Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-05T09:02:56.872Z Has data issue: false hasContentIssue false

The salivary transcriptome of Limnobdella mexicana (Annelida: Clitellata: Praobdellidae) and orthology determination of major leech anticoagulants

Published online by Cambridge University Press:  27 June 2019

Rafael Iwama*
Affiliation:
Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, ON M5S 2C6, Canada Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 2B4, Canada
Alejandro Oceguera-Figueroa
Affiliation:
Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito Zona Deportiva 53, Ciudad Universitaria, 04510 Coyoacan Ciudad de México, México
Gonzalo Giribet
Affiliation:
Museum of Comparative Zoology & Department of Organismic and Evolutionary Biology, Harvard University, Cambridge MA, 02138, USA
Sebastian Kvist
Affiliation:
Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, ON M5S 2C6, Canada Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 2B4, Canada
*
Author for correspondence: Rafael Iwama, E-mail: [email protected]

Abstract

Bloodfeeding requires several adaptations that allow the parasite to feed efficiently. Leeches and other hematophagous animals have developed different mechanisms to inhibit hemostasis, one of the main barriers imposed by their hosts. Limnobdella mexicana is a member of the leech family Praobdellidae, a family of host generalists known for their preference to attach on mucosal membranes of mammals, such as those in nasopharyngeal cavities, bladders and ocular orbits. Previous studies have hypothesized a positive relationship between diversity of anticoagulants and diversity of hosts in bloodfeeding leeches. However, orthology determination of putative anticoagulants and the lack of standardization of sequencing effort and method hinder comparisons between publicly available transcriptomes generated in different laboratories. In the present study, we examine the first transcriptome of a praobdellid leech and identify 15 putative anticoagulants using a phylogeny-based inference approach, amino-acid conservation, Pfam domains and BLAST searches. Our phylogenetic analyses suggest that the ancestral leech was able to inhibit factor Xa and that some hirudins that have been reported in previous studies on leech anticoagulants may not be orthologous with the archetypal hirudin.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Apakupakul, K, Siddall, ME and Burreson, EM (1999) Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution 12, 350359.Google Scholar
Ballesteros, JA and Hormiga, G (2016) A New orthology assessment method for phylogenomic data: unrooted phylogenetic orthology. Molecular Biology and Evolution 33, 21172134.Google Scholar
Barnes, CS, Krafft, B, Frech, M, Hofmann, UR, Papendieck, A, Dahlems, U, Gellissen, G and Hoylaerts, MF (2001) Production and characterization of saratin, an inhibitor of von willebrand factor-dependent platelet adhesion to collagen. Seminars in Thrombosis and Hemostasis 27, 337347.Google Scholar
Blankenship, DT, Brankamp, RG, Manley, GD and Cardin, AD (1990) Amino acid sequence of ghilanten: anticoagulant-antimetastic principle of the south American leech, Haementeria ghilianii. Biochemical and Biophysical Research Communucation 166, 13841389.Google Scholar
Borda, E and Siddall, ME (2004) Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): Phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution 30, 213225.Google Scholar
Brocker, CN, Vasiliou, V and Nebert, DW (2009) Evolutionary divergence and functions of the ADAM and ADAMTS gene families. Human Genomics 4, 4355.Google Scholar
Cruz, CP, Eidt, J, Drouilhet, J, Brown, AT, Wang, YF, Barnes, CS and Moursi, MM (2001) Saratin, an inhibitor of von willebrand factor-dependent platelet adhesion, decreases platelet aggregation and intimal hyperplasia in a rat carotid endarterectomy model. Journal of Vascular Surgery 34, 724729.Google Scholar
Dunwiddie, C, Thornberry, NA, Bull, HG, Sardana, M, Friedman, PA, Jacobs, JW and Simpson, E (1989) Antistasin, a leech-derived inhibitor of factor Xa. Kinetic analysis of enzyme inhibition and identification of the reactive site. Journal of Biological Chemistry 264, 1669416699.Google Scholar
Eddy, SR (2011) Accelerated profile HMM searches. PLoS Computational Biology 7, 117. doi: 10.1371/journal.pcbi.1002195.Google Scholar
Elliott, JM and Kutschera, U (2011) Medicinal leeches: historical use, ecology, genetics and conservation. Freshwater Reviews 4, 2141.Google Scholar
Finn, RD, Coggill, P, Eberhardt, RY, Eddy, SR, Mistry, J, Mitchell, AL, Potter, SC, Punta, M, Qureshi, M, Sangrador-Vegas, A, Salazar, GA, Tate, J and Bateman, A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44, D279D285.Google Scholar
Fujita, T, Matsushita, M and Endo, Y (2004) The lectin-complement pathway – Its role in innate immunity and evolution. Immunological Reviews 198, 185202.Google Scholar
Furie, BBC and Furie, BBC (2005) Review series Thrombus formation in vivo. The Journal of Clincial Investigation 115, 33553362.Google Scholar
Goloboff, PA and Catalano, SA (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221238.Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.Google Scholar
Koh, Y and Kini, R (2009) Molecular diversity of anticoagulants from haematophagous animals. Thrombosis and Haemostasis 102, 437453.Google Scholar
Krowarsch, D, Cierpicki, T, Jelen, F and Otlewski, J (2003) Canonical protein inhibitors of serine proteases. Cellular and Molecular Life Sciences 60, 24272444.Google Scholar
Kvist, S, Sarkar, IN and Siddall, ME (2011) Genome-wide search for leech antiplatelet proteins in the non-blood-feeding leech Helobdella robusta (Rhyncobdellida: Glossiphoniidae) reveals evidence of secreted anticoagulants. Invertebrate Biology 130, 344350.Google Scholar
Kvist, S, Min, GS and Siddall, ME (2013) Diversity and selective pressures of anticoagulants in three medicinal leeches (Hirudinida: Hirudinidae, Macrobdellidae). Ecology and Evolution 3, 918933.Google Scholar
Kvist, S, Brugler, MR, Goh, TG, Giribet, G and Siddall, ME (2014) Pyrosequencing the salivary transcriptome of Haemadipsa interrupta (Annelida: Clitellata: Haemadipsidae): Anticoagulant diversity and insight into the evolution of anticoagulation capabilities in leeches. Invertebrate Biology 133, 7498.Google Scholar
Kvist, S, Oceguera-Figueroa, A, Tessler, M, Jiménez-Armenta, J, Freeman, RM, Giribet, G and Siddall, ME (2017) When predator becomes prey: investigating the salivary transcriptome of the shark-feeding leech Pontobdella macrothela (Hirudinea: Piscicolidae). Zoological Journal of the Linnean Society 179, 725737.Google Scholar
Min, G-S, Sarkar, IN and Siddall, ME (2010) Salivary transcriptome of the north American medicinal leech, Macrobdella decora. The Journal of Parasitology 96, 12111221.Google Scholar
Müller, C, Mescke, K, Liebig, S, Mahfoud, H, Lemke, S and Hildebrandt, JP (2016) More than just one: multiplicity of hirudins and hirudin-like factors in the medicinal leech, Hirudo medicinalis. Molecular Genetics and Genomics 291, 227240.Google Scholar
Müller, C, Haase, M, Lemke, S and Hildebrandt, JP (2017) Hirudins and hirudin-like factors in Hirudinidae: implications for function and phylogenetic relationships. Parasitology Research 116, 313325.Google Scholar
Nakano, T, Tomikawa, K, Sakono, T and Yoshikawa, N (2017) Praobdellidae (Hirudinida: Arhynchobdellida) is not specific only to the mucous-membrane after all: discovery of a praobdellid leech feeding on the Japanese freshwater crab Geothelphusa dehaani. Parasitology International 66, 210213.Google Scholar
Oka, A (1934) Note sur les moeurs dela Myxobdella sinanensis. Proceeding of the Imperial Academy (Tokyo) 10, 519520.Google Scholar
Ompraba, G, Chapeaurouge, A, Doley, R, Devi, KR, Padmanaban, P, Venkatraman, C, Velmurugan, D, Lin, Q and Kini, RM (2010) Identification of a novel family of snake venom proteins veficolins from cerberus rynchops using a venom gland transcriptomics and proteomics approach. Journal of Proteome Research 9, 18821893.Google Scholar
Petersen, TN, Brunak, S, Von Heijne, G and Nielsen, H (2011) Signalp 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785786.Google Scholar
Phillips, AJ, Arauco-Brown, R, Oceguera-Figueroa, A, Gomez, GP, Beltrán, M, Lai, YT and Siddall, ME (2010) Tyrannobdella rex n. gen. n. sp. and the evolutionary origins of mucosal leech infestations. PLoS ONE 5, 18. doi: 10.1371/journal.pone.0010057.Google Scholar
Porter, S, Clark, IM, Kevorkian, L and Edwards, D (2005) The ADAMTS metalloproteinases Sarah. Biochemical Journal 386, 1527.Google Scholar
Ribeiro, JMC and Arcà, B (2009) From Sialomes to the sialoverse. An insight into salivary potion of blood-feeding insects. Advances in Insect Physiology 37, 59118. doi: 10.1016/S0065-2806(09)37002-2.Google Scholar
Ribeiro, JMC and Francischetti, IMB (2003) Role of arthropods saliva in blood feeding: Sialome and post-sialome perspectives. Annual Review of Entomology 48, 7388.Google Scholar
Ribeiro, JMC, Arcà, B, Lombardo, F, Calvo, E, Phan, VM, Chandra, PK and Wikel, SK (2007) An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8, 127.Google Scholar
Salzet, M (2001) Anticoagulants and inhibitors of platelet aggregation derived from leeches. FEBS Letters 492, 187192.Google Scholar
Salzet, M (2002) Leech thrombin inhibitors. Current Pharmaceutical Design 8, 493503.Google Scholar
Sawyer, RT (1986) Leech Biology and Behavior. Oxford: Claredon Press.Google Scholar
Scacheri, E, Nitti, G, Valsasina, B, Orsini, G, Visco, C, Ferrera, M, Sawyer, RT and Sarmientos, P (1993) Novel hirudin variants from the leech Hirudinaria manillensis: amino acid sequence, cDNA cloning and genomic organization. European Journal of Biochemistry 214, 295304.Google Scholar
Sharp, KA (1996) Electrostatic interactions in hirudin-thrombin binding. Biophysical Chemistry 61, 3749.Google Scholar
Siddall, ME and Burreson, EM (1995). Phylogeny of the Euhirudinea: Independent evolution of blood feeding by leeches? Canadian Journal of Zoology 73, 10481064.Google Scholar
Siddall, ME, Rood-goldman, R, Barriot, A and Barboutist, C (2013) The eyes have tt: long-distance dispersal by an intraorbital leech parasite of birds. The Journal of Parasitology 99, 11371139.Google Scholar
Siddall, ME, Brugler, MR and Kvist, S (2016) Comparative transcriptomic analyses of three species of Placobdella (rhynchobdellida: glossiphoniidae) confirms a single origin of blood feeding in leeches. Journal of Parasitology 102, 143150.Google Scholar
Tang, BL (2001) ADAMTS: a novel family of extracellular matrix proteases. International Journal of Biochemistry and Cell Biology 33, 3344.Google Scholar
Tessler, M, de Carle, D, Voiklis, ML, Gresham, OA, Neumann, JS, Cios, S and Siddall, ME (2018 a) Worms that suck: Phylogenetic analysis of Hirudinea solidifies the position of Acanthobdellida and necessitates the dissolution of Rhynchobdellida. Molecular Phylogenetics and Evolution 127, 129134.Google Scholar
Tessler, M, Marancik, D, Champagne, D, Dove, A, Camus, A, Siddall, ME and Kvist, S (2018 b) Marine leech anticoagulant diversity and evolution. Journal of Parasitology 104, 210220.Google Scholar
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. and Barton, G. J. (2009). Jalview version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics (Oxford, England) 25, 11891191.Google Scholar
Wilkinson, M, McInerney, JO, Hirt, RP, Foster, PG and Embley, TM (2007) Of clades and clans: terms for phylogenetic relationships in unrooted trees. Trends in Ecology and Evolution 22, 114115.Google Scholar
Supplementary material: Image

Iwama et al. supplementary material

Iwama et al. supplementary material 1

Download Iwama et al. supplementary material(Image)
Image 6.1 MB
Supplementary material: File

Iwama et al. supplementary material

Iwama et al. supplementary material 2

Download Iwama et al. supplementary material(File)
File 13.3 KB
Supplementary material: Image

Iwama et al. supplementary material

Iwama et al. supplementary material 3

Download Iwama et al. supplementary material(Image)
Image 2.8 MB