The Ctenophore Genome and the Evolutionary Origins of Neural Systems

The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes, and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well recognized in ctenophores, many bilaterian neuron-specific genes and genes of ‘classical’ neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.

[1]  F. Harrison Microscopic anatomy of invertebrates , 1991 .

[2]  U. Sieben,et al.  STRUCTURE, REGULATION AND FUNCTION OF NF-1d3 , 1994 .

[3]  C. Nielsen Animal Evolution: Interrelationships of the Living Phyla , 1995 .

[4]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[5]  J. Thompson,et al.  Multiple sequence alignment with Clustal X. , 1998, Trends in biochemical sciences.

[6]  R. Gillette,et al.  Single Neuron Analysis by Capillary Electrophoresis with Fluorescence Spectroscopy , 1998, Neuron.

[7]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[8]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[9]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[10]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[11]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

[12]  C. Fischer Handbook of statistical genetics: , 2002, Human Genetics.

[13]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[14]  J. Dzik Possible ctenophoran affinities of the precambrian “sea‐pen” Rangea , 2002, Journal of morphology.

[15]  O. Krishtal The ASICs: Signaling molecules? Modulators? , 2003, Trends in Neurosciences.

[16]  Rodrigo Lopez,et al.  Multiple sequence alignment with the Clustal series of programs , 2003, Nucleic Acids Res..

[17]  S. Hisano Vesicular glutamate transporters in the brain , 2003, Anatomical science international.

[18]  Gregory D. Schuler,et al.  Database resources of the National Center for Biotechnology Information: update , 2004, Nucleic acids research.

[19]  D. Balding,et al.  Handbook of statistical genetics , 2004 .

[20]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[21]  Robert D. Finn,et al.  The Pfam protein families database , 2004, Nucleic Acids Res..

[22]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[23]  Y. Panchin Evolution of gap junction proteins – the pannexin alternative , 2005, Journal of Experimental Biology.

[24]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[25]  Sathyanarayanan V. Puthanveettil,et al.  Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry , 2006, Cell.

[26]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[27]  A. Minelli Animal Evolution: Interrelationships of the Living Phyla , 2007 .

[28]  E. Birney,et al.  Velvet: algorithms for de novo short read assembly using de Bruijn graphs. , 2008, Genome research.

[29]  B. Lemaître,et al.  Toll-like receptors — taking an evolutionary approach , 2008, Nature Reviews Genetics.

[30]  David Q. Matus,et al.  Broad phylogenomic sampling improves resolution of the animal tree of life , 2008, Nature.

[31]  David Haussler,et al.  Using native and syntenically mapped cDNA alignments to improve de novo gene finding , 2008, Bioinform..

[32]  Corinne Da Silva,et al.  Phylogenomics Revives Traditional Views on Deep Animal Relationships , 2009, Current Biology.

[33]  Steven J. M. Jones,et al.  Abyss: a Parallel Assembler for Short Read Sequence Data Material Supplemental Open Access , 2022 .

[34]  M. Martindale,et al.  Assessing the root of bilaterian animals with scalable phylogenomic methods , 2009, Proceedings of the Royal Society B: Biological Sciences.

[35]  J. Jurka,et al.  Simple and fast classification of non-LTR retrotransposons based on phylogeny of their RT domain protein sequences. , 2009, Gene.

[36]  J. Sweedler,et al.  Capillary electrophoresis with electrospray ionization mass spectrometric detection for single-cell metabolomics. , 2009, Analytical chemistry.

[37]  B. Schierwater,et al.  Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis , 2009, PLoS biology.

[38]  L. Moroz On the Independent Origins of Complex Brains and Neurons , 2009, Brain, Behavior and Evolution.

[39]  A. Mele,et al.  Nova2 Regulates Neuronal Migration through an RNA Switch in Disabled-1 Signaling , 2010, Neuron.

[40]  B. Morgenstern,et al.  Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships , 2010, Molecular biology and evolution.

[41]  D. Licatalosi,et al.  Integrative Modeling Defines the Nova Splicing-Regulatory Network and Its Combinatorial Controls , 2010, Science.

[42]  R. Dingledine,et al.  Glutamate Receptor Ion Channels: Structure, Regulation, and Function , 2010, Pharmacological Reviews.

[43]  J. Mullikin,et al.  The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa , 2010, EvoDevo.

[44]  L. Holm,et al.  The Pfam protein families database , 2005, Nucleic Acids Res..

[45]  K. Nishikura Functions and regulation of RNA editing by ADAR deaminases. , 2010, Annual review of biochemistry.

[46]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[47]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[48]  Ulrich C. Klostermeier,et al.  Defining the origins of the NOD-like receptor system at the base of animal evolution. , 2011, Molecular biology and evolution.

[49]  L. Moroz,et al.  Phylogenomics reveals deep molluscan relationships , 2011, Nature.

[50]  L. Descarries,et al.  From glutamate co-release to vesicular synergy: vesicular glutamate transporters. , 2011, Nature reviews. Neuroscience.

[51]  S. Bengtson,et al.  Eoandromeda and the origin of Ctenophora , 2011, Evolution & development.

[52]  J. Sweedler,et al.  Metabolic differentiation of neuronal phenotypes by single-cell capillary electrophoresis-electrospray ionization-mass spectrometry. , 2011, Analytical chemistry.

[53]  D. Tautz,et al.  The evolutionary origin of orphan genes , 2011, Nature Reviews Genetics.

[54]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[55]  D. Hillis,et al.  Evolution of sodium channels predates the origin of nervous systems in animals , 2011, Proceedings of the National Academy of Sciences.

[56]  Y. Moriyama,et al.  Vesicular neurotransmitter transporter: bioenergetics and regulation of glutamate transport. , 2011, Biochemistry.

[57]  Laurie Goodman,et al.  Large and linked in scientific publishing , 2012, GigaScience.

[58]  Yiannis A. Savva,et al.  The ADAR protein family , 2012, Genome Biology.

[59]  Susumu Goto,et al.  KEGG for integration and interpretation of large-scale molecular data sets , 2011, Nucleic Acids Res..

[60]  Andrey A. Ptitsyn,et al.  Computational workflow for analysis of gain and loss of genes in distantly related genomes , 2012, BMC Bioinformatics.

[61]  B. Degnan,et al.  Independent evolution of striated muscles in cnidarians and bilaterians , 2012, Nature.

[62]  L. Moroz,et al.  Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei. , 2012, Molecular Phylogenetics and Evolution.

[63]  L. Moroz Phylogenomics Meets Neuroscience: How Many Times Might Complex Brains Have Evolved? , 2012, Acta biologica Hungarica.

[64]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[65]  K. Palczewski,et al.  From atomic structures to neuronal functions of g protein-coupled receptors. , 2013, Annual review of neuroscience.

[66]  E. Pennisi 2013 Society for Integrative and Comparative Biology Annual Meeting. Nervous system may have evolved twice. , 2013, Science.

[67]  M. Maldonado,et al.  Additional data to: Deep metazoan phylogeny: When different genes tell different stories , 2013 .

[68]  William A. Pastor,et al.  TETonic shift: biological roles of TET proteins in DNA demethylation and transcription , 2013, Nature Reviews Molecular Cell Biology.

[69]  L. Moroz,et al.  Single-neuron transcriptome and methylome sequencing for epigenomic analysis of aging. , 2013, Methods in molecular biology.

[70]  L. Moroz,et al.  Single-cell semiconductor sequencing. , 2013, Methods in molecular biology.

[71]  Nicholas H. Putnam,et al.  The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution , 2013, Science.

[72]  M. Long,et al.  New genes as drivers of phenotypic evolution , 2013, Nature Reviews Genetics.

[73]  Analysis of Gene Expression in Neurons and Synapses by Multi-color In Situ Hybridization , 2015 .

[74]  Supplemental Information 2: Kyoto Encyclopedia of genes and genomes. , 2022 .