Skip to main content
×
×
Home

Long-read sequencing improves assembly of Trichinella genomes 10-fold, revealing substantial synteny between lineages diverged over 7 million years

  • PETER C. THOMPSON (a1), DANTE S. ZARLENGA (a1), MING-YUAN LIU (a2) and BENJAMIN M. ROSENTHAL (a1)
Summary

Genome assemblies can form the basis of comparative analyses fostering insight into the evolutionary genetics of a parasite's pathogenicity, host–pathogen interactions, environmental constraints and invasion biology; however, the length and complexity of many parasite genomes has hampered the development of well-resolved assemblies. In order to improve Trichinella genome assemblies, the genome of the sylvatic encapsulated species Trichinella murrelli was sequenced using third-generation, long-read technology and, using syntenic comparisons, scaffolded to a reference genome assembly of Trichinella spiralis, markedly improving both. A high-quality draft assembly for T. murrelli was achieved that totalled 63·2 Mbp, half of which was condensed into 26 contigs each longer than 571 000 bp. When compared with previous assemblies for parasites in the genus, ours required 10-fold fewer contigs, which were five times longer, on average. Better assembly across repetitive regions also enabled resolution of 8 Mbp of previously indeterminate sequence. Furthermore, syntenic comparisons identified widespread scaffold misassemblies in the T. spiralis reference genome. The two new assemblies, organized for the first time into three chromosomal scaffolds, will be valuable resources for future studies linking phenotypic traits within each species to their underlying genetic bases.

Copyright
Corresponding author
*Corresponding author: USDA, Agricultural Research Service, Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, BARC-East Bldg. 1180 Rm. 104, 10300 Baltimore Avenue, Beltsville, MD 20705, USA. E-mail: pete.c.thompson@gmail.com
References
Hide All
Assefa, S., Keane, T. M., Otto, T. D., Newbold, C. and Berriman, M. (2009). ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25, 19681969.
Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.
Boyd, E. M. and Huston, E. J. (1954). The distribution, longevity and sex ratio of Trichinella spiralis in hamsters following an initial infection. The Journal of Parasitology 40, 686690.
Coghlan, A. and Wolfe, K. H. (2002). Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Research 12, 857867.
Darling, A. E., Mau, B. and Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147.
Dittmar, K. (2009). Old parasites for a new world: the future of paleoparasitological research. A review. Journal of Parasitology 95, 365371.
Foth, B. J., Tsai, I. J., Reid, A. J., Bancroft, A. J., Nichol, S., Tracey, A., Holroyd, N., Cotton, J. A., Stanley, E. J., Zarowiecki, M., Liu, J. Z., Huckvale, T., Cooper, P. J., Grencis, R. K. and Berriman, M. (2014). Whipworm genome and dual-species transcriptome analyses provide molecular insights into an intimate host-parasite interaction. Nature Genetics 46, 693700.
Garrett, K. A., Dendy, S. P., Frank, E. E., Rouse, M. N. and Travers, S. E. (2006). Climate change effects on plant disease: genomes to ecosystems. Annual Review of Phytopathology 44, 489509.
Ghedin, E., Bringaud, F., Peterson, J., Myler, P., Berriman, M., Ivens, A., Andersson, B., Bontempi, E., Eisen, J., Angiuoli, S., Wanless, D., Von Arx, A., Murphy, L., Lennard, N., Salzberg, S., Adams, M. D., White, O., Hall, N., Stuart, K., Fraser, C. M. and El-Sayed, N. M. A. (2004). Gene synteny and evolution of genome architecture in trypanosomatids. Molecular and Biochemical Parasitology 134, 183191.
Guiliano, D., Hall, N., Jones, S., Clark, L., Corton, C., Barrell, B. and Blaxter, M. (2002). Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes. Genome Biology 3, Research0057.1–Research0057.14.
Gurevich, A., Saveliev, V., Vyahhi, N. and Tesler, G. (2013). QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 10721075.
Gursch, O. F. (1949). Intestinal phase of Trichinella spiralis (Owen, 1835) Railliet, 1895. The Journal of Parasitology 35, 1926.
Hall, R. L., Lindsay, A., Hammond, C., Montgomery, S. P., Wilkins, P. P., da Silva, A. J., McAuliffe, I., de Almeida, M., Bishop, H., Mathison, B., Sun, B., Largusa, R. and Jones, J. L. (2012). Outbreak of human trichinellosis in northern California caused by Trichinella murrelli . The American Journal of Tropical Medicine and Hygiene 87, 297302.
Hillier, L. W., Miller, R. D., Baird, S. E., Chinwalla, A., Fulton, L. A., Koboldt, D. C. and Waterston, R. H. (2007). Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 5, e167.
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. Journal of Biogeography 35, 15331555.
Holterman, M., van der Wurff, A., van den Elsen, S., van Megen, H., Bongers, T., Holovachov, O., Bakker, J. and Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 17921800.
Husemann, P. and Stoye, J. (2010). r2cat: synteny plots and comparative assembly. Bioinformatics 26, 570571.
Kapel, C. M. O. and Gamble, H. R. (2000). Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. International Journal for Parasitology 30, 215221.
Kapel, C. M. O., Webster, P. and Gamble, H. R. (2005). Muscle distribution of sylvatic and domestic Trichinella larvae in production animals and wildlife. Veterinary Parasitology 132, 101105.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.
Korhonen, P. K., Pozio, E., La Rosa, G., Chang, B. C. H., Koehler, A. V., Hoberg, E. P., Boag, P. R., Tan, P., Jex, A. R., Hofmann, A., Sternberg, P. W., Young, N. D. and Gasser, R. B. (2016). Phylogenomic and biogeographic reconstruction of the Trichinella complex. Nature Communications 7, 10513.
Lanctôt, C., Cheutin, T., Cremer, M., Cavalli, G. and Cremer, T. (2007). Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nature Reviews Genetics 8, 104115.
Merchant, N., Lyons, E., Goff, S., Vaughn, M., Ware, D., Micklos, D. and Antin, P. (2016). The iPlant collaborative: cyberinfrastructure for enabling data to discovery for the life sciences. PLoS Biology 14, e1002342.
Mitreva, M. and Jasmer, D. P. (2008). Advances in the sequencing of the genome of the adenophorean nematode Trichinella spiralis . Parasitology 135, 869880.
Mitreva, M., Jasmer, D. P., Zarlenga, D. S., Wang, Z., Abubucker, S., Martin, J., Taylor, C. M., Yin, Y., Fulton, L., Minx, P., Yang, S.-P., Warren, W. C., Fulton, R. S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S. W., McCarter, J. P., Appleton, J., Mardis, E. R. and Wilson, R. K. (2011). The draft genome of the parasitic nematode Trichinella spiralis . Nature Genetics 43, 228235.
Mohandas, N., Pozio, E., La Rosa, G., Korhonen, P. K., Young, N. D., Koehler, A. V., Hall, R. S., Sternberg, P. W., Boag, P. R., Jex, A. R., Chang, B. C. H. and Gasser, R. B. (2014). Mitochondrial genomes of Trichinella species and genotypes – a basis for diagnosis, and systematic and epidemiological explorations. International Journal for Parasitology 44, 10731080.
Mutafova, T., Dimitrova, Y. and Komandarev, S. (1982). The karyotype of four Trichinella species. Seitschrift fur Parasitenkunde 67, 115120.
Parra, G., Bradnam, K. and Korf, I. (2007). CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 10611067.
Peacock, C. S., Seeger, K., Harris, D., Murphy, L., Ruiz, J. C., Quail, M. A., Peters, N., Adlem, E., Tivey, A., Aslett, M., Kerhornou, A., Ivens, A., Fraser, A., Rajandream, M.-A., Carver, T., Norbertczak, H., Chillingworth, T., Hance, Z., Jagels, K., Moule, S., Ormond, D., Rutter, S., Squares, R., Whitehead, S., Rabbinowitsch, E., Arrowsmith, C., White, B., Thurston, S., Bringaud, F., Baldauf, S. L., Faulconbridge, A., Jeffares, D., Depledge, D. P., Oyola, S. O., Hilley, J. D., Brito, L. O., Tosi, L. R. O., Barrell, B., Cruz, A. K., Mottram, J. C., Smith, D. F. and Berriman, M. (2007). Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nature Genetics 39, 839847.
Pozio, E. (2007). World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 321.
Raffaele, S. and Kamoun, S. (2012). Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 10, 417430.
Rappaport, I. (1943). A comparison of three strains of Trichinella spiralis II. Longevity and sex ratio of adults in the intestine and rapidity of larval development in the musculature. The American Journal of Tropical Medicine and Hygiene s1-23, 351362.
Richter, D. C., Schuster, S. C. and Huson, D. H. (2007). OSLay: optimal syntenic layout of unfinished assemblies. Bioinformatics 23, 15731579.
Simakov, O., Marletaz, F., Cho, S.-J., Edsinger-Gonzales, E., Havlak, P., Hellsten, U., Kuo, D.-H., Larsson, T., Lv, J., Arendt, D., Savage, R., Osoegawa, K., de Jong, P., Grimwood, J., Chapman, J. A., Shapiro, H., Aerts, A., Otillar, R. P., Terry, A. Y., Boore, J. L., Grigoriev, I. V., Lindberg, D. R., Seaver, E. C., Weisblat, D. A., Putnam, N. H. and Rokhsar, D. S. (2013). Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526531.
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. and Zdobnov, E. M. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 32103212. doi: 10.1093/bioinformatics/btv351.
Smit, A. F. and Hubley, R. (2008). RepeatModeler Open-1·0. http://www.repeatmasker.org
Smit, A. F., Hubley, R. and Green, P. (2013). RepeatMasker Open-4·0. http://www.repeatmasker.org
Webb, K. M. and Rosenthal, B. M. (2011). Next-generation sequencing of the Trichinella murrelli mitochondrial genome allows comprehensive comparison of its divergence from the principal agent of human trichinellosis, Trichinella spiralis . Infection, Genetics and Evolution 11, 116123.
Zarlenga, D. S., Al-Yaman, F., Minchella, D. J. and La Rosa, G. (1991). A repetitive DNA probe specific for a North American sylvatic genotype of Trichinella . Molecular and Biochemical Parasitology 48, 131137.
Zarlenga, D. S., Rosenthal, B. M., Rosa, G. L., Pozio, E. and Hoberg, E. P. (2006). Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella . Proceedings of the National Academy of Sciences 103, 73547359.
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

Altmetric attention score

Full text views

Total number of HTML views: 16
Total number of PDF views: 92 *
Loading metrics...

Abstract views

Total abstract views: 423 *
Loading metrics...

* Views captured on Cambridge Core between 6th June 2017 - 20th August 2018. This data will be updated every 24 hours.