Detection of Prokaryotic Genes in the Amphimedon queenslandica Genome

Horizontal gene transfer (HGT) is common between prokaryotes and phagotrophic eukaryotes. In metazoans, the scale and significance of HGT remains largely unexplored but is usually linked to a close association with parasites and endosymbionts. Marine sponges (Porifera), which host many microorganisms in their tissues and lack an isolated germ line, are potential carriers of genes transferred from prokaryotes. In this study, we identified a number of potential horizontally transferred genes within the genome of the sponge, Amphimedon queenslandica. We further identified homologs of some of these genes in other sponges. The transferred genes, most of which possess catalytic activity for carbohydrate or protein metabolism, have assimilated host genome characteristics and are actively expressed. The diversity of functions contributed by the horizontally transferred genes is likely an important factor in the adaptation and evolution of A. queenslandica. These findings highlight the potential importance of HGT on the success of sponges in diverse ecological niches.

[1]  C. Conaco,et al.  Comparative transcriptome analysis reveals insights into the streamlined genomes of haplosclerid demosponges , 2016, Scientific Reports.

[2]  R. Murphy,et al.  Horizontal functional gene transfer from bacteria to fishes , 2015, Scientific Reports.

[3]  David Bryant,et al.  Endosymbiotic origin and differential loss of eukaryotic genes , 2015, Nature.

[4]  J. Jessen,et al.  Matrix metalloproteinase function in non-mammalian model organisms. , 2015, Frontiers in bioscience.

[5]  Selene L. Fernandez-Valverde,et al.  Deep developmental transcriptome sequencing uncovers numerous new genes and enhances gene annotation in the sponge Amphimedon queenslandica , 2015, BMC Genomics.

[6]  Gos Micklem,et al.  Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes , 2015, Genome Biology.

[7]  S. Degnan.  Think laterally: horizontal gene transfer from symbiotic microbes may extend the phenotype of marine sessile hosts , 2014, Front. Microbiol..

[8]  C. Prigent-Combaret,et al.  Frequent, independent transfers of a catabolic gene from bacteria to contrasted filamentous eukaryotes , 2014, Proceedings of the Royal Society B: Biological Sciences.

[9]  A. Nederbragt,et al.  The chloroplast genome of the diatom Seminavis robusta: new features introduced through multiple mechanisms of horizontal gene transfer. , 2014, Marine genomics.

[10]  N. Satoh,et al.  Massive Gene Transfer and Extensive RNA Editing of a Symbiotic Dinoflagellate Plastid Genome , 2014, Genome biology and evolution.

[11]  L. Boto,et al.  Horizontal gene transfer in the acquisition of novel traits by metazoans , 2014, Proceedings of the Royal Society B: Biological Sciences.

[12]  Guiling Sun,et al.  The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis , 2013, BMC Genomics.

[13]  Neil D. Rawlings,et al.  MEROPS: the database of proteolytic enzymes, their substrates and inhibitors , 2013, Nucleic Acids Res..

[14]  J. Werren,et al.  Characterization of an Ancient Lepidopteran Lateral Gene Transfer , 2013, PloS one.

[15]  M. Syvanen,et al.  Evolutionary implications of horizontal gene transfer. , 2012, Annual review of genetics.

[16]  W. Guo,et al.  EcpA, an extracellular protease, is a specific virulence factor required by Xanthomonas oryzae pv. oryzicola but not by X. oryzae pv. oryzae in rice. , 2012, Microbiology.

[17]  R. Friedman,et al.  Codon Usage Methods for Horizontal Gene Transfer Detection Generate an Abundance of False Positive and False Negative Results , 2012, Current Microbiology.

[18]  B. Degnan,et al.  Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions , 2012, BMC Genomics.

[19]  D. Fitzpatrick.  Horizontal gene transfer in fungi. , 2012, FEMS microbiology letters.

[20]  M. Grynberg,et al.  Recurrent Horizontal Transfer of Bacterial Toxin Genes to Eukaryotes , 2012, Molecular biology and evolution.

[21]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[22]  J. Reitner,et al.  A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy , 2011, BMC Evolutionary Biology.

[23]  S. Degnan,et al.  A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function , 2011, BMC Evolutionary Biology.

[24]  M. Ilan,et al.  Diversity of sponge mitochondrial introns revealed by cox 1 sequences of Tetillidae , 2010, BMC Evolutionary Biology.

[25]  Todd H. Oakley,et al.  The Amphimedon queenslandica genome and the evolution of animal complexity , 2010, Nature.

[26]  N. Moran,et al.  Lateral Transfer of Genes from Fungi Underlies Carotenoid Production in Aphids , 2010, Science.

[27]  A. Ereskovsky.  The Comparative Embryology of Sponges , 2010 .

[28]  K. Shin‐ya,et al.  Sponge-derived Streptomyces producing isoprenoids via the mevalonate pathway. , 2010, Journal of natural products.

[29]  Erich Bornberg-Bauer,et al.  Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species , 2010, Science.

[30]  N. Funayama.  The stem cell system in demosponges: Insights into the origin of somatic stem cells , 2010, Development, growth & differentiation.

[31]  H. Lumbsch,et al.  Ancient Horizontal Gene Transfer from Bacteria Enhances Biosynthetic Capabilities of Fungi , 2009, PloS one.

[32]  G. Daum,et al.  Phosphatidylserine decarboxylases, key enzymes of lipid metabolism , 2009, IUBMB life.

[33]  V. Andrésdóttir,et al.  The AsaP1 Peptidase of Aeromonas salmonicida subsp. achromogenes Is a Highly Conserved Deuterolysin Metalloprotease (Family M35) and a Major Virulence Factor , 2008, Journal of bacteriology.

[34]  T. Bosch,et al.  Compagen, a comparative genomics platform for early branching metazoan animals, reveals early origins of genes regulating stem‐cell differentiation , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[35]  H. Alexandre,et al.  Characterization of EprA, a major extracellular protein of Oenococcus oeni with protease activity. , 2008, International journal of food microbiology.

[36]  P. Davies,et al.  Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes , 2008, PloS one.

[37]  G. Butler,et al.  Evidence of recent interkingdom horizontal gene transfer between bacteria and Candida parapsilosis , 2008, BMC Evolutionary Biology.

[38]  M. Meselson,et al.  Massive Horizontal Gene Transfer in Bdelloid Rotifers , 2008, Science.

[39]  Andrés Moya,et al.  Estimating the extent of horizontal gene transfer in metagenomic sequences , 2008, BMC Genomics.

[40]  Kenneth S. Kosik,et al.  Reconstructing ancestral genome content based on symmetrical best alignments and Dollo parsimony , 2008, Bioinform..

[41]  P. Long,et al.  Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins , 2008, Proceedings of the National Academy of Sciences.

[42]  S. Richards,et al.  Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes , 2007, Science.

[43]  Nicholas H. Putnam,et al.  Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization , 2007, Science.

[44]  M. W. Taylor,et al.  Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential , 2007, Microbiology and Molecular Biology Reviews.

[45]  Eugene V Koonin,et al.  Evolution of glyoxylate cycle enzymes in Metazoa: evidence of multiple horizontal transfer events and pseudogene formation , 2006, Biology Direct.

[46]  Thomas Lengauer,et al.  Improved scoring of functional groups from gene expression data by decorrelating GO graph structure , 2006, Bioinform..

[47]  P. Bork,et al.  Environments shape the nucleotide composition of genomes , 2005, EMBO reports.

[48]  V. Rodwell,et al.  The 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductases , 2004, Genome Biology.

[49]  M. Garson,et al.  Biosynthetic pathways to isocyanides and isothiocyanates; precursor incorporation studies on terpene metabolites in the tropical marine sponges Amphimedon terpenensis and Axinyssa n.sp. , 2004, Organic & biomolecular chemistry.

[50]  N. Satoh,et al.  The evolutionary origin of animal cellulose synthase , 2004, Development Genes and Evolution.

[51]  W. Doolittle,et al.  Lateral gene transfer and the origins of prokaryotic groups. , 2003, Annual review of genetics.

[52]  J. Lake,et al.  Horizontal gene transfer accelerates genome innovation and evolution. , 2003, Molecular biology and evolution.

[53]  H. Won,et al.  Horizontal gene transfer from flowering plants to Gnetum , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Jeffrey D. Palmer,et al.  Widespread horizontal transfer of mitochondrial genes in flowering plants , 2003, Nature.

[55]  Eduardo P C Rocha,et al.  Base composition bias might result from competition for metabolic resources. , 2002, Trends in genetics : TIG.

[56]  J. Braekman,et al.  Cellular location of (2R, 3R, 7Z)-2-aminotetradec-7-ene-1, 3-diol, a potent antimicrobial metabolite produced by the Caribbean sponge Haliclona vansoesti , 2001, Cell and Tissue Research.

[57]  M. Ragan.  On surrogate methods for detecting lateral gene transfer. , 2001, FEMS microbiology letters.

[58]  B. M. Lange,et al.  Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[60]  V. Rodwell,et al.  Sequence comparisons reveal two classes of 3-hydroxy-3-methylglutaryl coenzyme A reductase. , 1999, Molecular genetics and metabolism.

[61]  H. Ochman,et al.  Molecular archaeology of the Escherichia coli genome. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[62]  H. Ochman,et al.  Amelioration of Bacterial Genomes: Rates of Change and Exchange , 1997, Journal of Molecular Evolution.

[63]  R. Croteau,et al.  Terpenoid metabolism. , 1995, The Plant cell.

[64]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[65]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[66]  M. Gouy,et al.  Codon catalog usage and the genome hypothesis. , 1980, Nucleic acids research.

[67]  Julie C. Dunning Hotopp,et al.  Horizontal gene transfer between bacteria and animals. , 2011, Trends in genetics : TIG.

[68]  David Moreira,et al.  Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. , 2011, Molecular biology and evolution.

[69]  E. Koonin,et al.  Horizontal gene transfer in prokaryotes: quantification and classification. , 2001, Annual review of microbiology.