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An Illumina approach to MHC typing of Atlantic salmon

  • Arvind Y. M. Sundaram
  • Åse Helen Garseth
  • Giuseppe Maccari
  • Unni GrimholtEmail author
Review
  • 68 Downloads
Part of the following topical collections:
  1. Nomenclature, databases and bioinformatics in Immunogenetics

Abstract

The IPD-MHC Database represents the official repository for non-human major histocompatibility complex (MHC) sequences, overseen and supported by the Comparative MHC Nomenclature Committee, providing access to curated MHC data and associated analysis tools. IPD-MHC gathers allelic MHC class I and class II sequences from classical and non-classical MHC loci from various non-human animals including pets, farmed and experimental model animals. So far, Atlantic salmon and rainbow trout are the only teleost fish species with MHC class I and class II sequences present. For the remaining teleost or ray-finned species, data on alleles originating from given classical locus is scarce hampering their inclusion in the database. However, a fast expansion of sequenced genomes opens for identification of classical loci where high-throughput sequencing (HTS) will enable typing of allelic variants in a variety of new teleost or ray-finned species. HTS also opens for large-scale studies of salmonid MHC diversity challenging the current database nomenclature and analysis tools. Here we establish an Illumina approach to identify allelic MHC diversity in Atlantic salmon, using animals from an endangered wild population, and alter the salmonid MHC nomenclature to accommodate the expected sequence expansions.

Keywords

MHC Illumina IPD-MHC database Nomenclature Salmonid Atlantic salmon 

Notes

Acknowledgements

We thank Randi Faller at the Norwegian Veterinary Institute for excellent technical assistance.

Author contribution

Study was conceptualised by UG, ÅHG and AYMS. AYMS along with UG designed the primers used in library preparation and analysed the sequence data. AYMS wrote the custom scripts with assistance from GM. Library preparation and optimisation were performed by UG. Results were further analysed and interpreted by UG with assistance from AS. Nomenclature was changed by GM and UG. All authors contributed to writing the manuscript.

Funding information

This study was funded by the strategic institute projects “BioDirect” and “Seq-Tech” at the Norwegian Veterinary Institute and the Norwegian Research Council project no. 274635. ÅHG is supported by funding from the Norwegian Environment Agency. GM is supported by funding from the UKRI-BBSRC award BB/M011488/1. Sequencing was performed at Norwegian Sequencing Centre, Ulevål, Oslo, Norway. 

Supplementary material

251_2019_1143_MOESM1_ESM.pdf (726 kb)
Supplementary file 1. New IPD-MHC Fish nomenclature (PDF 725 kb)
251_2019_1143_MOESM2_ESM.pdf (518 kb)
Supplementary file 2. Illumina Statistics (PDF 518 kb)
251_2019_1143_MOESM3_ESM.pdf (589 kb)
Supplementary file 3. MHC sequences (PDF 589 kb)
251_2019_1143_MOESM4_ESM.pdf (543 kb)
Supplementary file 4. UBA primer regions (PDF 543 kb)
251_2019_1143_MOESM5_ESM.pdf (1.3 mb)
Supplementary file 5. MHC sequence alignments (PDF 1303 kb)

References

  1. Aoyagi K, Dijkstra JM, Xia C, Denda I, Ototake M, Hashimoto K, Nakanishi T (2002) Classical MHC class I genes composed of highly divergent sequence lineages share a single locus in rainbow trout (Oncorhynchus mykiss). J Immunol 168:260–273.  https://doi.org/10.4049/jimmunol.168.1.260 CrossRefPubMedGoogle Scholar
  2. Bannai HP, Nonaka M (2013) Comprehensive analysis of medaka major histocompatibility complex (MHC) class II genes: implications for evolution in teleosts. Immunogenetics 65:883–895.  https://doi.org/10.1007/s00251-013-0731-8 CrossRefPubMedGoogle Scholar
  3. Barlaup BTE (2008) Now or never for the Vosso salmon- recommended actions based on population development and threat factors. Norwegian Environment Agency, https://www.miljodirektoratet.no/globalassets/dokumenter/publikasjoner/overvakingsrapporter/vossolaksen_rapport.pdf
  4. Bingulac-Popovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46:129–134.  https://doi.org/10.1007/s002510050251 CrossRefPubMedGoogle Scholar
  5. Carapito R, Radosavljevic M, Bahram S (2016) Next-generation sequencing of the HLA locus: methods and impacts on HLA typing, population genetics and disease association studies. Hum Immunol 77:1016–1023.  https://doi.org/10.1016/j.humimm.2016.04.002 CrossRefPubMedGoogle Scholar
  6. Christensen KA, Leong JS, Sakhrani D, Biagi CA, Minkley DR, Withler RE, Rondeau EB, Koop BF, Devlin RH (2018a) Chinook salmon (Oncorhynchus tshawytscha) genome and transcriptome. PLoS One 13:e0195461.  https://doi.org/10.1371/journal.pone.0195461 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Christensen KA, Rondeau EB, Minkley DR, Leong JS, Nugent CM, Danzmann RG, Ferguson MM, Stadnik A, Devlin RH, Muzzerall R, Edwards M, Davidson WS, Koop BF (2018b) The Arctic charr (Salvelinus alpinus) genome and transcriptome assembly. PLoS One 13:e0204076.  https://doi.org/10.1371/journal.pone.0204076 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Croisetiere S, Tarte PD, Bernatchez L, Belhumeur P (2008) Identification of MHC class IIbeta resistance/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis). Mol Immunol 45:3107–3116.  https://doi.org/10.1016/j.molimm.2008.03.007 CrossRefPubMedGoogle Scholar
  9. de Muinck EJ, Trosvik P, Gilfillan GD, Hov JR, Sundaram AYM (2017) A novel ultra high-throughput 16S rRNA gene amplicon sequencing library preparation method for the Illumina HiSeq platform. Microbiome 5:68.  https://doi.org/10.1186/s40168-017-0279-1 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dijkstra JM, Katagiri T, Hosomichi K, Yanagiya K, Inoko H, Ototake M, Aoki T, Hashimoto K, Shiina T (2007) A third broad lineage of major histocompatibility complex (MHC) class I in teleost fish; MHC class II linkage and processed genes. Immunogenetics 59:305–321.  https://doi.org/10.1007/s00251-007-0198-6 CrossRefPubMedGoogle Scholar
  11. Dijkstra JM, Grimholt U, Leong J, Koop BF, Hashimoto K (2013) Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol Biol 13:260.  https://doi.org/10.1186/1471-2148-13-260 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Duke JL, Lind C, Mackiewicz K, Ferriola D, Papazoglou A, Gasiewski A, Heron S, Huynh A, McLaughlin L, Rogers M, Slavich L, Walker R, Monos DS (2016) Determining performance characteristics of an NGS-based HLA typing method for clinical applications. HLA 87:141–152.  https://doi.org/10.1111/tan.12736 CrossRefPubMedGoogle Scholar
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797.  https://doi.org/10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Forseth T et al (2017) The major threats to Atlantic salmon in Norway. ICES J Mar Sci 74:1496–1513.  https://doi.org/10.1093/icesjms/fsx020 CrossRefGoogle Scholar
  15. Garseth AH, Ekrem T, Biering E (2013) Phylogenetic evidence of long distance dispersal and transmission of piscine reovirus (PRV) between farmed and wild Atlantic salmon. PLoS One 8:e82202.  https://doi.org/10.1371/journal.pone.0082202 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gjedrem T (2000) Genetic improvement of cold-water fish species. Aquac Res:25-33 doi: https://doi.org/10.1046/j.1365-2109.2000.00389.x CrossRefGoogle Scholar
  17. Gjedrem T, Gjøen HM, Gjerde B (1991) Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98:41–50.  https://doi.org/10.1016/0044-8486(91)90369-I CrossRefGoogle Scholar
  18. Glover K, Quintela M, Wennevik V, Besnier F, Sørvik AGE (2012) Three decades of farmed escapees in the wild: a spatio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS One 7(8):e43129.  https://doi.org/10.1371/journal.pone.0043129 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Grimholt U (2016) MHC and evolution in teleosts. Biology (Basel) 5 doi: https://doi.org/10.3390/biology5010006 CrossRefGoogle Scholar
  20. Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saebø S, Stet RJ (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55:210–219.  https://doi.org/10.1007/s00251-003-0567-8 CrossRefPubMedGoogle Scholar
  21. Grimholt U, Tsukamoto K, Azuma T, Leong J, Koop BF, Dijkstra JM (2015) A comprehensive analysis of teleost MHC class I sequences. BMC Evol Biol 15.  https://doi.org/10.1186/s12862-015-0309-1 CrossRefGoogle Scholar
  22. Grimholt U, Tsukamoto K, Hashimoto K, Dijkstra JM (2019) Discovery of a novel MHC class I lineage in teleost fish which shows unprecedented levels of ectodomain deterioration while possessing an impressive cytoplasmic tail motif. Cells 8 doi: https://doi.org/10.3390/cells8091056 CrossRefGoogle Scholar
  23. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162.  https://doi.org/10.1126/science.1063699 CrossRefPubMedGoogle Scholar
  24. Hjeltnes B, Bang Jensen B, Bornø G, Haukaas A, Walde CS (2019) Fish Health Report 2018. Norwegian Veterinary Institute, https://www.vetinst.no/rapporter-og-publikasjoner/rapporter/2019/fiskehelserapporten-2018
  25. Huerta-Cepas J, Serra F, Bork P (2016) ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 33:1635–1638.  https://doi.org/10.1093/molbev/msw046 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jonsson B, Jonsson N, Hansen LP (1991) Differences in life-history and migratory behavior between wild and hatchery-reared Atlantic salmon in nature. Aquaculture 98:69–78.  https://doi.org/10.1016/0044-8486(91)90372-e CrossRefGoogle Scholar
  27. Jonsson B, Jonsson N, Hansen LP (2003) Atlantic salmon straying from the River Imsa. J Fish Biol 62:641–657.  https://doi.org/10.1046/j.0022-1112.2003.00053.x CrossRefGoogle Scholar
  28. Karlsson S, Moen T, Lien S, Glover KA, Hindar K (2011) Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP-chip. Mol Ecol Resour 11(Suppl 1):247–253.  https://doi.org/10.1111/j.1755-0998.2010.02959.x CrossRefPubMedGoogle Scholar
  29. Karlsson S, Diserud OH, Moen T, Hindar K (2014) A standardized method for quantifying unidirectional genetic introgression. Ecol Evol 4:3256–3263.  https://doi.org/10.1002/ece3.1169 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kiryu I, Dijkstra JM, Sarder RI, Fujiwara A, Yoshiura Y, Ototake M (2005) New MHC class Ia domain lineages in rainbow trout (Oncorhynchus mykiss) which are shared with other fish species. Fish Shellfish Immun:243-254 doi: https://doi.org/10.1016/j.fsi.2004.07.007 CrossRefGoogle Scholar
  31. Kjoglum S, Larsen S, Bakke HG, Grimholt U (2008) The effect of specific MHC class I and class II combinations on resistance to furunculosis in Atlantic salmon (Salmo salar). Scand J Immunol 67:160–168.  https://doi.org/10.1111/j.1365-3083.2007.02052.x CrossRefPubMedGoogle Scholar
  32. Klein J (1986) The natural history of the major histocompatibility complex. John Wiley & Sons, New YorkGoogle Scholar
  33. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Langefors A, Lohm J, Grahn M, Andersen O, von Schantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. ProcBiolSci 268:479–485.  https://doi.org/10.1098/rspb.2000.1378 CrossRefGoogle Scholar
  35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan P, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lea E (1910) On the methods used in the Herring-investigations. Conseil permanent international pour l’exploration de la mer. vol 53. Publ. de Circonst. Copenhagen, DenmarkGoogle Scholar
  37. Lee RM (1920) A review of the methods of age and growth determination in fishes by means of scales. Fisheries Investigations London Series 2:1–32Google Scholar
  38. Lighten J, van Oosterhout C, Paterson IG, McMullan M, Bentzen P (2014) Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (Poecilia reticulata). Mol Ecol Resour 14:753–767.  https://doi.org/10.1111/1755-0998.12225 CrossRefPubMedGoogle Scholar
  39. Lohm J, Grahn M, Langefors A, Andersen O, Storset A, von Schantz T (2002) Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection. Proc Biol Sci 269:2029–2033.  https://doi.org/10.1098/rspb.2002.2114 CrossRefGoogle Scholar
  40. Lukacs MF et al (2007) Genomic organization of duplicated major histocompatibility complex class I regions in Atlantic salmon (Salmo salar). BMC Genomics 8:251.  https://doi.org/10.1186/1471-2164-8-251 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lund RA, Hansen LP (1991) Identification of wild and reared Atlantic salmon, Salmo salar L., using scale characters. Aquac Res 22(4):499-508CrossRefGoogle Scholar
  42. Maccari G, Robinson J, Ballingall K, Guethlein LA, Grimholt U, Kaufman J, Ho CS, de Groot NG, Flicek P, Bontrop RE, Hammond JA, Marsh SG (2017) IPD-MHC 2.0: an improved inter-species database for the study of the major histocompatibility complex. Nucleic Acids Res 45:D860–D864.  https://doi.org/10.1093/nar/gkw1050 CrossRefPubMedGoogle Scholar
  43. Maccari G, Robinson J, Bontrop RE, Otting N, de Groot NG, Ho CS, Ballingall KT, Marsh SGE, Hammond JA (2018) IPD-MHC: nomenclature requirements for the non-human major histocompatibility complex in the next-generation sequencing era. Immunogenetics 70:619–623.  https://doi.org/10.1007/s00251-018-1072-4 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963.  https://doi.org/10.1093/bioinformatics/btr507 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Marsh SG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, Erlich HA, Fernández-Viña M, Geraghty DE, Holdsworth R, Hurley CK, Lau M, Lee KW, Mach B, Maiers M, Mayr WR, Müller CR, Parham P, Petersdorf EW, Sasazuki T, Strominger JL, Svejgaard A, Terasaki PI, Tiercy JM, Trowsdale J (2010) Nomenclature for factors of the HLA system, 2010. Tissue Antigens 75:291–455.  https://doi.org/10.1111/j.1399-0039.2010.01466.x CrossRefPubMedPubMedCentralGoogle Scholar
  46. McConnell SC, Restaino AC, de Jong JL (2014) Multiple divergent haplotypes express completely distinct sets of class I MHC genes in zebrafish. Immunogenetics 66:199–213.  https://doi.org/10.1007/s00251-013-0749-y CrossRefPubMedGoogle Scholar
  47. Nonaka MI, Nonaka M (2010) Evolutionary analysis of two classical MHC class I loci of the medaka fish, Oryzias latipes: haplotype-specific genomic diversity, locus-specific polymorphisms, and interlocus homogenization. Immunogenetics 62:319–332.  https://doi.org/10.1007/s00251-010-0426-3 CrossRefPubMedGoogle Scholar
  48. NorwegianEnvironmentAgency (2014) Guidelines for stock enhancement for anadromous salmonids. vol M-nummer: 186 M.N.E.Agency. https://www.miljodirektoratet.no/globalassets/publikasjoner/M186/M186.pdf
  49. O’Farrell B, Benzie JA, McGinnity P, de Eyto E, Dillane E, Coughlan J, Cross TF (2013) Selection and phylogenetics of salmonid MHC class I: wild brown trout (Salmo trutta) differ from a non-native introduced strain. PLoS One 8:e63035.  https://doi.org/10.1371/journal.pone.0063035 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ono H, Klein D, Vincek V, Figueroa F, O’hUigin C, Tichy H, Klein J (1992) Major histocompatibility complex class II genes of zebrafish. Proc Natl Acad Sci U S A 89:11886–11890.  https://doi.org/10.1073/pnas.89.24.11886 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277.  https://doi.org/10.1016/s0168-9525(00)02024-2 CrossRefPubMedGoogle Scholar
  52. Savilammi T et al (2019) The chromosome-level genome assembly of European grayling reveals aspects of a unique genome evolution process within salmonids. G3 (Bethesda) 9:1283–1294.  https://doi.org/10.1534/g3.118.200919 CrossRefGoogle Scholar
  53. Shiina T, Dijkstra JM, Shimizu S, Watanabe A, Yanagiya K, Kiryu I, Fujiwara A, Nishida-Umehara C, Kaba Y, Hirono I, Yoshiura Y, Aoki T, Inoko H, Kulski JK, Ototake M (2005) Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56:878–893.  https://doi.org/10.1007/s00251-004-0755-1 CrossRefPubMedGoogle Scholar
  54. Shum BP, Rajalingam R, Magor KE, Azumi K, Carr WH, Dixon B, Stet RJ, Adkison MA, Hedrick RP, Parham P (1999) A divergent non-classical class I gene conserved in salmonids. Immunogenetics 49:479–490.  https://doi.org/10.1007/s002510050524 CrossRefPubMedGoogle Scholar
  55. Stabell O (1984) Homing and olfaction in salmonids: a critical review with special reference to the Atlantic salmon. Biol Rev 59:333–388CrossRefGoogle Scholar
  56. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrøm M, Gregers TF, Rounge TB, Paulsen J, Solbakken MH, Sharma A, Wetten OF, Lanzén A, Winer R, Knight J, Vogel JH, Aken B, Andersen O, Lagesen K, Tooming-Klunderud A, Edvardsen RB, Tina KG, Espelund M, Nepal C, Previti C, Karlsen BO, Moum T, Skage M, Berg PR, Gjøen T, Kuhl H, Thorsen J, Malde K, Reinhardt R, du L, Johansen SD, Searle S, Lien S, Nilsen F, Jonassen I, Omholt SW, Stenseth NC, Jakobsen KS (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210.  https://doi.org/10.1038/nature10342 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Stet RJ, Kruiswijk CP, Saeij JP, Wiegertjes GF (1998) Major histocompatibility genes in cyprinid fishes: theory and practice. Immunol Rev 166:301–316.  https://doi.org/10.1111/j.1600-065x.1998.tb01271.x CrossRefPubMedGoogle Scholar
  58. Stet RJ, de Vries B, Mudde K, Hermsen T, van Heerwaarden J, Shum BP, Grimholt U (2002) Unique haplotypes of co-segregating major histocompatibility class II A and class II B alleles in Atlantic salmon (Salmo salar) give rise to diverse class II genotypes. Immunogenetics 54:320–331.  https://doi.org/10.1007/s00251-002-0477-1 CrossRefPubMedGoogle Scholar
  59. Sultmann H, Meyer WE, Figueroa F, O’hUigin C, Klein J (1993) Zebrafish Mhc class II alpha chain-encoding genes: polymorphism, expression and function. Immunogenetics 38:408–420.  https://doi.org/10.1007/bf00184521 CrossRefPubMedGoogle Scholar
  60. Sultmann H, Mayer WE, Figueroa F, O’Huigin C, Klein J (1994) Organization of Mhc class II B genes in the zebrafish (Brachydanio rerio). Genomics 23:1–14.  https://doi.org/10.1006/geno.1994.1452 CrossRefPubMedGoogle Scholar
  61. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191.  https://doi.org/10.1093/bioinformatics/btp033 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699.  https://doi.org/10.1093/oxfordjournals.molbev.a003851 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Norwegian Veterinary InstituteOsloNorway
  2. 2.Department of Medical GeneticsOslo University HospitalOsloNorway
  3. 3.The Pirbright InstituteWokingUK
  4. 4.Anthony Nolan Research InstituteLondonUK

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