Hostname: page-component-84b7d79bbc-fnpn6 Total loading time: 0 Render date: 2024-07-31T01:02:16.517Z Has data issue: false hasContentIssue false
  • English
  • Français

Diverse single-amino-acid repeat profiles in the genus Cryptosporidium

Published online by Cambridge University Press:  12 February 2018

Giovanni Widmer
Giovanni Widmer*
Affiliation:
Department of Infectious Disease & Global Health, Cummings School of Veterinary Medicine at Tufts University, 200 Westboro Road, Building 20, North Grafton, Massachusetts 01536, USA
*
Author for correspondence: Giovanni Widmer, E-mail: giovanni.widmer@tufts.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Genome sequencing has greatly contributed to our understanding of parasitic protozoa. This is particularly the case for Cryptosporidium species (phylum Apicomplexa) which are difficult to propagate. Because of their polymorphic nature, simple sequence repeats have been used extensively as genotypic markers to differentiate between isolates, but no global analysis of amino acid repeats in Cryptosporidium genomes has been reported. Taking advantage of several newly sequenced Cryptosporidium genomes, a comparative analysis of single-amino-acid repeats (SAARs) in seven species was undertaken. This analysis revealed a striking difference between the SAAR profile of the gastric and intestinal species which infect mammals and one species which infects birds. In average, total SAAR length in gastric species is only 25% of the cumulative SAAR length in the genome of Cryptosporidium parvum, Cryptosporidium hominis and Cryptosporidium meleagridis, species infectious to humans. The SAAR profile in the avian parasite Cryptosporidium baileyi stands out due to the presence of long asparagine repeats. Cryptosporidium baileyi proteins with repeats ⩾20 residues are significantly enriched in regulatory functions. As postulated for the related apicomplexan species Plasmodium falciparum, these observations suggest that Cryptosporidium SAARs evolve in response to selective pressure. The putative selective mechanisms driving SAAR evolution in Cryptosporidium species are unknown.

Keywords

cryptosporidiosisCryptosporidiummicrosatellitemucinsimple sequence repeatsingle-amino-acid repeat
Type
Research Article
Information
Parasitology , Volume 145 , Issue 9 , August 2018 , pp. 1151 - 1160
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Abrahamsen, MS, Templeton, TJ, Enomoto, S, Abrahante, JE, Zhu, G, Lancto, CA, Deng, M, Liu, C, Widmer, G, Tzipori, S, Buck, GA, Xu, P, Bankier, AT, Dear, PH, Konfortov, BA, Spriggs, HF, Iyer, L, Anantharaman, V, Aravind, L and Kapur, V (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441–445.Google Scholar
Afgan, E, Baker, D, van den Beek, M, Blankenberg, D, Bouvier, D, Cech, M, Chilton, J, Clements, D, Coraor, N, Eberhard, C, Gruning, B, Guerler, A, Hillman-Jackson, J, Von Kuster, G, Rasche, E, Soranzo, N, Turaga, N, Taylor, J, Nekrutenko, A and Goecks, J (2016) The galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Research 44, W3–W10.Google Scholar
An, L, Fitzpatrick, D and Harrison, PM (2016) Emergence and evolution of yeast prion and prion-like proteins. BMC Evolution Biol. 16, 24.Google Scholar
Aravind, L, Iyer, LM, Wellems, TE and Miller, LH (2003) Plasmodium biology: genomic gleanings. Cell 115, 771–785.Google Scholar
Barnes, DA, Bonnin, A, Huang, JX, Gousset, L, Wu, J, Gut, J, Doyle, P, Dubremetz, JF, Ward, H and Petersen, C (1998) A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion. Molecular Biochemical Parasitology 96, 93–110.Google Scholar
Bhalchandra, S, Ludington, J, Coppens, I and Ward, HD (2013) Identification and characterization of Cryptosporidium parvum Clec, a novel C-type lectin domain-containing mucin-like glycoprotein. Infection and Immunity 81, 3356–3365.Google Scholar
Braak, C and Šmilauer, P (2002) CANOCO Reference Manual and CanoDraw for Windows user's Guide: Software for Canonical Community Ordination (Version 4.5). Ithaca, New York: Microcomputer Power.Google Scholar
Capizzi, RL, Bertino, JR and Handschumacher, RE (1970) L-asparaginase. Annual Revue in Medicine 21, 433–444.Google Scholar
Cevallos, AM, Bhat, N, Verdon, R, Hamer, DH, Stein, B, Tzipori, S, Pereira, ME, Keusch, GT and Ward, HD (2000) Mediation of Cryptosporidium parvum infection in vitro by mucin-like glycoproteins defined by a neutralizing monoclonal antibody. Infection and Immunity 68, 5167–5175.Google Scholar
Chatterjee, A, Banerjee, S, Steffen, M, O'Connor, RM, Ward, HD, Robbins, PW and Samuelson, J (2010) Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryotic Cell 9, 84–96.Google Scholar
Cutts, EE, Laasch, N, Reiter, DM, Trenker, R, Slater, LM, Stansfeld, PJ and Vakonakis, I (2017) Structural analysis of P. falciparum KAHRP and PfEMP1 complexes with host erythrocyte spectrin suggests a model for cytoadherent knob protrusions. PLoS Pathogens 13(8), e1006552.Google Scholar
Davies, HM, Thalassinos, K and Osborne, AR (2016) Expansion of lysine-rich repeats in Plasmodium proteins generates novel localization sequences that target the periphery of the host erythrocytes. Journal of Biological Chemistry 291, 26188–26207.Google Scholar
DePristo, MA, Zilversmit, MM and Hartl, DL (2006) On the abundance, amino acid composition, and evolutionary dynamics of low-complexity regions in proteins. Gene 378, 19–30.Google Scholar
Escher, D, Bodmer-Glavas, M, Barberis, A and Schaffner, W (2000) Conservation of glutamine-rich transactivation function between yeast and humans. Molecular Cell Biology 20, 2774–2782.Google Scholar
Feng, Y, Tiao, N, Li, N, Hlavsa, M and Xiao, L (2014) Multilocus sequence typing of an emerging Cryptosporidium hominis subtype in the United States. Journal of Clinical Microbiology 52, 524–530.Google Scholar
Ferreira, MU, Ribeiro, WL, Tonon, AP, Kawamoto, F and Rich, SM (2003) Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene 304, 65–75.Google Scholar
Fidalgo, M, Barrales, RR, Ibeas, JI and Jimenez, J (2006) Adaptive evolution by mutations in the FLO11 gene. Proceedings of the National Academy of Sciences of the USA 103, 11228–112233.Google Scholar
Frugier, M, Bour, T, Ayach, M, Santos, MA, Rudinger-Thirion, J, Theobald-Dietrich, A and Pizzi, E (2010) Low complexity regions behave as tRNA sponges to help co-translational folding of plasmodial proteins. FEBS Letters 584, 448–454.Google Scholar
Gajria, B, Bahl, A, Brestelli, J, Dommer, J, Fischer, S, Gao, X, Heiges, M, Iodice, J, Kissinger, JC, Mackey, AJ, Pinney, DF, Roos, DS, Stoeckert, CJ Jr, Wang, H and Brunk, BP (2008) ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Research 36, D553–D556.Google Scholar
Garcia, RJ and Hayman, DT (2016) Origin of a major infectious disease in vertebrates: the timing of Cryptosporidium evolution and its hosts. Parasitology 143, 1683–1690.Google Scholar
Gatei, W, Das, P, Dutta, P, Sen, A, Cama, V, Lal, AA and Xiao, L (2007) Multilocus sequence typing and genetic structure of Cryptosporidium hominis from children in Kolkata, India. Infection, Genetics and Evolution 7, 197–205.Google Scholar
Heiges, M, Wang, H, Robinson, E, Aurrecoechea, C, Gao, X, Kaluskar, N, Rhodes, P, Wang, S, He, CZ, Su, Y, Miller, J, Kraemer, E and Kissinger, JC (2006) CryptoDB: a Cryptosporidium bioinformatics resource update. Nucleic Acids Research 34, D419–D422.Google Scholar
Holubova, N, Sak, B, Horcickova, M, Hlaskova, L, Kvetonova, D, Menchaca, S, McEvoy, J and Kvac, M (2016) Cryptosporidium avium n. sp. (Apicomplexa: Cryptosporidiidae) in birds. Parasitology Research 115, 2243–2251.Google Scholar
Hughes, AL (2004) The evolution of amino acid repeat arrays in Plasmodium and other organisms. Journal of Molecular Evolution 59, 528–535.Google Scholar
Ifeonu, OO, Chibucos, MC, Orvis, J, Su, Q, Elwin, K, Guo, F, Zhang, H, Xiao, L, Sun, M, Chalmers, RM, Fraser, CM, Zhu, G, Kissinger, JC, Widmer, G and Silva, JC (2016) Annotated draft genome sequences of three species of Cryptosporidium: Cryptosporidium meleagridis isolate UKMEL1, C. baileyi isolate TAMU-09Q1 and C. hominis isolates TU502_2012 and UKH1. Pathology of Disease 74(7), pii: ftw080.Google Scholar
Isaza, JP, Galvan, AL, Polanco, V, Huang, B, Matveyev, AV, Serrano, MG, Manque, P, Buck, GA and Alzate, JF (2015) Revisiting the reference genomes of human pathogenic Cryptosporidium species: reannotation of C. parvum Iowa and a new C. hominis reference. Science Reports 5, 16324.Google Scholar
Johansson, ME, Sjovall, H and Hansson, GC (2013) The gastrointestinal mucus system in health and disease. Nature Review in Gastroenterology and Hepatology 10, 352–361.Google Scholar
Karlin, S, Brocchieri, L, Bergman, A, Mrazek, J and Gentles, AJ (2002) Amino acid runs in eukaryotic proteomes and disease associations. Proceedings of the National Academy of Sciences U S A 99, 333–338.Google Scholar
Koprivnikar, J, McCloskey, J and Faderl, S (2017) Safety, efficacy, and clinical utility of asparaginase in the treatment of adult patients with acute lymphoblastic leukemia. Oncology Targets and Therapy 10, 1413–1422.Google Scholar
Krumsiek, J, Arnold, R and Rattei, T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23, 1026–1028.Google Scholar
Li, L, Stoeckert, CJ Jr and Roos, DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research 13, 2178–2189.Google Scholar
Mallon, ME, MacLeod, A, Wastling, JM, Smith, H and Tait, A (2003) Multilocus genotyping of Cryptosporidium parvum type 2: population genetics and sub-structuring. Infection Genetics and Evolution 3, 207–218.Google Scholar
McHugh, E, Batinovic, S, Hanssen, E, McMillan, PJ, Kenny, S, Griffin, MD, Crawford, S, Trenholme, KR, Gardiner, DL, Dixon, MW and Tilley, L (2015) A repeat sequence domain of the ring-exported protein-1 of Plasmodium falciparum controls export machinery architecture and virulence protein trafficking. Molecular Microbiology 98, 1101–1114.Google Scholar
Morgan, UM, Monis, PT, Xiao, L, Limor, J, Sulaiman, I, Raidal, S, O'Donoghue, P, Gasser, R, Murray, A, Fayer, R, Blagburn, BL, Lal, AA and Thompson, RC (2001) Molecular and phylogenetic characterisation of Cryptosporidium from birds. International Journal for Parasitology 31, 289–296.Google Scholar
Muralidharan, V and Goldberg, DE (2013) Asparagine repeats in Plasmodium falciparum proteins: good for nothing? PLoS Pathology 9, e1003488.Google Scholar
Muralidharan, V, Oksman, A, Iwamoto, M, Wandless, TJ and Goldberg, DE (2011) Asparagine repeat function in a Plasmodium falciparum protein assessed via a regulatable fluorescent affinity tag. Proceedings of the National Academy of Sciences U S A 108, 4411–4416.Google Scholar
Nagaraj, VA, Mukhi, D, Sathishkumar, V, Subramani, PA, Ghosh, SK, Pandey, RR, Shetty, MC and Padmanaban, G (2015) Asparagine requirement in Plasmodium berghei as a target to prevent malaria transmission and liver infections. Nature Communications 6, 8775.Google Scholar
Newman, AM and Cooper, JB (2007) XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8, 382.Google Scholar
O'Connor, RM, Burns, PB, Ha-Ngoc, T, Scarpato, K, Khan, W, Kang, G and Ward, H (2009) Polymorphic mucin antigens CpMuc4 and CpMuc5 are integral to Cryptosporidium parvum infection in vitro. Eukaryotic Cell 8, 461–469.Google Scholar
Okhuysen, PC, Rich, SM, Chappell, CL, Grimes, KA, Widmer, G, Feng, XC and Tzipori, S (2002) Infectivity of a Cryptosporidium parvum isolate of cervine origin for healthy adults and interferon-gamma knockout mice. Journal of Infectious Diseases 185, 1320–1325.Google Scholar
Paulson, HL (2000) Toward an understanding of polyglutamine neurodegeneration. Brain Pathology 10, 293–299.Google Scholar
Peakall, R and Smouse, PE (2012) Genalex 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.Google Scholar
Petersen, C, Gut, J, Nelson, RG and Leech, JH (1991) Characterization of a Cryptosporidium parvum sporozoite glycoprotein. Journal of Protozoology 38, 20S–21S.Google Scholar
Schaefer, MH, Wanker, EE and Andrade-Navarro, MA (2012) Evolution and function of CAG/polyglutamine repeats in protein-protein interaction networks. Nucleic Acids Research 40, 4273–4287.Google Scholar
Shimada, MK, Sanbonmatsu, R, Yamaguchi-Kabata, Y, Yamasaki, C, Suzuki, Y, Chakraborty, R, Gojobori, T and Imanishi, T (2016) Selection pressure on human STR loci and its relevance in repeat expansion disease. Molecular and Genetic Genomics 291, 1851–1869.Google Scholar
Sim, KL and Creamer, TP (2002) Abundance and distributions of eukaryote protein simple sequences. Molecular and Cellular Proteomics 1, 983–995.Google Scholar
Singh, GP, Chandra, BR, Bhattacharya, A, Akhouri, RR, Singh, SK and Sharma, A (2004) Hyper-expansion of asparagines correlates with an abundance of proteins with prion-like domains in Plasmodium falciparum. Molecular and Biochemical Parasitology 137, 307–319.Google Scholar
Slapeta, J (2013) Cryptosporidiosis and Cryptosporidium species in animals and humans: a thirty colour rainbow? Int J Parasitology 43, 957–970.Google Scholar
Slavin, D (1955) Cryptosporidium meleagridis (sp. nov.). Journal of Comparative Pathology 65, 262–266.Google Scholar
Steentoft, C, Vakhrushev, SY, Joshi, HJ, Kong, Y, Vester-Christensen, MB, Schjoldager, KT, Lavrsen, K, Dabelsteen, S, Pedersen, NB, Marcos-Silva, L, Gupta, R, Bennett, EP, Mandel, U, Brunak, S, Wandall, HH, Levery, SB and Clausen, H (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO Journal 32, 1478–1488.Google Scholar
Steinbiss, S, Silva-Franco, F, Brunk, B, Foth, B, Hertz-Fowler, C, Berriman, M and Otto, TD (2016) Companion: a web server for annotation and analysis of parasite genomes. Nucleic Acids Research 44, W29–W34.Google Scholar
Strong, WB, Gut, J and Nelson, RG (2000) Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infection and Immunity 68, 4117–4134.Google Scholar
Tanriverdi, S, Grinberg, A, Chalmers, RM, Hunter, PR, Petrovic, Z, Akiyoshi, DE, London, E, Zhang, L, Tzipori, S, Tumwine, JK and Widmer, G (2008) Inferences about the global population structures of Cryptosporidium parvum and Cryptosporidium hominis. Applied and Environmental Microbiology 74, 7227–7234.Google Scholar
van Eyk, CL, McLeod, CJ, O'Keefe, LV and Richards, RI (2012) Comparative toxicity of polyglutamine, polyalanine and polyleucine tracts in Drosophila models of expanded repeat disease. Human Molecular Genetics 21, 536–547.Google Scholar
Verstrepen, KJ, Jansen, A, Lewitter, F and Fink, GR (2005) Intragenic tandem repeats generate functional variability. Nature Genetics 37, 986–990.Google Scholar
Widmer, G, Lee, Y, Hunt, P, Martinelli, A, Tolkoff, M and Bodi, K (2012) Comparative genome analysis of two Cryptosporidium parvum isolates with different host range. Infection Genetics and Evolution 12, 1213–1221.Google Scholar
Wootton, JC (1994) Non-globular domains in protein sequences: automated segmentation using complexity measures. Computational Chemistry 18, 269–285.Google Scholar
Xu, P, Widmer, G, Wang, Y, Ozaki, LS, Alves, JM, Serrano, MG, Puiu, D, Manque, P, Akiyoshi, D, Mackey, AJ, Pearson, WR, Dear, PH, Bankier, AT, Peterson, DL, Abrahamsen, MS, Kapur, V, Tzipori, S and Buck, GA (2004) The genome of Cryptosporidium hominis. Nature 431, 1107–1112.Google Scholar
Young, ET, Sloan, JS and Van Riper, K (2000) Trinucleotide repeats are clustered in regulatory genes in Saccharomyces cerevisiae. Genetics 154, 1053–1068.Google Scholar
Zilversmit, MM, Volkman, SK, DePristo, MA, Wirth, DF, Awadalla, P and Hartl, DL (2010) Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Molecular Biology and Evolution 27, 2198–2209.Google Scholar
Supplementary material: File

Widmer supplementary material 1

Widmer supplementary material

Download Widmer supplementary material 1(File)
File 790 KB