Complete representation of a tapeworm genome reveals chromosomes capped by centromeres, necessitating a dual role in segregation and protection.
Centromeres
Chromosome assembly
Flatworms
Hymenolepis
Telomere loss
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
09 11 2020
09 11 2020
Historique:
received:
11
06
2020
accepted:
14
10
2020
entrez:
10
11
2020
pubmed:
11
11
2020
medline:
3
7
2021
Statut:
epublish
Résumé
Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution. Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes. Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.
Sections du résumé
BACKGROUND
Chromosome-level assemblies are indispensable for accurate gene prediction, synteny assessment, and understanding higher-order genome architecture. Reference and draft genomes of key helminth species have been published, but little is yet known about the biology of their chromosomes. Here, we present the complete genome of the tapeworm Hymenolepis microstoma, providing a reference quality, end-to-end assembly that represents the first fully assembled genome of a spiralian/lophotrochozoan, revealing new insights into chromosome evolution.
RESULTS
Long-read sequencing and optical mapping data were added to previous short-read data enabling complete re-assembly into six chromosomes, consistent with karyology. Small genome size (169 Mb) and lack of haploid variation (1 SNP/3.2 Mb) contributed to exceptionally high contiguity with only 85 gaps remaining in regions of low complexity sequence. Resolution of repeat regions reveals novel gene expansions, micro-exon genes, and spliced leader trans-splicing, and illuminates the landscape of transposable elements, explaining observed length differences in sister chromatids. Syntenic comparison with other parasitic flatworms shows conserved ancestral linkage groups indicating that the H. microstoma karyotype evolved through fusion events. Strikingly, the assembly reveals that the chromosomes terminate in centromeric arrays, indicating that these motifs play a role not only in segregation, but also in protecting the linear integrity and full lengths of chromosomes.
CONCLUSIONS
Despite strong conservation of canonical telomeres, our results show that they can be substituted by more complex, species-specific sequences, as represented by centromeres. The assembly provides a robust platform for investigations that require complete genome representation.
Identifiants
pubmed: 33167983
doi: 10.1186/s12915-020-00899-w
pii: 10.1186/s12915-020-00899-w
pmc: PMC7653826
doi:
Substances chimiques
DNA Transposable Elements
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
165Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 206194
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M003949/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : MR/L001020/1
Pays : United Kingdom
Références
Genome Biol. 2013 Jan 30;14(1):R10
pubmed: 23363705
Curr Opin Genet Dev. 1997 Dec;7(6):822-8
pubmed: 9468793
Sci Rep. 2018 Mar 1;8(1):3877
pubmed: 29497070
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Genome Biol. 2011 Oct 24;12(10):R107
pubmed: 22023798
Nat Rev Mol Cell Biol. 2016 Jan;17(1):16-29
pubmed: 26601620
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Bioinformatics. 2016 Mar 1;32(5):767-9
pubmed: 26559507
Nat Commun. 2014 Jul 09;5:4378
pubmed: 25007141
Exp Parasitol. 1969 Aug;25(1):72-84
pubmed: 5362601
Genome Res. 2010 Aug;20(8):1112-21
pubmed: 20606017
Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4209-14
pubmed: 22371573
Nature. 2013 Apr 04;496(7443):57-63
pubmed: 23485966
BMC Biol. 2018 Feb 26;16(1):25
pubmed: 29482548
BMC Genomics. 2017 May 26;18(1):414
pubmed: 28549457
Genome Biol. 2004;5(2):R12
pubmed: 14759262
Elife. 2019 Sep 16;8:
pubmed: 31524597
Bioinformatics. 2009 Jul 15;25(14):1836-7
pubmed: 19439563
Mol Phylogenet Evol. 2013 Nov;69(2):313-9
pubmed: 22982435
PLoS Negl Trop Dis. 2012 Jan;6(1):e1455
pubmed: 22253936
Plant Biotechnol J. 2016 Jul;14(7):1523-31
pubmed: 26801360
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Evodevo. 2018 Nov 9;9:21
pubmed: 30455861
G3 (Bethesda). 2019 Apr 9;9(4):1211-1230
pubmed: 30770412
J Theor Biol. 1973 Sep 14;41(1):181-90
pubmed: 4754905
Mol Biochem Parasitol. 2017 Jul;215:23-29
pubmed: 28126543
Nat Genet. 2012 Jan 15;44(2):221-5
pubmed: 22246508
J Biol Chem. 2000 Dec 8;275(49):38311-8
pubmed: 10973970
Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9451-9457
pubmed: 32300014
Genome Res. 2003 Jun;13(6A):1216-21
pubmed: 12799353
Genome Res. 2017 May;27(5):722-736
pubmed: 28298431
Curr Biol. 2006 Jan 10;16(1):R8-9
pubmed: 16401417
Trends Genet. 1995 Feb;11(2):58-62
pubmed: 7716808
EBioMedicine. 2017 Jul;21:14-20
pubmed: 28347656
BMC Biol. 2016 Mar 04;14:10
pubmed: 26941070
Genome Res. 2003 Sep;13(9):2178-89
pubmed: 12952885
Nat Genet. 2019 Jan;51(1):163-174
pubmed: 30397333
Gene. 2014 Jan 1;533(1):156-67
pubmed: 24120894
Bioinformatics. 2011 Aug 1;27(15):2156-8
pubmed: 21653522
Can J Genet Cytol. 1981;23(1):151-4
pubmed: 7237234
Cytogenet Genome Res. 2015;147(4):217-39
pubmed: 26967166
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
BMC Genomics. 2020 May 7;21(1):346
pubmed: 32380953
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Science. 2001 Aug 10;293(5532):1098-102
pubmed: 11498581
Trends Parasitol. 2019 Jan;35(1):72-84
pubmed: 30529253
J Cell Biol. 1997 Feb 10;136(3):501-13
pubmed: 9024683
Parasite Immunol. 2012 Feb-Mar;34(2-3):130-50
pubmed: 21793855
Mol Cell Biol. 1993 Mar;13(3):1583-9
pubmed: 8441399
J Mol Evol. 2017 Aug;85(1-2):37-45
pubmed: 28744787
Parasit Vectors. 2010 Dec 31;3:123
pubmed: 21194465
Genes (Basel). 2019 Mar 16;10(3):
pubmed: 30884847
Trends Genet. 2020 Apr;36(4):232-242
pubmed: 32155445
Folia Parasitol (Praha). 2018 Feb 23;65:
pubmed: 29528298
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
Mol Biol Evol. 2010 Mar;27(3):684-93
pubmed: 19942614
J Biol Chem. 2006 Jan 13;281(2):733-43
pubmed: 16230357
Nat Methods. 2013 Jun;10(6):563-9
pubmed: 23644548
Nature. 2009 Jul 16;460(7253):352-8
pubmed: 19606141
J Parasitol. 1963 Apr;49:305-7
pubmed: 13964161
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Bioinformatics. 2010 Jul 15;26(14):1699-703
pubmed: 20513662
Mol Biol Evol. 2018 Mar 1;35(3):543-548
pubmed: 29220515
Mol Biochem Parasitol. 2017 Jul;215:2-10
pubmed: 27899279
Genome Biol. 2015 Sep 24;16:207
pubmed: 26403281
J Histochem Cytochem. 1998 Jun;46(6):771-7
pubmed: 9603790