Genomic survey maps differences in the molecular complement of vesicle formation machinery between Giardia intestinalis assemblages

. 2023 Dec ; 17 (12) : e0011837. [epub] 20231218

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38109380

Giardia intestinalis is a globally important microbial pathogen with considerable public health, agricultural, and economic burden. Genome sequencing and comparative analyses have elucidated G. intestinalis to be a taxonomically diverse species consisting of at least eight different sub-types (assemblages A-H) that can infect a great variety of animal hosts, including humans. The best studied of these are assemblages A and B which have a broad host range and have zoonotic transmissibility towards humans where clinical Giardiasis can range from asymptomatic to diarrheal disease. Epidemiological surveys as well as previous molecular investigations have pointed towards critical genomic level differences within numerous molecular pathways and families of parasite virulence factors within assemblage A and B isolates. In this study, we explored the necessary machinery for the formation of vesicles and cargo transport in 89 Canadian isolates of assemblage A and B G. intestinalis. Considerable variability within the molecular complement of the endolysosomal ESCRT protein machinery, adaptor coat protein complexes, and ARF regulatory system have previously been reported. Here, we confirm inter-assemblage, but find no intra-assemblage variation within the trafficking systems examined. This variation includes losses of subunits belonging to the ESCRTIII as well as novel lineage specific duplications in components of the COPII machinery, ARF1, and ARFGEF families (BIG and CYTH). Since differences in disease manifestation between assemblages A and B have been controversially reported, our findings may well have clinical implications and even taxonomic, as the membrane trafficking system underpin parasite survival, pathogenesis, and propagation.

Zobrazit více v PubMed

Esch KJ, Petersen CA. Transmission and Epidemiology of Zoonotic Protozoal Diseases of Companion Animals. Clin Microbiol Rev. 2013;26(1):58–85. doi: 10.1128/CMR.00067-12 PubMed DOI PMC

Heyworth MF. Giardia duodenalis genetic assemblages and hosts. Parasite Paris Fr. 2016/03/16 ed. 2016;23:13–13. doi: 10.1051/parasite/2016013 PubMed DOI PMC

Cacciò SM, Beck R, Lalle M, Marinculic A, Pozio E. Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int J Parasitol. 2008;38(13):1523–31. doi: 10.1016/j.ijpara.2008.04.008 PubMed DOI

Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, et al.. Genomic Minimalism in the Early Diverging Intestinal Parasite Giardia lamblia. Science. 2007;317(5846):1921. doi: 10.1126/science.1143837 PubMed DOI

Adam RD, Dahlstrom EW, Martens CA, Bruno DP, Barbian KD, Ricklefs SM, et al.. Genome Sequencing of Giardia lamblia Genotypes A2 and B Isolates (DH and GS) and Comparative Analysis with the Genomes of Genotypes A1 and E (WB and Pig). Genome Biol Evol. 2013;5(12):2498–511. doi: 10.1093/gbe/evt197 PubMed DOI PMC

Franzén O, Jerlström-Hultqvist J, Castro E, Sherwood E, Ankarklev J, Reiner DS, et al.. Draft Genome Sequencing of Giardia intestinalis Assemblage B Isolate GS: Is Human Giardiasis Caused by Two Different Species? Petri W, editor. PLoS Pathog. 2009;5(8):e1000560. doi: 10.1371/journal.ppat.1000560 PubMed DOI PMC

Wielinga C, Thompson RCA, Monis P, Ryan U. Identification of polymorphic genes for use in assemblage B genotyping assays through comparative genomics of multiple assemblage B Giardia duodenalis isolates. Mol Biochem Parasitol. 2015;201(1):1–4. doi: 10.1016/j.molbiopara.2015.05.002 PubMed DOI

Xu F, Jex A, Svärd SG. A chromosome-scale reference genome for Giardia intestinalis WB. Sci Data. 2020;7(1):38. doi: 10.1038/s41597-020-0377-y PubMed DOI PMC

Klotz C, Schmid MW, Winter K, Ignatius R, Weisz F, Saghaug CS, et al.. Highly contiguous genomes of human clinical isolates of Giardia duodenalis reveal assemblage- and sub-assemblage-specific presence–absence variation in protein-coding genes. Microb Genomics. 2023. Mar 28;9(3). doi: 10.1099/mgen.0.000963 PubMed DOI PMC

Pollo SMJ, Reiling SJ, Wit J, Workentine ML, Guy RA, Batoff GW, et al.. Benchmarking hybrid assemblies of Giardia and prediction of widespread intra-isolate structural variation. Parasit Vectors. 2020;13(1):108. doi: 10.1186/s13071-020-3968-8 PubMed DOI PMC

Jerlström-Hultqvist J, Franzén O, Ankarklev J, Xu F, Nohýnková E, Andersson JO, et al.. Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics. 2010;11(1):543. doi: 10.1186/1471-2164-11-543 PubMed DOI PMC

Kooyman FNJ, Wagenaar JA, Zomer A. Whole-genome sequencing of dog-specific assemblages C and D of Giardia duodenalis from single and pooled cysts indicates host-associated genes. Microb Genomics. 2019;5(12):e000302. doi: 10.1099/mgen.0.000302 PubMed DOI PMC

Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia Assemblage E in Humans Points to a New Anthropozoonotic Cycle. J Infect Dis. 2016;214(8):1256–9. doi: 10.1093/infdis/jiw361 PubMed DOI

Adam RD. Chromosome-size variation in Giardia lamblia: the role of rDNA repeats. Nucleic Acids Res. 1992;20(12):3057–61. doi: 10.1093/nar/20.12.3057 PubMed DOI PMC

Tůmová P, Hofštetrová K, Nohýnková E, Hovorka O, Král J. Cytogenetic evidence for diversity of two nuclei within a single diplomonad cell of Giardia. Chromosoma. 2007;116(1):65–78. doi: 10.1007/s00412-006-0082-4 PubMed DOI

Ankarklev J, Jerlström-Hultqvist J, Ringqvist E, Troell K, Svärd SG. Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol. 2010;8(6):413–22. doi: 10.1038/nrmicro2317 PubMed DOI

Cacciò SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol. 2008;160(2):75–80. doi: 10.1016/j.molbiopara.2008.04.006 PubMed DOI

Ferguson LC, Smith-Palmer A, Alexander CL. An update on the incidence of human giardiasis in Scotland, 2011–2018. Parasit Vectors. 2020;13(1):291. doi: 10.1186/s13071-020-04160-9 PubMed DOI PMC

Minetti C, Lamden K, Durband C, Cheesbrough J, Fox A, Wastling JM. Determination of Giardia duodenalis assemblages and multi-locus genotypes in patients with sporadic giardiasis from England. Parasit Vectors. 2015;8:444–444. doi: 10.1186/s13071-015-1059-z PubMed DOI PMC

Minetti C, Lamden K, Durband C, Cheesbrough J, Platt K, Charlett A, et al.. Case-Control Study of Risk Factors for Sporadic Giardiasis and Parasite Assemblages in North West England. J Clin Microbiol. 2015. Oct;53(10):3133–40. doi: 10.1128/JCM.00715-15 PubMed DOI PMC

Noussa R. Basha El, Zaki Mayssa M., Hassanin Omayma M., Rehan Mohamed K., Omran Dalia. Giardia Assemblages A and B in Diarrheic Patients: A Comparative Study in Egyptian Children and Adults. J Parasitol. 2016;102(1):69–74. doi: 10.1645/14-676 PubMed DOI

Prucca CG, Lujan HD. Antigenic variation in Giardia lamblia. Cell Microbiol. 2009;11(12):1706–15. doi: 10.1111/j.1462-5822.2009.01367.x PubMed DOI

Rodríguez-Walker M, Molina CR, Luján LA, Saura A, Jerlström-Hultqvist J, Svärd SG, et al.. Comprehensive characterization of Cysteine-rich protein-coding genes of Giardia lamblia and their role during antigenic variation. Genomics. 2022;114(5):110462. doi: 10.1016/j.ygeno.2022.110462 PubMed DOI

Tsui CKM, Miller R, Uyaguari-Diaz M, Tang P, Chauve C, Hsiao W, et al.. Beaver Fever: Whole-Genome Characterization of Waterborne Outbreak and Sporadic Isolates To Study the Zoonotic Transmission of Giardiasis. mSphere. 2018;3(2):e00090–18. doi: 10.1128/mSphere.00090-18 PubMed DOI PMC

Natalie Prystajecky, Tsui Clement K.-M., Hsiao William W. L., Uyaguari-Diaz Miguel I., Jordan Ho, Patrick Tang, et al.. Giardia spp. Are Commonly Found in Mixed Assemblages in Surface Water, as Revealed by Molecular and Whole-Genome Characterization. Appl Environ Microbiol. 2015;81(14):4827–34. doi: 10.1128/AEM.00524-15 PubMed DOI PMC

Andrews S. FastQC: a quality control tool for high throughput sequence data [Internet]. 2010. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20(1):257. doi: 10.1186/s13059-019-1891-0 PubMed DOI PMC

Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics. 2011;12(1):385. PubMed PMC

Zimin AV, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA. The MaSuRCA genome assembler. Bioinformatics. 2013;29(21):2669–77. doi: 10.1093/bioinformatics/btt476 PubMed DOI PMC

Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinforma Oxf Engl. 2013;29(8):1072–5. doi: 10.1093/bioinformatics/btt086 PubMed DOI PMC

Kriventseva EV, Kuznetsov D, Tegenfeldt F, Manni M, Dias R, Simão FA, et al.. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2019;47(D1):D807–11. doi: 10.1093/nar/gky1053 PubMed DOI PMC

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2. doi: 10.1093/bioinformatics/btv351 PubMed DOI

Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al.. Welcome to the Tidyverse. Open Source Software. 2019;4(43):1686.

R Core Team. R: A Language and Environment for Statistical Computing [Internet]. R Foundation for Statistical Computing, Vienna, Austria; 2020. Available from: https://www.R-project.org/

Shumate A, Salzberg SL. Liftoff: accurate mapping of gene annotations. Bioinformatics. 2021;(btaa1016). Available from: 10.1093/bioinformatics/btaa1016 PubMed DOI PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34(18):3094–100. doi: 10.1093/bioinformatics/bty191 PubMed DOI PMC

Leung KF, Dacks JB, Field MC. Evolution of the Multivesicular Body ESCRT Machinery; Retention Across the Eukaryotic Lineage. Traffic. 2008;9(10):1698–716. doi: 10.1111/j.1600-0854.2008.00797.x PubMed DOI

Marti M, Regös A, Li Y, Schraner EM, Wild P, Müller N, et al.. An Ancestral Secretory Apparatus in the Protozoan Parasite Giardia intestinalis. J Biol Chem. 2003;278(27):24837–48. PubMed

Pipaliya SV, Santos R, Salas-Leiva D, Balmer EA, Wirdnam CD, Roger AJ, et al.. Unexpected organellar locations of ESCRT machinery in Giardia intestinalis and complex evolutionary dynamics spanning the transition to parasitism in the lineage Fornicata. BMC Evol Biol; 2021; 19(127) doi: 10.1186/s12915-021-01077-2 PubMed DOI PMC

Pipaliya SV, Thompson LA, Dacks JB. The reduced ARF regulatory system in Giardia intestinalis pre-dates the transition to parasitism in the lineage Fornicata. Int J Parasitol. 2021; 51(10):825–839. doi: 10.1016/j.ijpara.2021.02.004 PubMed DOI

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic Local Alignment Search Tool. 1990;8. PubMed

Karnkowska A, Treitli SC, Brzoň O, Novák L, Vacek V, Soukal P, et al.. The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion. Mol Biol Evol. 2019;36(10):2292–312. doi: 10.1093/molbev/msz147 PubMed DOI PMC

Salas-Leiva DE, Tromer EC, Curtis BA, Jerlström-Hultqvist J, Kolisko M, Yi Z, et al.. A free-living protist that lacks canonical eukaryotic DNA replication and segregation systems. Nat Commun. 2021; 12(1):6003. PubMed PMC

Tanifuji G, Takabayashi S, Kume K, Takagi M, Nakayama T, Kamikawa R, et al.. The draft genome of Kipferlia bialata reveals reductive genome evolution in fornicate parasites. PLOS ONE. 2018;13(3):e0194487. doi: 10.1371/journal.pone.0194487 PubMed DOI PMC

Ankarklev J, Franzén O, Peirasmaki D, Jerlström-Hultqvist J, Lebbad M, Andersson J, et al.. Comparative genomic analyses of freshly isolated Giardia intestinalis assemblage A isolates. BMC Genomics. 2015;16(1):697. doi: 10.1186/s12864-015-1893-6 PubMed DOI PMC

Weisz F, Lalle M, Nohynkova E, Sannella AR, Dluhošová J, Cacciò SM. Testing the impact of Whole Genome Amplification on genome comparison using the polyploid flagellated Giardia duodenalis as a model. Exp Parasitol. 2019;207:107776. doi: 10.1016/j.exppara.2019.107776 PubMed DOI

Upcroft JA, Chen N, Upcroft P. Mapping variation in chromosome homologues of different Giardia strains. Mol Biochem Parasitol. 1996;76(1):135–43. doi: 10.1016/0166-6851(95)02554-5 PubMed DOI

Upcroft JA, Krauer KG, Upcroft P. Chromosome sequence maps of the Giardia lamblia assemblage A isolate WB. Trends Parasitol. 2010;26(10):484–91. doi: 10.1016/j.pt.2010.07.002 PubMed DOI PMC

Faso C, Konrad C, Schraner EM, Hehl AB. Export of cyst wall material and Golgi organelle neogenesis in Giardia lamblia depend on endoplasmic reticulum exit sites: ER exit sites in Giardia lamblia. Cell Microbiol. 2013;15(4):537–53. PubMed

Hehl AB, Marti M, Köhler P. Stage-Specific Expression and Targeting of Cyst Wall Protein–Green Fluorescent Protein Chimeras in Giardia. Mol Biol Cell. 2000;11(5):1789–800. doi: 10.1091/mbc.11.5.1789 PubMed DOI PMC

Miras SL, Merino MC, Gottig N, Rópolo AS, Touz MC. The giardial VPS35 retromer subunit is necessary for multimeric complex assembly and interaction with the vacuolar protein sorting receptor. Biochim Biophys Acta BBA—Mol Cell Res. 2013;1833(12):2628–38. doi: 10.1016/j.bbamcr.2013.06.015 PubMed DOI PMC

Rivero MR, Miras SL, Feliziani C, Zamponi N, Quiroga R, Hayes SF, et al.. Vacuolar Protein Sorting Receptor in Giardia lamblia. PLOS ONE. 2012;7(8):e43712. doi: 10.1371/journal.pone.0043712 PubMed DOI PMC

Touz MC, Kulakova L, Nash TE. Adaptor Protein Complex 1 Mediates the Transport of Lysosomal Proteins from a Golgi-like Organelle to Peripheral Vacuoles in the Primitive Eukaryote Giardia lamblia. Mol Biol Cell. 2004;15(7):3053–60. PubMed PMC

Zumthor JP, Cernikova L, Rout S, Kaech A, Faso C, Hehl AB. Static Clathrin Assemblies at the Peripheral Vacuole—Plasma Membrane Interface of the Parasitic Protozoan Giardia lamblia. Johnson PJ, editor. PLOS Pathog. 2016;12(7):e1005756. doi: 10.1371/journal.ppat.1005756 PubMed DOI PMC

Saha N, Dutta S, Datta SP, Sarkar S. The minimal ESCRT machinery of Giardia lamblia has altered inter-subunit interactions within the ESCRT-II and ESCRT-III complexes. Eur J Cell Biol. 2018;97(1):44–62. doi: 10.1016/j.ejcb.2017.11.004 PubMed DOI

Stefanic S, Morf L, Kulangara C, Regos A, Sonda S, Schraner E, et al.. Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote. J Cell Sci. 2009;122(16):2846–56. PubMed

Zamponi N, Zamponi E, Mayol GF, Lanfredi-Rangel A, Svärd SG, Touz MC. Endoplasmic reticulum is the sorting core facility in the Golgi-lacking protozoan Giardia lamblia. Traffic. 2017;18(9):604–21. PubMed

de Queiroz K. Ernst Mayr and the modern concept of species. Proc Natl Acad Sci. 2005;102(suppl 1):6600. doi: 10.1073/pnas.0502030102 PubMed DOI PMC

de Queiroz K. Species Concepts and Species Delimitation. Syst Biol. 2007;56(6):879–86. doi: 10.1080/10635150701701083 PubMed DOI

Huey CS, Mahdy MAK, Al-Mekhlafi HM, Nasr NA, Lim YAL, Mahmud R, et al.. Multilocus genotyping of Giardia duodenalis in Malaysia. Infect Genet Evol. 2013;17:269–76. doi: 10.1016/j.meegid.2013.04.013 PubMed DOI

Lee H, Jung B, Lim JS, Seo MG, Lee SH, Choi KH, et al.. Multilocus genotyping of Giardia duodenalis from pigs in Korea. Parasitol Int. 2020;78:102154. doi: 10.1016/j.parint.2020.102154 PubMed DOI

Xu F, Jerlström-Hultqvist J, Andersson JO. Genome-Wide Analyses of Recombination Suggest That Giardia intestinalis Assemblages Represent Different Species. Mol Biol Evol. 2012;29(10):2895–8. doi: 10.1093/molbev/mss107 PubMed DOI

Andrews RH, Adams M, Boreham PFL, Mayrhofer G, Melonis BP. Giardia intestinalis: Electrophoretic evidence fora species complex. 1989; 19(2):183–90 PubMed

Cacciò SM, Lalle M, Svärd SG. Host specificity in the Giardia duodenalis species complex. Infect Genet Evol. 2018;66:335–45. doi: 10.1016/j.meegid.2017.12.001 PubMed DOI

Seabolt MH, Roellig DM, Konstantinidis KT. Genomic comparisons confirm Giardia duodenalis sub-assemblage AII as a unique species. Front Cell Infect Microbiol. 2022;12:1010244. doi: 10.3389/fcimb.2022.1010244 PubMed DOI PMC

Wielinga C, Williams A, Monis P, Thompson RCA. Proposed taxonomic revision of Giardia duodenalis. Infect Genet Evol. 2023;111:105430. doi: 10.1016/j.meegid.2023.105430 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...