Transcriptome sequencing of the long-nosed bandicoot (Perameles nasuta) reveals conservation and innovation of immune genes in the marsupial order Peramelemorphia
Bandicoots are omnivorous marsupials of the order Peramelemorphia. Conservation concerns and their unique biological characteristics suggest peramelomorphs are worthy research subjects, but knowledge of their genetics and immunology has lagged behind that of other high-profile marsupials. Here, we characterise the transcriptome of the long-nose bandicoot (Perameles nasuta), the first high-throughput data set from any peramelomorph. We investigate the immune gene repertoire of the bandicoot, with a focus on key immune gene families, and compare to previously characterised marsupial and mammalian species. We find that the immune gene complement in bandicoot is often conserved with respect to other marsupials; however, the diversity of expressed transcripts in several key families, such as major histocompatibility complex, T cell receptor μ and natural killer cell receptors, appears greater in the bandicoot than other Australian marsupials, including devil and koala. This transcriptome is an important first step for future studies of bandicoots and the bilby, allowing for population level analysis and construction of bandicoot-specific immunological reagents and assays. Such studies will be critical to understanding the immunology and physiology of Peramelemorphia and to inform the conservation of these unique marsupials.
KeywordsMarsupial Metatherian Immunity Transcriptome
This study was partially funded by a University of the Sunshine Coast internal seed grant to HJW.
Compliance with ethical standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Conflict of interest
The authors declare that they have no conflict of interest.
- Belov K, Deakin JE, Papenfuss AT, Baker ML, Melman SD, Siddle HV, Gouin N, Goode DL, Sargeant TJ, Robinson MD, Wakefield MJ, Mahony S, Cross JG, Benos PV, Samollow PB, Speed TP, Graves JA, Miller RD (2006) Reconstructing an ancestral mammalian immune supercomplex from a marsupial major histocompatibility complex. PLoS Biol 4:e46CrossRefPubMedPubMedCentralGoogle Scholar
- Belov K, Sanderson CE, Deakin JE, Wong ES, Assange D, McColl KA, Gout A, de Bono B, Barrow AD, Speed TP, Trowsdale J (2007) Characterization of the opossum immune genome provides insights into the evolution of the mammalian immune system. Genome Res 17:982–991CrossRefPubMedPubMedCentralGoogle Scholar
- Bennett MD, Woolford L, O'Hara AJ, Nicholls PK, Warren K, Hobbs RP (2006) A new Eimeria species parasitic in western barred bandicoots, Perameles bougainville (Marsupialia: Peramelidae), in western Australia. J Parasitol 92(6):1292–1294. https://doi.org/10.1645/GE-892R.1 CrossRefPubMedGoogle Scholar
- Bennett MD, Woolford L, O'Hara AJ, Nicholls PK, Warren KS, Friend JA, Swan RA (2007) Klossiella quimrensis (Apicomplexa: Klossiellidae) causes renal coccidiosis in western barred bandicoots Perameles bougainville (Marsupialia: Peramelidae) in Western Australia. J Parasitol 93(1):89–92. https://doi.org/10.1645/GE-1023.1 CrossRefPubMedGoogle Scholar
- Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G (2004) GO::TermFinder—open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 20(18):3710–3715. https://doi.org/10.1093/bioinformatics/bth456 CrossRefPubMedPubMedCentralGoogle Scholar
- Delneste Y, Beauvillain C, Jeannin P (2007) Innate immunity: structure and function of TLRs. Med Sci 23:67–73Google Scholar
- DoEE (2017) EPBC Act List of Threatened Fauna. Department of Environment and Energy, CanberraGoogle Scholar
- Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512. https://doi.org/10.1038/nprot.2013.084 CrossRefPubMedGoogle Scholar
- Herberman RB (1986) Natural killer cells. Annu Rev Med 37(1):347–352. https://doi.org/10.1146/annurev.me.37.020186.002023 CrossRefPubMedGoogle Scholar
- Hobbs M, Pavasovic A, King A, Prentis P, Eldridge M, Chen Z, Colgan D, Polkinghorne A, Wilkins M, Flanagan C, Gillett A, Hanger J, Johnson R, Timms P (2014) A transcriptome resource for the koala (Phascolarctos cinereus): insights into koala retrovirus transcription and sequence diversity. BMC Genomics 15(1):786. https://doi.org/10.1186/1471-2164-15-786 CrossRefPubMedPubMedCentralGoogle Scholar
- Janeway CA, Travers P, Walport M, Shlomchik MJ (2001) Immunobiology, 5th edn. Garland Science, New York and LondonGoogle Scholar
- Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8(3):275-282Google Scholar
- Klein J, Hoøejsí V (1997) Immunology. Blackwell Science, OxfordGoogle Scholar
- Leary T, Wright D, Hamilton Z, Singadan R et al (2016) IUCN red list of threatened species. Version 2016. International Union for Conservation of Nature. http://www.iucnredlist.org/details/19711/0 Accessed 01 July 2017
- Mackerras IM, Mackerras MJ, Sandars DF (1953) Parasites of the bandicoot, Isoodon obesulus. Proc R Soc Queensl 63:61–63Google Scholar
- Marsh SGE, 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. Tiss Ant 75(4):291–455. https://doi.org/10.1111/j.1399-0039.2010.01466.x CrossRefGoogle Scholar
- Mitchell KJ, Pratt RC, Watson LN, Gibb GC, Llamas B, Kasper M, Edson J, Hopwood B, Mlae D, Armstrong KN, Meyer M, Hofreiter M, Austin J, Donnellan SC, Lee MSY, Phillips MJ, Cooper A (2014) Molecular phylogeny, biogeography and habitat preference evolution of marsupials. Mol Biol Evol 31(9):2322–2330. https://doi.org/10.1093/molbev/msu176 CrossRefPubMedGoogle Scholar
- Morris K, Prentis PJ, O’Meally D, Pavasovic A, Brown AT, Timms P, Belov K, Polkinghorne A (2014) The koala immunological toolkit: sequence identification and comparison of key markers of the koala (Phascolarctos cinereus) immune response. Aust J Zool 62(3):195–199. https://doi.org/10.1071/ZO13105 CrossRefGoogle Scholar
- Morris KM, Mathew M, Waugh C, Ujvari B, Timms P, Polkinghorne A, Belov K (2015b) Identification, characterisation and expression analysis of natural killer receptor genes in chlamydia pecorum infected koalas (Phascolarctos cinereus). BMC Genomics 16(1):796. https://doi.org/10.1186/s12864-015-2035-x CrossRefPubMedPubMedCentralGoogle Scholar
- Obendorf DL, Munday BL (1990) Toxoplasmosis in wild eastern barred bandicoots, Perameles gunnii. In: Seebeck JH (ed) Bandicoots and bilbies. Surrey Beatty and Sons, Sydney, pp 193–197Google Scholar
- Papenfuss AT, Baker ML, Feng ZP, Tachedjian M, Crameri G, Cowled C, Ng J, Janardhana V, Field HE, Wang LF (2012) The immune gene repertoire of an important viral reservoir, the Australian black flying fox. BMC Genomics 13(1):261. https://doi.org/10.1186/1471-2164-13-261 CrossRefPubMedPubMedCentralGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30(12):2725-2729Google Scholar
- van der Kraan LE, Wong ES, Lo N, Ujvari B, Belov K (2013) Identification of natural killer cell receptor genes in the genome of the marsupial Tasmanian devil (Sarcophilus harrisii). Immunogenetics 65(1):25–35. https://doi.org/10.1007/s00251-012-0643-z
- Woolford L, Rector A, Van Ranst M, Ducki A, Bennett MD, Nicholls PK, Warren KS, Swan RA, Wilcox GE, O'Hara AJ (2007) A novel virus detected in papillomas and carcinomas of the endangered western barred bandicoot (Perameles bougainville) exhibits genomic features of both the Papillomaviridae and Polyomaviridae. J Virol 81(24):13280–13290. https://doi.org/10.1128/JVI.01662-07 CrossRefPubMedPubMedCentralGoogle Scholar
- Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K, Foy E, Loo YM, Gale M, Akira S, Yonehara S (2005) Shared and unique functions of the DExD/H-Box Helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175(5):2851–2858. https://doi.org/10.4049/jimmunol.175.5.2851 CrossRefPubMedGoogle Scholar