New approaches for reconstructing phylogenies from gene order data , 2001, ISMB.

[47]  A. Austin,et al.  Evolutionary dynamics of a mitochondrial rearrangement "hot spot" in the Hymenoptera. , 1999, Molecular biology and evolution.

[48]  P. Pevzner,et al.  Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. , 2004, Genome research.

[49]  Matthias Bernt,et al.  A comprehensive analysis of bilaterian mitochondrial genomes and phylogeny. , 2013, Molecular phylogenetics and evolution.

[50]  J. Boore,et al.  The mitochondrial genome of the Sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. , 2002, Molecular biology and evolution.

[51]  Xin-She Yang,et al.  Introduction to Algorithms , 2021, Nature-Inspired Optimization Algorithms.

[52]  Matthias Bernt,et al.  Combinatorics of Tandem Duplication Random Loss Mutations on Circular Genomes , 2018, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[53]  R. Copley,et al.  Phylogenomic analysis of echinoderm class relationships supports Asterozoa , 2014, Proceedings of the Royal Society B: Biological Sciences.

[54]  Toby Walsh,et al.  Handbook of Constraint Programming (Foundations of Artificial Intelligence) , 2006 .

[55]  R. Zardoya,et al.  A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. , 2005, Molecular biology and evolution.

[56]  D. Lavrov,et al.  Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages , 2016, Genome biology and evolution.

[57]  Maria Emilia M. T. Walter,et al.  Reversal Distance of Signed Circular Chromosomes , 2000 .

[58]  J. Boore,et al.  Phylogenetic position of the Pentastomida and (pan)crustacean relationships , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[59]  Michael J. Smith,et al.  Complete mitochondrial genome DNA sequence for two ophiuroids and a holothuroid: the utility of protein gene sequence and gene maps in the analyses of deep deuterostome phylogeny. , 2004, Molecular phylogenetics and evolution.

[60]  P. Pevzner,et al.  Genome-scale evolution: reconstructing gene orders in the ancestral species. , 2002, Genome research.

[61]  M. Milinkovitch,et al.  Mitochondrial genome and nuclear sequence data support myzostomida as part of the annelid radiation. , 2007, Molecular biology and evolution.

[62]  M. Whiting,et al.  Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. , 2009, Molecular biology and evolution.

[63]  M. Dowton,et al.  Intramitochondrial recombination - is it why some mitochondrial genes sleep around? , 2001, Trends in ecology & evolution.

[64]  W. Brown,et al.  Mitochondrial gene arrangement of the horseshoe crab Limulus polyphemus L.: conservation of major features among arthropod classes. , 1997, Molecular biology and evolution.

[65]  Michael R. Genesereth,et al.  Logical foundations of artificial intelligence , 1987 .

[66]  P. Stadler,et al.  Computational methods for the analysis of mitochondrial genome rearrangements , 2014 .

[67]  A. Austin,et al.  Coexistence of minicircular and a highly rearranged mtDNA molecule suggests that recombination shapes mitochondrial genome organization. , 2014, Molecular biology and evolution.

[68]  J. Boore Animal mitochondrial genomes. , 1999, Nucleic acids research.