Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes
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{"title"=>"Lateral transfer of a lectin-like antifreeze protein gene in fishes", "type"=>"journal", "authors"=>[{"first_name"=>"Laurie A.", "last_name"=>"Graham", "scopus_author_id"=>"7202091286"}, {"first_name"=>"Stephen C.", "last_name"=>"Lougheed", "scopus_author_id"=>"6603821827"}, {"first_name"=>"K. Vanya", "last_name"=>"Ewart", "scopus_author_id"=>"6603944628"}, {"first_name"=>"Peter L.", "last_name"=>"Davies", "scopus_author_id"=>"8523161900"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-49949083546", "pui"=>"352197200", "doi"=>"10.1371/journal.pone.0002616", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"49949083546", "pmid"=>"18612417"}, "id"=>"07ea600d-e94a-3daf-aef3-01b8eed49b5a", "abstract"=>"Fishes living in icy seawater are usually protected from freezing by endogenous antifreeze proteins (AFPs) that bind to ice crystals and stop them from growing. The scattered distribution of five highly diverse AFP types across phylogenetically disparate fish species is puzzling. The appearance of radically different AFPs in closely related species has been attributed to the rapid, independent evolution of these proteins in response to natural selection caused by sea level glaciations within the last 20 million years. In at least one instance the same type of simple repetitive AFP has independently originated in two distant species by convergent evolution. But, the isolated occurrence of three very similar type II AFPs in three distantly related species (herring, smelt and sea raven) cannot be explained by this mechanism. These globular, lectin-like AFPs have a unique disulfide-bonding pattern, and share up to 85% identity in their amino acid sequences, with regions of even higher identity in their genes. A thorough search of current databases failed to find a homolog in any other species with greater than 40% amino acid sequence identity. Consistent with this result, genomic Southern blots showed the lectin-like AFP gene was absent from all other fish species tested. The remarkable conservation of both intron and exon sequences, the lack of correlation between evolutionary distance and mutation rate, and the pattern of silent vs non-silent codon changes make it unlikely that the gene for this AFP pre-existed but was lost from most branches of the teleost radiation. We propose instead that lateral gene transfer has resulted in the occurrence of the type II AFPs in herring, smelt and sea raven and allowed these species to survive in an otherwise lethal niche.", "link"=>"http://www.mendeley.com/research/lateral-transfer-lectinlike-antifreeze-protein-gene-fishes", "reader_count"=>73, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>9, "Researcher"=>13, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>19, "Student > Master"=>10, "Other"=>3, "Student > Bachelor"=>9, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>9, "Researcher"=>13, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>19, "Student > Master"=>10, "Other"=>3, "Student > Bachelor"=>9, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>53, "Physics and Astronomy"=>2, "Chemistry"=>4, "Computer Science"=>1, "Immunology and Microbiology"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>53}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Sweden"=>2, "United States"=>4, "Denmark"=>1, "United Kingdom"=>1, "Germany"=>2, "Spain"=>2, "India"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/927050"], "description"=>"<p>(A,B) Atlantic herring type II AFP gene (Herring, GenBank #DQ003023) compared to (A), the rainbow smelt type II AFP gene (Smelt, GenBank #DQ004949), and (B), the sea raven type II AFP gene. The genes are draw to scale with exons (boxes) numbered 1–6 and colour-coded, where yellow represents untranslated regions, red the signal polypeptide, green other coding regions, and blue the extra exon in the rainbow smelt AFP gene. Introns are designated i to v. Data points represent a 17/20 nucleotide match. (C,D) Atlantic herring type II AFP gene compared to (C), zebrafish lectin gene at a 13/20 nucleotide match, and to (D), the sea raven type II AFP gene at a 15/20 nucleotide match. (E,F) Dot matrix comparison of a segment (exons 10–14) of the rainbow smelt Prp8p gene compared to (E), the Atlantic herring Prp8p gene at a 14/20 nucleotide match and to (F), the pufferfish (<i>Fugu</i>) Prp8p gene at a 14/20 nucleotide match.</p>", "links"=>[], "tags"=>["matrix", "comparisons", "lectin-like", "afp"], "article_id"=>597499, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dot_matrix_comparisons_of_lectin_like_AFP_and_control_genes_/597499", "title"=>"Dot matrix comparisons of lectin-like AFP and control genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-09 02:04:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/457335", "https://ndownloader.figshare.com/files/457483", "https://ndownloader.figshare.com/files/457650", "https://ndownloader.figshare.com/files/457718"], "description"=>"<div><p>Fishes living in icy seawater are usually protected from freezing by endogenous antifreeze proteins (AFPs) that bind to ice crystals and stop them from growing. The scattered distribution of five highly diverse AFP types across phylogenetically disparate fish species is puzzling. The appearance of radically different AFPs in closely related species has been attributed to the rapid, independent evolution of these proteins in response to natural selection caused by sea level glaciations within the last 20 million years. In at least one instance the same type of simple repetitive AFP has independently originated in two distant species by convergent evolution. But, the isolated occurrence of three very similar type II AFPs in three distantly related species (herring, smelt and sea raven) cannot be explained by this mechanism. These globular, lectin-like AFPs have a unique disulfide-bonding pattern, and share up to 85% identity in their amino acid sequences, with regions of even higher identity in their genes. A thorough search of current databases failed to find a homolog in any other species with greater than 40% amino acid sequence identity. Consistent with this result, genomic Southern blots showed the lectin-like AFP gene was absent from all other fish species tested. The remarkable conservation of both intron and exon sequences, the lack of correlation between evolutionary distance and mutation rate, and the pattern of silent vs non-silent codon changes make it unlikely that the gene for this AFP pre-existed but was lost from most branches of the teleost radiation. We propose instead that lateral gene transfer has resulted in the occurrence of the type II AFPs in herring, smelt and sea raven and allowed these species to survive in an otherwise lethal niche.</p></div>", "links"=>[], "tags"=>["lateral", "lectin-like", "antifreeze", "fishes"], "article_id"=>150092, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0002616.s001", "https://dx.doi.org/10.1371/journal.pone.0002616.s002", "https://dx.doi.org/10.1371/journal.pone.0002616.s003", "https://dx.doi.org/10.1371/journal.pone.0002616.s004"], "stats"=>{"downloads"=>5, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Lateral_Transfer_of_a_Lectin_Like_Antifreeze_Protein_Gene_in_Fishes/150092", "title"=>"Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-07-09 00:01:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/927389"], "description"=>"<p>The columns labeled with % are the identities. The first (no gaps) is calculated by pair wise exclusion of gaps and the second (gaps) is calculated over the length of the alignment, gaps included. The column labeled with bp shows the total length of each alignment (first no gaps/second with gaps). The second intron is not included as large portions of the sequence are probably not homologous.</p>", "links"=>[], "tags"=>["identities", "intron", "exon", "herring", "rainbow", "smelt", "raven", "afp"], "article_id"=>597830, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.t001", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Percent_identities_between_each_intron_and_exon_in_the_herring_H_rainbow_smelt_S_and_sea_raven_SR_AFP_gene_sequences_/597830", "title"=>"Percent identities between each intron and exon in the herring (H), rainbow smelt (S) and sea raven (SR) AFP gene sequences.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-07-09 02:10:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/927220"], "description"=>"<p>(A) Blot probed with rainbow smelt AFP genomic DNA from exon 3 to 6. (B) same blot probed with chicken beta-tubulin cDNA. Lane 1 contains markers. Lanes 2, 4, 7, 11 and 13 are blank. Other lanes contain Pvu II-digested genomic DNAs (10 µg) from the following species: 3, bowfin; 5, Atlantic herring; 6, Pacific herring; 8, zebrafish; 9, rainbow trout; 10, cisco; 12, rainbow smelt; 14, Atlantic cod; 15, sea raven; 16, yellow perch; 17, winter flounder; and 18, zebrafish. Lane 18 also contains plasmid DNAs for the herring and rainbow smelt AFP genes at a single gene copy loading.</p>", "links"=>[], "tags"=>["blot", "genomic"], "article_id"=>597667, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Southern_blot_of_fish_genomic_DNAs_/597667", "title"=>"Southern blot of fish genomic DNAs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-09 02:07:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/926745"], "description"=>"<p>C-type lectin homolog alignment showing the cysteine pair that makes up the 5<sup>th</sup> disulfide bond is common to the type II AFPs but is missing in other lectins from the database. Sequences aligned are type II AFPs from the sea raven, <i>Hemitripterus americanus</i>, (SeaRaven, GenBank #AAA49617); the Atlantic herring, <i>Clupea harengus</i>, (Herring, GenBank # AAY60837); the rainbow smelt, <i>Osmerus mordax</i>, (Smelt, GenBank #AAA49442); the Japanese smelt, <i>Hypomesus nipponensis</i>, (JpSmelt (Yamashita et al. 2003)); single lectin domain proteins from the common carp, <i>Cyprinus carpio</i>, (Carp, GenBank #BAA95671); the zebrafish, <i>Danio rerio</i>, (Zebraf, GenBank # XM_001337634); and the Atlantic salmon, <i>Salmo salar</i>, (Salmon, GenBank #AAO43604); as well as the human pancreatic stone protein (PSP, GenBank #NP_002900) and the C-type lectin domain from the rat mannose-binding protein (RatMBP, GenBank #AAA98781). Secondary structure elements from the rat mannose-binding protein (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002616#pone-0002616-g001\" target=\"_blank\">Figure 1</a>) are displayed above the alignment. Colour is used to indicate conservation of the residues between the 9 sequences with matches of 8–9 in black, 6–7 in green, and 3–5 in ochre or yellow. Cysteines are coloured red and their pairings are indicated by numbers under the alignment. Sequences are numbered from the start of the signal polypeptide (in italics) except for the rat mannose-binding protein where numbering starts at the beginning of the domain. Residues in the herring and rat mannose-binding protein that are involved in Ca<sup>2+</sup> coordination are indicated by blue stars below the sequence alignment.</p>", "links"=>[], "tags"=>["lectin"], "article_id"=>597195, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.g002", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antifreeze_protein_lectin_alignments_/597195", "title"=>"Antifreeze protein - lectin alignments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-09 01:59:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/926892"], "description"=>"<p>(<i>A</i>) Bayesian 50% majority rule consensus tree (from 7500 sampled trees) based on the protein sequences aligned in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002616#pone-0002616-g002\" target=\"_blank\">Figure 2</a>. The alignment was truncated to the beginning of the first helix (α0) to the end of the sea raven sequence. Branch lengths represent the expected fraction of changes, and Bayesian posterior probabilities above 50% and selected percent identities (italics) are indicated near the nodes. The highest identity between the AFPs and any other C-type lectin domain is 38%. Herring AFP is 84% and 85% identical to Japanese and rainbow smelt AFPs, respectively. The two smelt sequences share 79% identity. (<i>b</i>) Phylogenetic tree of teleosts based on ribosomal 16S RNA sequence comparison. Species are referred to by their common names. Those that are known to produce AFPs have the type of AFP they produce indicated alongside (AFGP, antifreeze glycoprotein; I, alanine-rich alpha-helical; II, lectin-like; III, beta-clip fold; IV, helix bundle). Those that produce type II AFP are highlighted. The rainbow smelt and herring sequences were double-checked by amplification from the DNAs used in this study and were almost identical to the sequences reported in the database. The non-teleost fish, the bowfin, was used to root the tree and only posterior probabilities >50% are shown. Putative type II gene loses (presuming the presence of the gene in the common ancestor) are indicated by grey stars. A further gene loss on the <i>Takifugu</i>/masked triggerfish lineage is not postulated since these fish group with yellow perch and Antarctic toothfish according to the phylogeny of Miya et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002616#pone.0002616-Miya1\" target=\"_blank\">[22]</a>.</p>", "links"=>[], "tags"=>["trees", "afps", "lectins", "teleost"], "article_id"=>597337, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.g003", "stats"=>{"downloads"=>3, "page_views"=>50, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_trees_of_AFPs_and_related_lectins_as_well_as_selected_teleost_fishes_/597337", "title"=>"Phylogenetic trees of AFPs and related lectins as well as selected teleost fishes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-09 02:02:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/926626"], "description"=>"<p>(A) Rat mannose-binding protein structure (PDB code: 1KWT) and (B) Herring AFP structure (PDB code: 2PY2) showing the location of the 5<sup>th</sup> disulfide bridge that is peculiar to the type II AFPs. Secondary structure elements (red – helix; green – beta-strand; grey – loop) are numbered from the N terminus. Disulfide bonds are shown in yellow with the linkages of numbered cysteines indicated in brackets. LLR is the long loop region.</p>", "links"=>[], "tags"=>["lectin"], "article_id"=>597074, "categories"=>["Biochemistry", "Molecular Biology", "Evolutionary Biology", "Genetics"], "users"=>["Laurie A. Graham", "Stephen C. Lougheed", "K. Vanya Ewart", "Peter L. Davies"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0002616.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antifreeze_protein_lectin_structural_comparisons_/597074", "title"=>"Antifreeze protein - lectin structural comparisons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-07-09 01:57:54"}

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Relative Metric

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