Skip to main content
×
Home

Bacterial symbiont and salivary peptide evolution in the context of leech phylogeny

  • MARK E. SIDDALL (a1), GI-SIK MIN (a2), FRANK M. FONTANELLA (a3), ANNA J. PHILLIPS (a1) (a4) and SARA C. WATSON (a1)...
Summary
SUMMARY

The evolutionary history of leeches is employed as a general framework for understanding more than merely the systematics of this charismatic group of annelid worms, and serves as a basis for understanding blood-feeding related correlates ranging from the specifics of gut-associated bacterial symbionts to salivary anticoagulant peptides. A variety of medicinal leech families were examined for intraluminal crop bacterial symbionts. Species of Aeromonas and Bacteroidetes were characterized with DNA gyrase B and 16S rDNA. Bacteroidetes isolates were found to be much more phylogenetically diverse and suggested stronger evidence of phylogenetic correlation than the gammaproteobacteria. Patterns that look like co-speciation with limited taxon sampling do not in the full context of phylogeny. Bioactive compounds that are expressed as gene products, like those in leech salivary glands, have ‘passed the test’ of evolutionary selection. We produced and bioinformatically mined salivary gland EST libraries across medicinal leech lineages to experimentally and statistically evaluate whether evolutionary selection on peptides can identify structure-function activities of known therapeutically relevant bioactive compounds like antithrombin, hirudin and antistasin. The combined information content of a well corroborated leech phylogeny and broad taxonomic coverage of expressed proteins leads to a rich understanding of evolution and function in leech history.

Copyright
Corresponding author
*Corresponding author: Mark E Siddall. E-mail: siddall@amnh.org
References
Hide All
Apakupakul K., Siddall M. E. and Burreson E. M. (1999). Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution 12, 350359. doi:10.1006/mpev.1999.0639.
Bader D. A., Roshan U. and Stamatakis A. (2006). Computational grand challenges in assembling the tree of life: problems and solutions. Advances in Computers 68, 127176. doi:10.1016/S0065-2458(06)68004-2.
Baskova I. P. and Zavalova L. L. (2001). Proteinase inhibitors from the medicinal leech Hirudo medicinalis. Biochemistry Moscow 66, 703717. doi:10.1023/A:1010223325313.
Batchelor A. G. G., Davison P. and Sully L. (1984). The salvage of congested skin flaps by the application of leeches. British Journal of Plastic Surgery 37, 358360. doi:10.1016/0007-1226(84)90079-1.
Borda E., Oceguera-Figueroa A. and Siddall M. E. (2008). On the evolution, classification and biogeography of some haemadipsoid leeches (Hirudinida: Arhynchobdellida: Hirudiniformes). Molecular Phylogenetics and Evolution 46, 142–54. doi:10.1016/j.ympev.2007.09.006.
Borda E. and Siddall M. E. (2004). Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Molecular Phylogenetics and Evolution 30, 213225. doi:10.1016/j.ympev.2003.09.002.
Borda E. and Siddall M. E. (2011). Insights into the evolutionary history of IndoPacific bloodfeeding terrestrial leeches (Hirudinida: Arhynchobdellida: Haemadipisdae). Invertebrate Systematics. 24, 456472. doi:10.1071/IS10013.
Bourtzis K. and Miller T. A. (2006). Insect Symbiosis, Volume 2. CRC Press/Taylor and Frances, Boca Raton, FL, London.
Brooks D. R. (1990). Parsimony analysis in historical biogeography and coevolution: methodological and theoretical update. Systematic Biology 39, 1430. doi:10.2307/2992205.
Carroll L. (1871). Through the Looking Glass and What Alice Found There. Macmillan, London.
Croizat L. (1958). Panbiogeography, Volumes 1, 2a, 2b. Published by author. Caracas, Venezuela.
Derganc M. and Zdravic F. (1960). Venous congestion of flaps treated by application of leeches. British Journal of Plastic Surgery 13, 187192.
Dunlap P. V., Ast J. C., Kimura S., Fukui A., Yoshino T. and Endo H. (2007). Phylogenetic analysis of host-symbiont specificity and codivergence in bioluminescent symbioses. Cladistics 23, 507532. doi:10.1111/j.1096-0031.2007.00157.x.
Faria F., Junqueira-de-Azevedo Ide L., Ho P. L., Sampaio M. U. and Chudzinski-Tavassi A. M. (2005). Gene expression in the salivary complexes from Haementeria depressa leech through the generation of expressed sequence tags. Gene 349, 173185. doi:10.1016/j.gene.2004. 12.022.
Farris J. S., Albert V. A., Källersjö M., Lipscomb D. and Kluge A. G. (1996). Parsimony jackknifing outperforms neighbor-joining. Cladistics 12, 99124. doi:10.1111/j.1096-0031.1996.tb00196.x.
Giribet G. (2008). Assembling the lophotrochozoan (=spiralian) tree of life. Philosophical Transactions of the Royal Society B 363, 15131522. doi:10.1098/rstb.2007.2241.
Goloboff P. A., Farris J. S. and Nixon K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774786. doi:10.1111/j.1096-0031.2008.00217.x.
Graf J. (1999). Symbiosis of Aeromonas veronii Biovar sobria and Hirudo medicinalis, the medicinal leech: a novel model for digestive tract associations. Infection and Immunity 67, 17.
Graf J. (2000). Symbiosis of Aeromonas and Hirudo medicinalis, the medicinal leech. American Society for Microbiology News 66, 147153.
Graf J. (2002). The effect of symbionts on the physiology of Hirudo medicinalis, the medicinal leech. Invertebrate Reproduction and Development 41, 269275.
Greinacher A., Völpel H., Janssens U., Hach-Wunderle V., Kemkes-Matthes B., Eichler P., Mueller-Velten H. G. and Pötzsch B. (1999). Recombinant hirudin (Lepirudin) provides safe and effective anticoagulation in patients with heparin-induced thrombocytopenia. Circulation 99, 7380.
Greinacher A. and Warkentin T. E. (2008). The direct thrombin inhibitor hirudin. Thrombosis and Haemostasis 99, 819–29.
Haas G. (1924). Versuche der Blutauswaschung am Lebenden mit Hilfe der Dialyse. Wiener Klinische Wochenschrift 4, 1314. doi:10.1007/BF01745400.
Hackett S. J., Kimball R. T., Reddy S., Bowie R. C. K., Braun E. L., Braun M. J., Chojnowski J. L., Cox W. A., Han K.-L., Harshman J., Huddleston C. J., Marks B. D., Miglia K. J., Moore W. S., Sheldon F. H., Steadman D. W., Witt C. C., and Yuri T. (2008). A phylogenetic study of birds reveals their evolutionary history. Science 230, 17631768. doi:10.1126/science.1157704
Hittinger C. T., Johnston M., Tossberg J. T. and Rokas A. (2010). Leveraging skewed transcript abundance by RNA-Seq to increase the genomic depth of the tree of life. Proceedings of the National Academy of Sciences, USA 107, 14761481. doi: 10.1073/pnas.0910449107.
Jackson W. A. (2001). A short guide to humoral medicine. TRENDS in Pharmacological Sciences 22, 487489.
Keading A. J., Ast J. C., Pearce M. M., Urbanczyk H., Kimura S., Endo H., Nakamura M. and Dunlap P. V. (2007). Phylogenetic diversity and cosymbiosis in the bioluminescent symbioses of “Photobacterium mandapamensis. Applied and Environmental Microbiology 73, 31733182. doi:10.1128/AEM.02212-06.
Kiskuchi Y. and Fukatsu T. (2002). Endosymbiotic bacteria in the esophageal organ of glossiphoniid leeches. Applied and Environmental Microbiology 68, 46374641. doi:10.1128/AEM.68.9.4637-4641.2002.
Kikuchi Y. and Graf J. (2007). Spatial and temporal population dynamics of a naturally occurring two-species microbial community inside the digestive tract of the medicinal leech. Applied and Environmental Microbiology 73, 19841991. doi:10.1128/AEM.01833-06.
Kimbell J. R. and McFall-Ngai M. J. (2003). The squid-Vibrio symbioses: from demes to genes. Integrative and Comparative Biology 43, 254260. doi: 10.1093/icb/43.2.254.
Kimbell J. R., McFall-Ngai M. J. and Roderick G. K. (2002). Two genetically distinct populations of bobtail squid, Euprymna scolopes, exist on the island of Oahu. Pacific Science 56, 347355. http://hdl.handle.net/10125/2570.
Kosakovsky Pond S. L., Frost S. D. W. and Muse. S. V. (2005). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676679. doi:10.1093/bioinformatics/bti079.
Kosiol C., Vinar T., da Fonseca R. R., Hubisz M. J., Bustamante C. D., Nielsen R. and Siepel A. (2008). Patterns of positive selection in six mammalian genomes. PLoS Genetics 4, e1000144. doi:10.1371/journal.pgen.1000144.
Kristensen D. M., Kannan L., Coleman M. K., Wolf Y. I., Sorokin A., Koonin E. V. and Mushegian A. (2010). A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches. Bioinformatics 26, 14811487.
Kvist S., Montanari S. A., Yi H., Fuks B. and Siddall M. E. (2011). Teaching Biodiversity & Evolutionary Biology in a North American Marine Coastal Environment. The American Biology Teacher 73, 7277. doi:10.1525/abt.2011.73.2.4.
Lakatos I. (1971). History of science and its rational reconstruction. Proceedings of the Biennial Meeting of the Philosophy of Science Association 1970, 91136 http://www.jstor.org/stable/495757.
Lapatto R., Krengel U., Schreuder H. A., Arkema A., de Boer B., Kalk K. H., Hol W. G., Grootenhuis P. D., Mulders J. W., Dijkema R., Theunissen H. J. and Dijkstra B. W. (1997). X-ray structure of antistasin at 1·9 A resolution and its modelled complex with blood coagulation factor Xa. EMBO Journal 16, 51515161. doi:10.1093/emboj/16.17.5151.
Laufer A. S., Siddall M. E. and Graf J. (2008). Characterization of the digestive-tract microbiota of Hirudo orientalis, a European medicinal leech. Applied and Environmental Microbiology 74, 61516154. doi:10.1128/AEM.00795-08.
Mason T. A., McIlroy P. J. and Shain D. H. (2004). A cysteine-rich protein in the Theromyzon (Annelida: Hirudinea) cocoon membrane. Federation of European Biochemical Societies Letters 561, 167172. doi:10.1016/S0014-5793(04)00167-X.
Markwardt F. (1992). Hirudin: The promising antithrombotic. Cardiovascular Drug Reviews 10, 211232. doi:10.1111/j.1527-3466.1992.tb00247.x.
McLaughlin D. J., Hibbett D. S., Lutzoni F., Spatafora’ J. W. and Vilgalys R. (2009). The search for the fungal tree of life. Trends in Microbiology 17, 488497. doi:10.1016/j.tim.2009.08.001.
Min G-S., Sarkar I. N., and Siddall M. E. (2010). Salivary transcriptome of the North American medicinal leech, Macrobdella decora. Journal of Parasitology 96, 12111221. doi:10.1645/GE-2496.1.
Morabia A. (1996). P. C. A. Louis and the birth of clinical epidemiology. Journal of Clinical Epidemiology 49, 13271333. doi:10.1016/S0895-4356(96)00294-6.
Moran N. A. (2001). The coevolution of bacterial endosymbionts and phloem-feeding insects. Annals of the Missouri Botanical Garden 88, 3544. http://www.jstor.org/stable/2666130.
Munro R., Siddall M., Desser S. S., and Sawyer R. T. (1992). The leech as a tool for studying comparative haematology. Comparative Haematology International 2, 7578. doi:10.1007/BF00186263.
Nishiguchi M. K. (2002). Host-symbiont recognition in the environmentally transmitted sepiolid squid-Vibrio mutualism. Microbial Ecology 44, 1018. doi:10.1007/BF03036870.
Nishiguchi M. K., Lopez J. E. and Boletzky S. V. (2004). Enlightenment of old ideas from new investigations: more questions regarding the evolution of bacteriogenic light organs in squids. Evolution and Development 6, 4149. doi:10.1111/j.1525-142X.2004.04009.x.
Nishiguchi M. K., Ruby E. G. and McTall-Ngai M. J. (1998). Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid-vibrio symbioses. Applied and Environmental Microbiology 64, 32093213.
Nixon K. C. (1999). The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15, 407414. doi:10.1111/j.1096-0031.1999.tb00277.x.
Nogge G. (1981). Significance of symbionts for the maintenance of an optional nutritional state for successful reproduction in haematophagous arthropods. Parasitology 82, 101104.
Nylander J. A. A., Olsson U., Alström P. and Sanmartín I. (2008). Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to Dispersal-vicariance Analysis of the thrushes (Aves: Turdus). Systematic Biology 57, 257268. doi: 10.1080/10635150802044003.
Oceguera-Figueroa A., Phillips A. J., Pacheco-Chaves B., Reeves W. K. and Siddall M. E. (2011). Phylogeny of macrophagous leeches (Hirudinea, Clitellata) based on molecular data and evaluation of the barcoding locus. Zoologica Scripta 40, 194203. doi:10.1111/j.14636-409.2010.00465.x.
Page R. D. M. (1990). Component analysis: a valiant failure? Cladistics 6, 119136. doi:10.1111/j.1096-0031.1990.tb00532.x.
Perkins S. L., Budinoff R. B. and Siddall M. E. (2005). New gammaproteobacteria associated with blood-feeding leeches and a broad phylogenetic analysis of leech endosymbionts. Applied and Environmental Microbiology 71, 52195224. doi:10.1128/AEM.71.9.5219-5224.2005.
Phillips A. J., Arauco-Brown R., Oceguera-Figueroa A., Gomez G. P., Beltran M., Lai Y.-T. and Siddall M. E. (2010). Tyrannobdella rex n. gen. n. sp. and the evolutionary origins of mucosal leech infestations. PLoS ONE 5, e10057. doi:10.1371/journal.pone.0010057.
Phillips A. J. and Siddall M. E. (2005). Phylogeny of the New World medicinal leech family Macrobdellidae (Oligochaeta: Hirudinida: Arhynchobdellida). Zoologica Scripta 34, 559564. doi:10.1111/j.1463-6409.2005.00210.x.
Phillips A. J. and Siddall M. E. (2009). Poly-paraphyly of Hirudinidae: Many lineages of medicinal leeches. BMC Evolutionary Biology 9, 246256. doi:10.1186/1471-2148-9-246.
Pond S. L. K. and Frost S. D. W. (2005). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 25312533. doi: 10.1093/bioinformatics/bti320.
Poon A. F. Y., Lewis F. I., Kosakovsky Pond S. L. and Frost S. D. W. (2007). An evolutionary-network model reveals stratified interactions in the V3 loop of the HIV-1 envelope. PLoS Computational Biology 3, e231. doi:10.1371/journal.pcbi.0030231.
Rados C. (2004). Beyond bloodletting: FDA gives leeches a medical makeover. FDA Consumer 38, 9.
Ree R. H. and Smith S. A. (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 414. doi: 10.1080/10635150701883881.
Rio R. V. M. (2008). Tsetse fly and medicinal leech symbioses: providing insights into microbial species interactions within gastrointestinal systems. Vie Milieu 58, 153163.
Rio R. V. M., Anderegg M. and Graf J. (2007). Characterization of a catalase gene from Aeromonas veronii, the digestive-tract symbiont of the medicinal leech. Microbiology 153, 18971906. doi:10.1099/mic.0.2006/003020-0
Rio R. V. M., Maltz M., McCormick B., Reiss A. and Graf J. (2009). Symbiont succession during embryonic development of the European medicinal leech, Hirudo verbana. Applied and Environmental Microbiology 75, 68906895. doi:10.1128/AEM.01129-09.
Rocha E. P., Smith J. M., Hurst L. D., Holden M. T., Cooper J. E., Smith N. H. and Feil E. J. (2005). Comparisons of dN/dS are time dependent for closely related bacterial genomes. Journal of Theoretical Biology 239, 226–35.
Ronquist F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195203. doi: 10.1093/sysbio/46.1.195.
Salzet M. (2001). Anticoagulants and inhibitors of platelet aggregation derived from leeches. Federation of European Biochemical Societies Letters 429, 187192. doi:10.1016/S0014-5793(01)02212-8.
Sawyer R. T. (1999). The trade in medicinal leeches in the southern Indian Ocean in the nineteenth century. Medical History 43, 241245.
Scheffler K., Martin D. P. and Seoighe C. (2006). Robust inference of positive selection from recombining coding sequences. Bioinformatics 22, 24932499. doi: 10.1093/bioinformatics/btl427.
Siddall M. E. (2002). Phylogeny and revision of the leech family Erpobdellidae (Hirudinida: Oligochaeta). Invertebrate Systematics 16, 16. doi:10.1071/IT01011.
Siddall M. E., Apakupakul K., Burreson E. M., Coates K. A., Erséus C., Gelder S. R., Källersjö M. and Trapido-Rosenthal H. (2001). Validating Livanow: Molecular data agree that leeches, Branchiobdellidans and Acanthobdella peledina form a monophyletic group of Oligochaetes. Molecular Phylogenetics and Evolution 21, 346351. doi:10.1006/mpev.2001.1021.
Siddall M. E., Budinoff R. B., and Borda E. (2005). Phylogenetic evaluation of systematics and biogeography of the leech family Glossphoniidae. Invertebrate Systematics 19, 105112. doi:10.1071/IS04034.
Siddall M. E. and Burreson E. M. (1998). Phylogeny of leeches (Hirudinea) based on mitochondrial cytochrome c Oxidase Subunit I. Molecular Phylogenetics and Evolution 9, 156162. doi:10.1006/mpev.1997.0455.
Siddall M. E. and Burreson E. M. (1995). Phylogeny of the Euhirudinea: Independent evolution of blood feeding by leeches? Canadian Journal of Zoology 73, 10481064. doi:10.1139/z95-125.
Siddall M. E., Perkins S. L. and Desser S. S. (2004). Leech mycetome endosymbionts are a new lineage of alphaproteobacteria related to the Rhizobiaceae. Molecular Phylogenetics and Evolution 30, 178186. doi:10.1016/S1055-7903(03)00184-2.
Siddall M. E., Trontelj P., Utevsky S. Y., Nkamany M. and Macdonald K. S. (2007 a). Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis. Proceedings of the Royal Society B 274, 14811487. doi: 10.1098/rspb.2007.0248.
Siddall M. E., Worthen P. L., Johnson M. and Graf J. (2007 b). Novel role for Aeromonas jandaei as a digestive tract symbiont of the North American medicinal leech. Applied and Environmental Microbiology 73, 655658. doi: 10.1128/AEM.01282-06.
Silver A., Rabinowitz N. M., Küffer S. and Graf J. (2007). Identification of Aeromonas veronii genes required for colonization of the medicinal leech, Hirudo verbana. Journal of Bacteriology 189, 67636772. doi:10.1128/JB.00685-07.
Soto W., Gutierrez J., Remmenga M. D. and Nishiguchi M. K. (2009). Salinity and temperature effects of physiological responses of Vibrio fischeri from diverse ecological niches. Microbial Ecology 57, 140150. doi:10.1007/s00248-008-9412-9.
Utevsky S. Y. and Trontelj P. (2004). Phylogenetic relationships of fish leeches (Hirudinea, Piscicolidae) based on mitochondrial DNA sequences and morphological data. Zoologica Scripta 33, 375385. doi:10.1111/j.0300-3256.2004.00156.x.
Warren R. L., Sutton G. G., Jones S. M. J. and Holt R. A. (2007). Assembling millions of short DNA sequences using SSAKE. Bioinformatics 23, 500501. doi:10.1093/bioinformatics/btl629.
Whitaker I. S., Kamya C., Azzopardi E. A., Graf J., Kon M. and Lineaweaver W. C. (2009). Preventing infective complications following leech therapy: Is practice keeping pace with current research? Microsurgery 29, 619625. doi:10.1002/micr.20666.
Williams J. I. and Burreson E. M. (2006). Phylogeny of the fish leeches (Oligochaeta, Hirudinida, Piscicolidae) based on nuclear and mitochondrial genes and morphology. Zoologica Scripta 35, 627639. doi:10.1111/j.1463-6409.2006.00246.x.
Worthen P. L., Gode C. J. and Graf J. (2006). Culture-independent characterization of the digestive-tract microbiota of the medicinal leech reveals a tripartite symbiosis. Applied and Environmental Microbiology 72, 47754781. doi:10.1128/AEM.00356-06.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 6
Total number of PDF views: 37 *
Loading metrics...

Abstract views

Total abstract views: 745 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 25th November 2017. This data will be updated every 24 hours.