دورية أكاديمية

Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals.

التفاصيل البيبلوغرافية
العنوان: Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals.
المؤلفون: Casewell NR; Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Pembroke Place, L3 5QA Liverpool, United Kingdom; nicholas.casewell@lstmed.ac.uk., Petras D; Institut für Chemie, Technische Universität Berlin, 10623 Berlin, Germany.; Collaborative Mass Spectrometry Innovation Center, University of California, San Diego, La Jolla, CA 92093., Card DC; Department of Biology, University of Texas at Arlington, Arlington, TX 76010.; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138.; Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138., Suranse V; Evolutionary Venomics Lab, Centre for Ecological Sciences, Indian Institute of Science, 560012 Bangalore, India., Mychajliw AM; Department of Biology, Stanford University, Stanford, CA 94305.; Department of Rancho La Brea, Natural History Museum of Los Angeles County, Los Angeles, CA 90036.; Institute of Low Temperature Science, Hokkaido University, 060-0819 Sapporo, Japan., Richards D; School of Life Sciences, University of Nottingham, University Park, NG7 2RD Nottingham, United Kingdom.; Biomedical Research Centre, University of East Anglia, Norwich Research Park, NR4 7TJ Norwich, United Kingdom., Koludarov I; Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Onna, Kunigami-gun, Okinawa, 904-0495, Japan., Albulescu LO; Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Pembroke Place, L3 5QA Liverpool, United Kingdom., Slagboom J; Division of BioAnalytical Chemistry, Amsterdam Institute of Molecules, Medicines and Systems, Vrije Universiteit Amsterdam, 1081 LA Amsterdam, The Netherlands., Hempel BF; Institut für Chemie, Technische Universität Berlin, 10623 Berlin, Germany., Ngum NM; School of Life Sciences, University of Nottingham, University Park, NG7 2RD Nottingham, United Kingdom., Kennerley RJ; Durrell Wildlife Conservation Trust, Les Augrès Manor, Trinity, Jersey JE3 5BP, British Channel Islands, United Kingdom., Brocca JL; SOH Conservación, Apto. 401 Residencial Las Galerías, Santo Domingo, 10130, Dominican Republic., Whiteley G; Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Pembroke Place, L3 5QA Liverpool, United Kingdom., Harrison RA; Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Pembroke Place, L3 5QA Liverpool, United Kingdom., Bolton FMS; Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Pembroke Place, L3 5QA Liverpool, United Kingdom., Debono J; Venom Evolution Lab, School of Biological Sciences, University of Queensland, St. Lucia, QLD 4067, Australia., Vonk FJ; Naturalis Biodiversity Center, 2333 CR Leiden, The Netherlands., Alföldi J; Vertebrate Genomics, Broad Institute of MIT and Harvard, Cambridge, MA 02142., Johnson J; Vertebrate Genomics, Broad Institute of MIT and Harvard, Cambridge, MA 02142., Karlsson EK; Vertebrate Genomics, Broad Institute of MIT and Harvard, Cambridge, MA 02142.; Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA 01655., Lindblad-Toh K; Vertebrate Genomics, Broad Institute of MIT and Harvard, Cambridge, MA 02142.; Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 751 23 Uppsala, Sweden., Mellor IR; School of Life Sciences, University of Nottingham, University Park, NG7 2RD Nottingham, United Kingdom., Süssmuth RD; Institut für Chemie, Technische Universität Berlin, 10623 Berlin, Germany., Fry BG; Venom Evolution Lab, School of Biological Sciences, University of Queensland, St. Lucia, QLD 4067, Australia., Kuruppu S; Monash Venom Group, Department of Pharmacology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia.; Department of Biochemistry & Molecular Biology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia., Hodgson WC; Monash Venom Group, Department of Pharmacology, Biomedicine Discovery Institute, Monash University, VIC 3800, Australia., Kool J; Division of BioAnalytical Chemistry, Amsterdam Institute of Molecules, Medicines and Systems, Vrije Universiteit Amsterdam, 1081 LA Amsterdam, The Netherlands., Castoe TA; Department of Biology, University of Texas at Arlington, Arlington, TX 76010., Barnes I; Department of Earth Sciences, Natural History Museum, SW7 5BD London, United Kingdom., Sunagar K; Evolutionary Venomics Lab, Centre for Ecological Sciences, Indian Institute of Science, 560012 Bangalore, India., Undheim EAB; Centre for Advanced Imaging, The University of Queensland, Brisbane QLD 4072, Australia.; Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia.; Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo 0316, Norway., Turvey ST; Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY London, United Kingdom.
المصدر: Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2019 Dec 17; Vol. 116 (51), pp. 25745-25755. Date of Electronic Publication: 2019 Nov 26.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Washington, DC : National Academy of Sciences
مواضيع طبية MeSH: Eutheria*/classification , Eutheria*/genetics , Eutheria*/physiology , Evolution, Molecular* , Shrews*/classification , Shrews*/genetics , Shrews*/physiology, Genome/*genetics , Venoms/*genetics, Animals ; Gene Duplication ; Male ; Phylogeny ; Proteomics ; Tissue Kallikreins/genetics
مستخلص: Venom systems are key adaptations that have evolved throughout the tree of life and typically facilitate predation or defense. Despite venoms being model systems for studying a variety of evolutionary and physiological processes, many taxonomic groups remain understudied, including venomous mammals. Within the order Eulipotyphla, multiple shrew species and solenodons have oral venom systems. Despite morphological variation of their delivery systems, it remains unclear whether venom represents the ancestral state in this group or is the result of multiple independent origins. We investigated the origin and evolution of venom in eulipotyphlans by characterizing the venom system of the endangered Hispaniolan solenodon ( Solenodon paradoxus ). We constructed a genome to underpin proteomic identifications of solenodon venom toxins, before undertaking evolutionary analyses of those constituents, and functional assessments of the secreted venom. Our findings show that solenodon venom consists of multiple paralogous kallikrein 1 ( KLK1 ) serine proteases, which cause hypotensive effects in vivo, and seem likely to have evolved to facilitate vertebrate prey capture. Comparative analyses provide convincing evidence that the oral venom systems of solenodons and shrews have evolved convergently, with the 4 independent origins of venom in eulipotyphlans outnumbering all other venom origins in mammals. We find that KLK1 s have been independently coopted into the venom of shrews and solenodons following their divergence during the late Cretaceous, suggesting that evolutionary constraints may be acting on these genes. Consequently, our findings represent a striking example of convergent molecular evolution and demonstrate that distinct structural backgrounds can yield equivalent functions.
Competing Interests: The authors declare no competing interest.
(Copyright © 2019 the Author(s). Published by PNAS.)
References: Br J Pain. 2013 Nov;7(4):179-88. (PMID: 26516522)
Bioinformatics. 2008 Mar 1;24(5):637-44. (PMID: 18218656)
Syst Biol. 2003 Apr;52(2):131-58. (PMID: 12746144)
J Proteome Res. 2015 Jun 5;14(6):2539-56. (PMID: 25896403)
Bioinformatics. 2019 Feb 1;35(3):526-528. (PMID: 30016406)
Curr Biol. 2016 Sep 26;26(18):2434-2445. (PMID: 27641771)
Mol Biol Evol. 2007 Aug;24(8):1586-91. (PMID: 17483113)
Bioinformatics. 2015 Oct 1;31(19):3210-2. (PMID: 26059717)
Mol Cell Proteomics. 2008 Feb;7(2):215-46. (PMID: 17855442)
PLoS Genet. 2012;8(7):e1002764. (PMID: 22807683)
Endocr Rev. 2010 Aug;31(4):407-46. (PMID: 20103546)
Zootaxa. 2015 Sep 23;4020(3):533-53. (PMID: 26624114)
Anal Bioanal Chem. 2018 Sep;410(23):5751-5763. (PMID: 30090989)
Nat Rev Dis Primers. 2017 Sep 14;3:17063. (PMID: 28905944)
Biol Chem. 2005 Feb;386(2):177-82. (PMID: 15843162)
Pharmacol Ther. 1992;53(2):199-215. (PMID: 1641406)
PeerJ. 2019 Feb 6;7:e6154. (PMID: 30755823)
Annu Rev Genomics Hum Genet. 2009;10:483-511. (PMID: 19640225)
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7542-7. (PMID: 15136743)
Nat Protoc. 2015 Jun;10(6):845-58. (PMID: 25950237)
PLoS One. 2013 Jul 10;8(7):e68074. (PMID: 23874499)
Gigascience. 2018 Jun 1;7(6):. (PMID: 29718205)
Trends Biochem Sci. 2019 Apr;44(4):365-379. (PMID: 30651181)
Curr Biol. 2009 Dec 1;19(22):1925-31. (PMID: 19879144)
J Proteomics. 2013 Aug 26;89:95-111. (PMID: 23748026)
Mol Biol Evol. 2015 May;32(5):1342-53. (PMID: 25697341)
PLoS Genet. 2015 Oct 22;11(10):e1005596. (PMID: 26492532)
Trends Ecol Evol. 2013 Apr;28(4):219-29. (PMID: 23219381)
Mol Cell Proteomics. 2013 Mar;12(3):651-63. (PMID: 23242553)
J Biol Chem. 1989 Oct 25;264(30):17947-52. (PMID: 2509450)
Mol Phylogenet Evol. 2007 Jul;44(1):126-37. (PMID: 17267241)
Toxins (Basel). 2018 Feb 28;10(3):. (PMID: 29495554)
Mol Biol Evol. 2013 May;30(5):1196-205. (PMID: 23420840)
Toxins (Basel). 2015 Jul 17;7(7):2639-58. (PMID: 26193318)
J Biol Chem. 1995 Apr 28;270(17):10246-55. (PMID: 7730329)
Mol Biol Evol. 2016 Dec;33(12):3095-3103. (PMID: 27624716)
Curr Protoc Bioinformatics. 2014 Dec 12;48:4.11.1-4.11.39. (PMID: 25501943)
Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6820-3. (PMID: 10359796)
Arch Biochem Biophys. 2000 Jun 1;378(1):131-41. (PMID: 10871053)
Trends Ecol Evol. 2016 May;31(5):366-371. (PMID: 26936225)
Toxicon. 1999 Nov;37(11):1635-8. (PMID: 10482397)
Curr Biol. 2017 Apr 24;27(8):1184-1191. (PMID: 28366739)
Toxicon. 2017 Sep 1;135:71-83. (PMID: 28625888)
PLoS One. 2013;8(3):e58866. (PMID: 23554944)
Mol Phylogenet Evol. 2018 Apr;121:158-165. (PMID: 29331683)
Toxicon. 2015 Dec 1;107(Pt B):163-74. (PMID: 26385313)
Genome Res. 2007 Apr;17(4):413-21. (PMID: 17322288)
معلومات مُعتمدة: United Kingdom WT_ Wellcome Trust; R01 HG008742 United States HG NHGRI NIH HHS; 200517/Z/16/Z United Kingdom WT_ Wellcome Trust
فهرسة مساهمة: Keywords: convergent molecular evolution; gene duplication; genotype phenotype; kallikrein toxin; venom systems
سلسلة جزيئية: figshare 10.6084/m9.figshare.7640456
المشرفين على المادة: 0 (Venoms)
EC 3.4.21.35 (Tissue Kallikreins)
تواريخ الأحداث: Date Created: 20191128 Date Completed: 20200413 Latest Revision: 20231027
رمز التحديث: 20240513
مُعرف محوري في PubMed: PMC6926037
DOI: 10.1073/pnas.1906117116
PMID: 31772017
قاعدة البيانات: MEDLINE
الوصف
تدمد:1091-6490
DOI:10.1073/pnas.1906117116