Phylogenomic and biogeographic reconstruction of the Trichinella complex

Nature Communications

Volumn 7, Issue , 2016, Pages

  Korhonen, Pasi K ^a   Pozio, Edoardo ^b   La Rosa, Giuseppe ^b   Chang, Bill C H ^a,c   Koehler, Anson V ^a   Hoberg, Eric P ^d   Boag, Peter R ^e   Tan, Patrick ^f,g   Jex, Aaron R ^a   Hofmann, Andreas ^a,h   Sternberg, Paul W ⁱ   Young, Neil D ^a   Gasser, Robin B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c Yourgene Bioscience Inc   (Taiwan)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e MONASH UNIVERSITY   (Australia)

^f GENOME INSTITUTE OF SINGAPORE   (Singapore)

^g DUKE NUS MEDICAL SCHOOL   (Singapore)

^h GRIFFITH UNIVERSITY   (Australia)

ⁱ CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELMINTH PROTEIN; TRANSCRIPTOME;

BIODIVERSITY; BIOGEOGRAPHY; COMMON ANCESTRY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; GENETIC VARIATION; GENOME; GENOTYPE; PARASITIC DISEASE; PHYLOGENY; POPULATION GENETICS;

AMINO ACID SEQUENCE; ARTICLE; ENCAPSULATION; EVOLUTIONARY ADAPTATION; GENE SEQUENCE; GENETIC DIFFERENCE; GENETIC VARIABILITY; GENOME; GENOME SIZE; HOST PARASITE INTERACTION; MICROBIAL DIVERSITY; NONHUMAN; PHYLOGENOMICS; PHYLOGEOGRAPHY; TAXONOMY; TRICHINELLA; TRICHINELLA BRITOVI; TRICHINELLA MURRELLI; TRICHINELLA NATIVA; TRICHINELLA NELSONI; TRICHINELLA PATAGONIENSIS; TRICHINELLA SPIRALIS; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GENOTYPE; PHYLOGENY; PHYSIOLOGY;

MYA; NEMATODA; TRICHINELLA;

ANIMALS; GENE EXPRESSION REGULATION; GENOME, HELMINTH; GENOMICS; GENOTYPE; PHYLOGENY; TRICHINELLA;

EID: 84956693743     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10513     Document Type: Article

References (75)

1. Pozio, E. World distribution of Trichinella spp. infections in animals and humans. Vet. Parasitol. 149, 3-21 (2007).
2. Murrell, K. D., Pozio, E. Worldwide occurrence and impact of human trichinellosis, 1986-2009. Emerg. Infect. Dis. 17, 2194-2202 (2011).
3. Owen, I. L., Gomez Morales, M. A., Pezzotti, P., Pozio, E. Trichinella infection in a hunting population of Papua New Guinea suggests an ancient relationship between Trichinella and human beings. Trans. R Soc. Trop. Med. Hyg. 99, 618-624 (2005).
4. Ribicich, M., Gamble, H. R., Rosa, A., Bolpe, J., Franco, A. Trichinellosis in Argentina: an historical review. Vet. Parasitol. 132, 137-142 (2005).
5. Blaga, R. et al. A dramatic increase in the incidence of human trichinellosis in Romania over the past 25 years: impact of political changes and regional food habits. Am. J. Trop. Med. Hyg. 76, 983-986 (2007).
6. Barennes, H. et al. A major trichinellosis outbreak suggesting a high endemicity of Trichinella infection in northern Laos. Am. J. Trop. Med. Hyg. 78, 40-44 (2008).
7. Vu Thi, N. et al. High prevalence of anti-Trichinella IgG in domestic pigs of the Son La province, Vietnam. Vet. Parasitol. 168, 136-140 (2010).
8. Cui, J., Wang, Z. Q., Xu, B. L. The epidemiology of human trichinellosis in China during 2004-2009. Acta Trop. 118, 1-5 (2011).
9. Cuttell, L., Cookson, B., Jackson, L. A., Gray, C., Traub, R. J. First report of a Trichinella papuae infection in a wild pig (Sus scrofa) from an Australian island in the Torres Strait region. Vet. Parasitol. 185, 343-345 (2012).
10. Pozio, E., Hoberg, E., La Rosa, G., Zarlenga, D. S. Molecular taxonomy, phylogeny and biogeography of nematodes belonging to the Trichinella genus. Infect. Genet. Evol. 9, 606-616 (2009).
11. Pozio, E., Zarlenga, D. S. New pieces of the Trichinella puzzle. Int. J. Parasitol. 43, 983-997 (2013).
12. Pozio, E., Murrell, K. D. Systematics and epidemiology of Trichinella. Adv. Parasitol. 63, 367-439 (2006).
13. Krivokapich, S. J. et al. Trichinella patagoniensis n. sp. (Nematoda), a new encapsulated species infecting carnivorous mammals in South America. Int. J. Parasitol. 42, 903-910 (2012).
14. Zarlenga, D. S., Rosenthal, B. M., La Rosa, G., Pozio, E., Hoberg, E. P. Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella. Proc. Natl Acad. Sci. USA 103, 7354-7359 (2006).
15. Krivokapich, S. J. et al. Molecular evidence for a novel encapsulated genotype of Trichinella from Patagonia, Argentina. Vet. Parasitol. 156, 234-240 (2008).
16. Mardis, E. R. The impact of next-generation sequencing technology on genetics. Trends Genet. 24, 133-141 (2008).
17. Cantacessi, C., Campbell, B. E., Gasser, R. B. Key strongylid nematodes of animals-impact of next-generation transcriptomics on systems biology and biotechnology. Biotechnol. Adv. 30, 469-488 (2012).
18. Koboldt, D. C., Steinberg, K. M., Larson, D. E., Wilson, R. K., Mardis, E. R. The next-generation sequencing revolution and its impact on genomics. Cell 155, 27-38 (2013).
19. Mitreva, M. et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat. Genet. 43, 228-235 (2011).
20. Webb, K. M., Rosenthal, B. M. Next-generation sequencing of the Trichinella murrelli mitochondrial genome allows comprehensive comparison of its divergence from the principal agent of human trichinellosis, Trichinella spiralis. Infect. Genet. Evol. 11, 116-123 (2011).
21. Mohandas, N. et al. Mitochondrial genomes of Trichinella species and genotypes-a basis for diagnosis, and systematic and epidemiological explorations. Int. J. Parasitol. 44, 1073-1080 (2014).
22. Jex, A. R. et al. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat. Genet. 46, 701-706 (2014).
23. Jex, A. R. et al. Ascaris suum draft genome. Nature 479, 529-533 (2011).
24. Schwarz, E. M. et al. The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome Biol. 14, R89 (2013).
25. Laing, R. et al. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol. 14, R88 (2013).
26. Zhu, X.-Q. et al. Genetic blueprint of the zoonotic pathogen Toxocara canis. Nat. Commun. 6, 6145 (2015).
27. Ghedin, E. et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756-1760 (2007).
28. C. elegans Sequencing Consortium, C. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018 (1998).
29. Robinson, M. W., Connolly, B. Proteomic analysis of the excretory-secretory proteins of the Trichinella spiralis L1 larva, a nematode parasite of skeletal muscle. Proteomics 5, 4525-4532 (2005).
30. Robinson, M. W., Gare, D. C., Connolly, B. Profiling excretory/secretory proteins of Trichinella spiralis muscle larvae by two-dimensional gel electrophoresis and mass spectrometry. Vet. Parasitol. 132, 37-41 (2005).
31. Robinson, M. W., Greig, R., Beattie, K. A., Lamont, D. J., Connolly, B. Comparative analysis of the excretory-secretory proteome of the muscle larva of Trichinella pseudospiralis and Trichinella spiralis. Int. J. Parasitol. 37, 139-148 (2007).
32. Robinson, M. W., Massie, D. H., Connolly, B. Secretion and processing of a novel multi-domain cystatin-like protein by intracellular stages of Trichinella spiralis. Mol. Biochem. Parasitol. 151, 9-17 (2007).
33. Rota-Stabelli, O., Daley, A. C., Pisani, D. Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr. Biol. 23, 392-398 (2013).
34. McGowran, B. et al. Neogene and quaternary coexisting in the geological time scale: the inclusive compromise. Earth Sci. Rev. 96, 249-262 (2009).
35. Hilgen, F. et al. The Global boundary Stratotype Section and Point (GSSP) of the Tortonian stage (Upper Miocene) at Monte Dei Corvi. Episodes 28, 6-17 (2005).
36. Hilgen, F. et al. The Global Boundary Stratotype Section and Point (GSSP) of the Messinian stage (uppermost Miocene). Episodes 23, 172-178 (2000).
37. Leckie, R. M., Webb, P.-N. Late oligocene-early miocene glacial record of the Ross Sea, Antarctica: evidence from DSDP Site 270. Geology 11, 578-582 (1983).
38. Keller, G., Barron, J. A. Paleoceanographic implications of Miocene deep-sea hiatuses. Geol. Soc. Am. Bull. 94, 590-613 (1983).
39. Janis, C. M. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annu. Rev. Ecol. Systematics 24, 467-500 (1993).
40. Molnar, P., England, P., Martinod, J. Mantle dynamics, uplift of the Tibetan Plateau, and the Indian monsoon. Rev. Geophys. 31, 357-396 (1993).
41. Markwick, P. J. Crocodilian diversity in space and time: the role of climate in paleoecology and its implication for understanding K/T extinctions. Paleobiology 24, 470-497 (1998).
42. Werdelin, L., Peigne, S. in Cenozoic Mammals of Africa. (eds Werdelin, L., Sanders, W. J.) 1008 (University of California Press, 2010).
43. Rosenthal, B. M. et al. Human dispersal of Trichinella spiralis in domesticated pigs. Infect. Genet. Evol. 8, 799-805 (2008).
44. Pozio, E. et al. Trichinella britovi etiological agent of sylvatic trichinellosis in the Republic of Guinea (West Africa) and a re-evaluation of geographical distribution for encapsulated species in Africa. Int. J. Parasitol. 35, 955-960 (2005).
45. Retallack, G. J. Cenozoic expansion of grasslands and climatic cooling. J. Geol. 109, 407-426 (2001).
46. Keeley, J. E., Rundel, P. W. Fire and the Miocene expansion of C4 grasslands. Ecol. Lett. 8, 683-690 (2005).
47. Van Valkenburgh, B. Major patterns in the history of carnivorous mammals. Annu. Rev. Earth Planet. Sci. 27, 463-493 (1999).
48. Hoberg, E. P., Galbreath, K. E., Cook, J. A., Kutz, S. J., Polley, L. Northern host-parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Adv. Parasitol. 79, 1-97 (2012).
49. Bacon, C. D. et al. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc. Natl Acad. Sci. USA 112, 6110-6115 (2015).
50. Hoorn, C., Flantua, S. Geology. An early start for the Panama land bridge. Science 348, 186-187 (2015).
51. Montes, C. et al. Middle Miocene closure of the Central American Seaway. Science 348, 226-229 (2015).
52. Johnson, W. E. et al. The late Miocene radiation of modern Felidae: a genetic assessment. Science 311, 73-77 (2006).
53. Ogasawara, K. Review and comments on late Neogene climatic fluctuations and the intermittence of the Bering Land Bridge. J. Asian Earth Sci. 16, 45-48 (1998).
54. Hoberg, E. P., Brooks, D. R. A macroevolutionary mosaic: episodic hostswitching, geographical colonization and diversification in complex hostparasite systems. J. Biogeogr. 35, 1533-1550 (2008).
55. Hoberg, E. P., Brooks, D. R. Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philos. Trans. R Soc. Lond. B. Biol. Sci. 370, pii: 20130553. doi:10.1098/rstb.2013.0553 (2015).
56. Bastolla, U., Moya, A., Viguera, E., van Ham, R. C. Genomic determinants of protein folding thermodynamics in prokaryotic organisms. J. Mol. Biol. 343, 1451-1466 (2004).
57. Bastien, O. et al. Analysis of the compositional biases in Plasmodium falciparum genome and proteome using Arabidopsis thaliana as a reference. Gene 336, 163-173 (2004).
58. Robinson, M. W. et al. A helminth cathelicidin-like protein suppresses antigen processing and presentation in macrophages via inhibition of lysosomal vATPase. FASEB J. 26, 4614-4627 (2012).
59. Richter, V. et al. Structural and functional analysis of MiD51, a dynamin receptor required for mitochondrial fission. J. Cell Biol. 204, 477-486 2014:
60. Mitreva, M. et al. Gene discovery in the adenophorean nematode Trichinella spiralis: an analysis of transcription from three life cycle stages. Mol. Biochem. Parasitol. 137, 277-291 (2004).
61. Capo, V. A., Despommier, D. D., Polvere, R. I. Trichinella spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. J. Parasitol. 84, 209-214 (1998).
62. Despommier, D. D. How Does trichinella spiralis make itself at home? Parasitol. Today 14, 318-323 (1998).
63. Matrisian, L. M. The matrix-degrading metalloproteinases. Bioessays 14, 455-463 (1992).
64. Chambers, R. C. et al. Thrombin stimulates fibroblast procollagen production via proteolytic activation of protease-activated receptor 1. Biochem. J. 333, 121-127 (1998).
65. Trap, C. et al. Cloning and analysis of a cDNA encoding a putative serine protease comprising two trypsin-like domains of Trichinella spiralis. Parasitol. Res. 98, 288-294 (2006).
66. Ochieng, J., Chaudhuri, G. Cystatin superfamily. J. Health Care Poor Underserved. 21, 51-70 (2010).
67. Khaznadji, E., Collins, P., Dalton, J. P., Bigot, Y., Moire, N. A new multidomain member of the cystatin superfamily expressed by Fasciola hepatica. Int. J. Parasitol. 35, 1115-1125 (2005).
68. Demetriou, M., Binkert, C., Sukhu, B., Tenenbaum, H. C., Dennis, J. W. Fetuin/alpha 2-HS glycoprotein is a transforming growth factor-beta type II receptor mimic and cytokine antagonist. J. Biol. Chem. 271, 12755-12761 (1996).
69. Knight, P. A. et al. Expression profiling reveals novel innate and inflammatory responses in the jejunal epithelial compartment during infection with Trichinella spiralis. Infect. Immun. 72, 6076-6086 (2004).
70. Hartmann, S., Lucius, R. Modulation of host immune responses by nematode cystatins. Int. J. Parasitol. 33, 1291-1302 (2003).
71. Pozio, E., La Rosa, G. Molecular Detection of Foodborne Pathogens (CRC Press, Taylor & Francis Group, 2010).
72. Mortazavi, A. et al. Scaffolding a Caenorhabditis nematode genome with RNA-seq. Genome Res. 20, 1740-1747 (2010).
73. Brown, C. T., Howe, A., Zhang, Q., Pyrkosz, A. B., Brom, T. H. A referencefree algorithm for computational normalization of shotgun sequencing data. http://arxiv.org/abs/1203.4802 (2012).
74. Zerbino, D. R., Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
75. Schulz, M. H., Zerbino, D. R., Vingron, M., Birney, E. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086-1092 (2012).