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The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)

Bloodfeeding is employed by many parasitic animals and requires specific innovations for efficient feeding. Some of these innovations are molecular features that are related to the inhibition of hemostasis. For example, bloodfeeding insects, bats, and leeches release proteins with anticoagulatory ac...

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Autores principales: Iwama, Rafael Eiji, Tessler, Michael, Siddall, Mark E, Kvist, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7851590/
https://www.ncbi.nlm.nih.gov/pubmed/33527140
http://dx.doi.org/10.1093/gbe/evaa242
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author Iwama, Rafael Eiji
Tessler, Michael
Siddall, Mark E
Kvist, Sebastian
author_facet Iwama, Rafael Eiji
Tessler, Michael
Siddall, Mark E
Kvist, Sebastian
author_sort Iwama, Rafael Eiji
collection PubMed
description Bloodfeeding is employed by many parasitic animals and requires specific innovations for efficient feeding. Some of these innovations are molecular features that are related to the inhibition of hemostasis. For example, bloodfeeding insects, bats, and leeches release proteins with anticoagulatory activity through their salivary secretions. The antistasin-like protein family, composed of serine protease inhibitors with one or more antistasin-like domains, is tightly linked to inhibition of hemostasis in leeches. However, this protein family has been recorded also in non-bloodfeeding invertebrates, such as cnidarians, mollusks, polychaetes, and oligochaetes. The present study aims to 1) root the antistasin-like gene tree and delimit the major orthologous groups, 2) identify potential independent origins of salivary proteins secreted by leeches, and 3) identify major changes in domain and/or motif structure within each orthologous group. Five clades containing leech antistasin-like proteins are distinguishable through rigorous phylogenetic analyses based on nine new transcriptomes and a diverse set of comparative data: the trypsin + leukocyte elastase inhibitors clade, the antistasin clade, the therostasin clade, and two additional, unnamed clades. The antistasin-like gene tree supports multiple origins of leech antistasin-like proteins due to the presence of both leech and non-leech sequences in one of the unnamed clades, but a single origin of factor Xa and trypsin + leukocyte elastase inhibitors. This is further supported by three sequence motifs that are exclusive to antistasins, the trypsin + leukocyte elastase inhibitor clade, and the therostasin clade, respectively. We discuss the implications of our findings for the evolution of this diverse family of leech anticoagulants.
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spelling pubmed-78515902021-02-04 The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata) Iwama, Rafael Eiji Tessler, Michael Siddall, Mark E Kvist, Sebastian Genome Biol Evol Research Article Bloodfeeding is employed by many parasitic animals and requires specific innovations for efficient feeding. Some of these innovations are molecular features that are related to the inhibition of hemostasis. For example, bloodfeeding insects, bats, and leeches release proteins with anticoagulatory activity through their salivary secretions. The antistasin-like protein family, composed of serine protease inhibitors with one or more antistasin-like domains, is tightly linked to inhibition of hemostasis in leeches. However, this protein family has been recorded also in non-bloodfeeding invertebrates, such as cnidarians, mollusks, polychaetes, and oligochaetes. The present study aims to 1) root the antistasin-like gene tree and delimit the major orthologous groups, 2) identify potential independent origins of salivary proteins secreted by leeches, and 3) identify major changes in domain and/or motif structure within each orthologous group. Five clades containing leech antistasin-like proteins are distinguishable through rigorous phylogenetic analyses based on nine new transcriptomes and a diverse set of comparative data: the trypsin + leukocyte elastase inhibitors clade, the antistasin clade, the therostasin clade, and two additional, unnamed clades. The antistasin-like gene tree supports multiple origins of leech antistasin-like proteins due to the presence of both leech and non-leech sequences in one of the unnamed clades, but a single origin of factor Xa and trypsin + leukocyte elastase inhibitors. This is further supported by three sequence motifs that are exclusive to antistasins, the trypsin + leukocyte elastase inhibitor clade, and the therostasin clade, respectively. We discuss the implications of our findings for the evolution of this diverse family of leech anticoagulants. Oxford University Press 2020-11-18 /pmc/articles/PMC7851590/ /pubmed/33527140 http://dx.doi.org/10.1093/gbe/evaa242 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Iwama, Rafael Eiji
Tessler, Michael
Siddall, Mark E
Kvist, Sebastian
The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title_full The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title_fullStr The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title_full_unstemmed The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title_short The Origin and Evolution of Antistasin-like Proteins in Leeches (Hirudinida, Clitellata)
title_sort origin and evolution of antistasin-like proteins in leeches (hirudinida, clitellata)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7851590/
https://www.ncbi.nlm.nih.gov/pubmed/33527140
http://dx.doi.org/10.1093/gbe/evaa242
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