Horizontal Gene Transfer and Gene Duplication of β-Fructofuranosidase Confer Lepidopteran Insects Metabolic Benefits

Abstract Horizontal gene transfer (HGT) is a potentially critical source of material for ecological adaptation and the evolution of novel genetic traits. However, reports on posttransfer duplication in organism genomes are lacking, and the evolutionary advantages conferred on the recipient are generally poorly understood. Sucrase plays an important role in insect physiological growth and development. Here, we performed a comprehensive analysis of the evolution of insect β-fructofuranosidase transferred from bacteria via HGT. We found that posttransfer duplications of β-fructofuranosidase were widespread in Lepidoptera and sporadic occurrences of β-fructofuranosidase were found in Coleoptera and Hymenoptera. β-fructofuranosidase genes often undergo modifications, such as gene duplication, differential gene loss, and changes in mutation rates. Lepidopteran β-fructofuranosidase gene (SUC) clusters showed marked divergence in gene expression patterns and enzymatic properties in Bombyx mori (moth) and Papilio xuthus (butterfly). We generated SUC1 mutations in B. mori using CRISPR/Cas9 to thoroughly examine the physiological function of SUC. BmSUC1 mutant larvae were viable but displayed delayed growth and reduced sucrase activities that included susceptibility to the sugar mimic alkaloid found in high concentrations in mulberry. BmSUC1 served as a critical sucrase and supported metabolic homeostasis in the larval midgut and silk gland, suggesting that gene transfer of β-fructofuranosidase enhanced the digestive and metabolic adaptation of lepidopteran insects. These findings highlight not only the universal function of β-fructofuranosidase with a link to the maintenance of carbohydrate metabolism but also an underexplored function in the silk gland. This study expands our knowledge of posttransfer duplication and subsequent functional diversification in the adaptive evolution and lineage-specific adaptation of organisms.

[1]  Yu Tang,et al.  Imaginal disc growth factor maintains cuticle structure and controls melanization in the spot pattern formation of Bombyx mori , 2020, PLoS genetics.

[2]  Xiang Sun,et al.  Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits , 2020, The ISME Journal.

[3]  E. Nevo,et al.  Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat , 2020, Science.

[4]  M. Goodisman,et al.  Gene duplication in the honeybee: Patterns of DNA methylation, gene expression, and genomic environment. , 2020, Molecular biology and evolution.

[5]  T. Shimada,et al.  Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects , 2019, Molecular ecology.

[6]  R. Li,et al.  Gene duplication and subsequent functional diversification of sucrose hydrolase in Papilio xuthus , 2019, Insect molecular biology.

[7]  Q. Xia,et al.  Deep Insight into the Transcriptome of the Single Silk Gland of Bombyx mori , 2019, International journal of molecular sciences.

[8]  E. Danchin,et al.  Gene copy number variations as signatures of adaptive evolution in the parthenogenetic, plant‐parasitic nematode Meloidogyne incognita , 2019, Molecular ecology.

[9]  Q. Xia,et al.  Cross-talk between juvenile hormone and ecdysone regulates transcription of fibroin modulator binding protein-1 in Bombyx mori. , 2019, International journal of biological macromolecules.

[10]  A. Fujiyama,et al.  High-quality genome assembly of the silkworm, Bombyx mori. , 2019, Insect biochemistry and molecular biology.

[11]  M. Mandrioli,et al.  The Evolutionary History and Functional Divergence of Trehalase (treh) Genes in Insects , 2019, Front. Physiol..

[12]  M. Reichelt,et al.  An Insect Counteradaptation against Host Plant Defenses Evolved through Concerted Neofunctionalization , 2019, Molecular biology and evolution.

[13]  C. Secombes,et al.  Insights into the Evolution of the Suppressors of Cytokine Signaling (SOCS) Gene Family in Vertebrates , 2018, Molecular biology and evolution.

[14]  Yi Guan,et al.  Two Methods for Mapping and Visualizing Associated Data on Phylogeny Using Ggtree. , 2018, Molecular biology and evolution.

[15]  A. McGregor,et al.  Homeobox Gene Duplication and Divergence in Arachnids , 2018, Molecular biology and evolution.

[16]  Xiaotong Li,et al.  Expression plasticity and evolutionary changes extensively shape the sugar‐mimic alkaloid adaptation of nondigestive glucosidase in lepidopteran mulberry‐specialist insects , 2018, Molecular ecology.

[17]  Q. Xia,et al.  Improved strength of silk fibers in Bombyx mori trimolters induced by an anti-juvenile hormone compound. , 2018, Biochimica et biophysica acta. General subjects.

[18]  Y. Meng,et al.  BmSUC1 is essential for glycometabolism modulation in the silkworm, Bombyx mori. , 2018, Biochimica et biophysica acta. Gene regulatory mechanisms.

[19]  Y. Meng,et al.  D181A Site-Mutagenesis Enhances Both the Hydrolyzing and Transfructosylating Activities of BmSUC1, a Novel β-Fructofuranosidase in the Silkworm Bombyx mori , 2018, International journal of molecular sciences.

[20]  Huawei He,et al.  Biochemical characterization and functional analysis of invertase Bmsuc1 from silkworm, Bombyx mori. , 2018, International journal of biological macromolecules.

[21]  J. McCutcheon,et al.  Functional horizontal gene transfer from bacteria to eukaryotes , 2017, Nature Reviews Microbiology.

[22]  H. Su,et al.  Secreted glycoprotein BmApoD1 plays a critical role in anti-oxidation and anti-apoptosis in Bombyx mori. , 2018, Biochemical and biophysical research communications.

[23]  Yuncai Liu,et al.  Comparative transcriptome analysis of Glyphodes pyloalis Walker (Lepidoptera: Pyralidae) reveals novel insights into heat stress tolerance in insects , 2017, BMC Genomics.

[24]  Kohtaro Tanaka,et al.  Diverse Cis-Regulatory Mechanisms Contribute to Expression Evolution of Tandem Gene Duplicates , 2017, Molecular biology and evolution.

[25]  Rongqiao Li,et al.  Molecular evolutionary mechanisms driving functional diversification of α-glucosidase in Lepidoptera , 2017, Scientific Reports.

[26]  Harmit S. Malik,et al.  Recurrent Gene Duplication Leads to Diverse Repertoires of Centromeric Histones in Drosophila Species , 2016, bioRxiv.

[27]  B. Beerntsen,et al.  Analysis of gene expression in the midgut of Bombyx mori during the larval molting stage , 2016, BMC Genomics.

[28]  Roland Eils,et al.  Complex heatmaps reveal patterns and correlations in multidimensional genomic data , 2016, Bioinform..

[29]  Q. Xia,et al.  Genome-wide identification and analysis of JHBP-domain family members in the silkworm Bombyx mori , 2016, Molecular Genetics and Genomics.

[30]  D. Heckel,et al.  Horizontal Gene Transfer Contributes to the Evolution of Arthropod Herbivory , 2016, Genome biology and evolution.

[31]  C. Cañestro,et al.  Evolution by gene loss , 2016, Nature Reviews Genetics.

[32]  E. Danchin,et al.  Horizontal Gene Transfer from Bacteria Has Enabled the Plant-Parasitic Nematode Globodera pallida to Feed on Host-Derived Sucrose. , 2016, Molecular biology and evolution.

[33]  Matthias Pechmann,et al.  Neofunctionalization of a Duplicate dachshund Gene Underlies the Evolution of a Novel Leg Segment in Arachnids. , 2016, Molecular biology and evolution.

[34]  Jinling Huang,et al.  Horizontal gene transfer: building the web of life , 2015, Nature Reviews Genetics.

[35]  T. Shimada,et al.  A novel sucrose hydrolase from the bombycoid silkworms Bombyx mori, Trilocha varians, and Samia cynthia ricini with a substrate specificity for sucrose. , 2015, Insect Biochemistry and Molecular Biology.

[36]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[37]  J. Gadau,et al.  Evolution of the Insect Desaturase Gene Family with an Emphasis on Social Hymenoptera , 2014, Molecular biology and evolution.

[38]  L. T. Kishi,et al.  A novel β-fructofuranosidase in Coleoptera: Characterization of a β-fructofuranosidase from the sugarcane weevil, Sphenophorus levis. , 2014, Insect biochemistry and molecular biology.

[39]  O. Mittapalli,et al.  Characterization of horizontally transferred β‐fructofuranosidase (ScrB) genes in Agrilus planipennis , 2014, Insect molecular biology.

[40]  Sumio Sugano,et al.  A single female-specific piRNA is the primary determiner of sex in the silkworm , 2014, Nature.

[41]  Yongping Huang,et al.  The CRISPR/Cas System mediates efficient genome engineering in Bombyx mori , 2013, Cell Research.

[42]  Raquel Assis,et al.  Neofunctionalization of young duplicate genes in Drosophila , 2013, Proceedings of the National Academy of Sciences.

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

[44]  H. Najafabadi,et al.  Insights into the insect salivary gland proteome: diet-associated changes in caterpillar labial salivary proteins. , 2013, Journal of insect physiology.

[45]  R. Murphy,et al.  Multiple ancient horizontal gene transfers and duplications in lepidopteran species , 2013, Insect molecular biology.

[46]  Steven J. M. Jones,et al.  Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest , 2013, Genome Biology.

[47]  B. Hamaker,et al.  Modulation of Starch Digestion for Slow Glucose Release through “Toggling” of Activities of Mucosal α-Glucosidases* , 2012, The Journal of Biological Chemistry.

[48]  Guangchuang Yu,et al.  clusterProfiler: an R package for comparing biological themes among gene clusters. , 2012, Omics : a journal of integrative biology.

[49]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[50]  J. Doyle,et al.  Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee , 2012, Proceedings of the National Academy of Sciences.

[51]  Z. Xiang,et al.  Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects , 2011, BMC Evolutionary Biology.

[52]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[53]  I. Braakman,et al.  Protein folding and modification in the mammalian endoplasmic reticulum. , 2011, Annual review of biochemistry.

[54]  G. Xie,et al.  Horizontal gene transfer in silkworm, Bombyx mori , 2011, BMC Genomics.

[55]  Bernard Henrissat,et al.  Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes , 2010, Proceedings of the National Academy of Sciences.

[56]  G. Felton,et al.  Survey of a Salivary Effector in Caterpillars: Glucose Oxidase Variation and Correlation with Host Range , 2010, Journal of Chemical Ecology.

[57]  Domènec Farré,et al.  Heterogeneous patterns of gene-expression diversification in mammalian gene duplicates. , 2010, Molecular biology and evolution.

[58]  F. Kondrashov,et al.  The evolution of gene duplications: classifying and distinguishing between models , 2010, Nature Reviews Genetics.

[59]  Peter M. Rice,et al.  The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants , 2009, Nucleic acids research.

[60]  P. Keeling.  Functional and ecological impacts of horizontal gene transfer in eukaryotes. , 2009, Current opinion in genetics & development.

[61]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[62]  Shu Fang,et al.  Molecular Evolution and Functional Diversification of Fatty Acid Desaturases after Recurrent Gene Duplication in Drosophila , 2009, Molecular biology and evolution.

[63]  J. Palmer,et al.  Horizontal gene transfer in eukaryotic evolution , 2008, Nature Reviews Genetics.

[64]  M. Long,et al.  Recurrent tandem gene duplication gave rise to functionally divergent genes in Drosophila. , 2008, Molecular biology and evolution.

[65]  T. Shimada,et al.  Beta-fructofuranosidase genes of the silkworm, Bombyx mori: insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. , 2008, The Journal of biological chemistry.

[66]  T. Shimada,et al.  β-Fructofuranosidase Genes of the Silkworm, Bombyx mori , 2008, Journal of Biological Chemistry.

[67]  Henrik Kaessmann,et al.  Functional diversification of duplicate genes through subcellular adaptation of encoded proteins , 2008, Genome Biology.

[68]  K. Konno,et al.  Differential effects of sugar-mimic alkaloids in mulberry latex on sugar metabolism and disaccharidases of Eri and domesticated silkworms: enzymatic adaptation of Bombyx mori to mulberry defense. , 2007, Insect biochemistry and molecular biology.

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

[70]  K. Tateishi,et al.  Mulberry latex rich in antidiabetic sugar-mimic alkaloids forces dieting on caterpillars , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. Townsend,et al.  Horizontal gene transfer, genome innovation and evolution , 2005, Nature Reviews Microbiology.

[72]  Dawei Li,et al.  A Draft Sequence for the Genome of the Domesticated Silkworm ( Bombyx mori ) , 2004 .

[73]  Jianzhi Zhang.  Evolution by gene duplication: an update , 2003 .

[74]  E. Kellogg.  What happens to genes in duplicated genomes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[75]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[76]  M. Nei,et al.  Positive Darwinian selection after gene duplication in primate ribonuclease genes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.