, Volume 26, Issue 4, pp 345–352 | Cite as

Genomic insights into the carbohydrate catabolism of Cairneyella variabilis gen. nov. sp. nov., the first reports from a genome of an ericoid mycorrhizal fungus from the southern hemisphere

  • David J. Midgley
  • Carly P. Rosewarne
  • Paul Greenfield
  • Dongmei Li
  • Cassandra J. Vockler
  • Catherine J. Hitchcock
  • Nicole A. Sawyer
  • Robyn Brett
  • Jacqueline Edwards
  • John I. Pitt
  • Nai Tran-Dinh
Original Article


This paper describes a novel species of ericoid mycorrhizal fungus from Australia, Cairneyella variabilis, Midgley and Tran-Dinh, gen. nov. sp. nov. The genome of C. variabilis was sequenced and a draft genome assembled. The draft genome of C. variabilis is 52.4 Mbp in length, and to our knowledge, this is the first study to present a genome of an ericoid mycorrhizal fungus from the southern hemisphere. Using the SignalP and dbCAN bioinformatic pipelines, a study of the catabolic potential of C. variabilis was undertaken and showed genes for an array of degradative enzymes, most of which appear to be secreted from the hyphae, to access a suite of different carbon sources. Isolates of C. variabilis have been previously shown to utilise cellulose, carboxymethyl cellulose (CMC), cellobiose, xylan, pectin, starch and tannic acid for growth, and in the current study, putative enzymes for these processes were revealed. These enzymes likely play key roles in nutrient cycling and other edaphic processes in heathland environments. ITS phylogenetic analyses showed C. variabilis to be distinct from the fungi of the “Hymenoscyphus ericae aggregate”.


Fungi Ericaceae Helotiales 



We thank Mr Mark Wilson for accessioning cultures into the FRR culture collection, and Dr. Mark Bradbury and Ms. Brodie Sutcliffe for their insightful comments on the text.

Supplementary material

572_2016_683_MOESM1_ESM.docx (13 kb)
Table S1 (DOCX 13 kb)


  1. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552. doi: 10.1080/10635150600755453 CrossRefPubMedGoogle Scholar
  2. Atlas of Living Australia (2013)
  3. Baral H-O, Krieglsteiner L (2006) Hymenoscyphus subcarneus, a little known bryicolous discomycete found in the Białowieża National Park. Acta Mycol 41:11–20CrossRefGoogle Scholar
  4. Bending GD, Read DJ (1996a) Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1603–1612CrossRefGoogle Scholar
  5. Bending GD, Read J (1996b) Effects of the soluble polyphenol tannic on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem 28:1595–1602CrossRefGoogle Scholar
  6. Bougoure DS, Cairney JWG (2005a) Assemblages of ericoid mycorrhizal and other root-associated fungi from Epacris pulchella (Ericaceae) as determined by culturing and direct DNA extraction from roots. Environ Microbiol 7:819–827. doi: 10.1111/j.1462-2920.2005.00755.x CrossRefPubMedGoogle Scholar
  7. Bougoure DS, Cairney JWG (2005b) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ Microbiol 7:1743–1754. doi: 10.1111/j.1462-2920.2005.00919.x CrossRefPubMedGoogle Scholar
  8. Burke RM, Cairney JWG (1997a) Carbohydrolase production by the ericoid mycorrhizal fungus Hymenoscyphus ericae under solid-state fermentation conditions. Mycol Res 101:1135–1139CrossRefGoogle Scholar
  9. Burke RM, Cairney JWG (1997b) Purification and characterization of a ß-l,4-endoxylanase from the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol 135:345–352CrossRefGoogle Scholar
  10. Cairney JWG, Ashford AE (2002) Biology of mycorrhizal associations of epacrids (Ericaceae). New Phytol 154:305–326CrossRefGoogle Scholar
  11. Cairney J, Meharg A (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740. doi: 10.1046/j.1365-2389.2003.00555.x CrossRefGoogle Scholar
  12. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334 CrossRefPubMedGoogle Scholar
  13. Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinf 7:439. doi: 10.1186/1471-2105-7-439 CrossRefGoogle Scholar
  14. Curlevski NJ A, Chambers SM, Anderson IC, Cairney JWG (2009) Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiol Ecol 67:411–420. doi: 10.1111/j.1574-6941.2008.00637.x CrossRefPubMedGoogle Scholar
  15. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469. doi: 10.1093/nar/gkn180 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res 32:1792–1797. doi: 10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gilbert HJ (2010) The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol 153:444–455. doi: 10.1104/pp.110.156646 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Greenfield P, Duesing K, Papanicolaou A, Bauer DC (2014) Blue: correcting sequencing errors using consensus and context. Bioinformatics. 1–8. doi: 10.1093/bioinformatics/btu368
  19. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi: 10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  20. Halvorson JJ, Gollany HT, Kennedy AC, Hagerman AE, Gonzalez JM, Wuest SB (2012) Sorption of tannin and related phenolic compounds and effects on extraction of soluble-n in soil amended with several carbon sources. Agriculture 2:52–72. doi: 10.3390/agriculture2010052 CrossRefGoogle Scholar
  21. Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27. doi: 10.3114/sim.53.1.1 CrossRefGoogle Scholar
  22. Hoff KJ, Stanke M (2013) WebAUGUSTUS—a web service for training AUGUSTUS and predicting genes in eukaryotes. Nucleic Acids Res 41:W123–W128. doi: 10.1093/nar/gkt418 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kerley SJ, Read DJ (1998) The biology of mycorrhiza in the Ericaceae XX. Plant and mycorrhizal necromass as nitrogenous Hymenoscyphus ericae and its host. New Phytol 139:353–360CrossRefGoogle Scholar
  24. Kernan MJ, Finocchio AF (1983) A new discomycete associated with the roots of Monotropa uniflora (Ericaceae). Mycologia 75:916–920CrossRefGoogle Scholar
  25. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja H-R, LaButti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R et al (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415. doi: 10.1038/ng.3223 CrossRefPubMedGoogle Scholar
  26. Liu G, Chambers S, Cairney J (1998) Molecular diversity of ericoid mycorrhizal endophytes isolated from Woollsia pungens. New Phytol 140:145–153CrossRefGoogle Scholar
  27. Marx DH, Bryan WC (1975) Growth and ectomycorrhizal development of loblolly pine seedlings in fumigated soil infested with the fungal symbiont Pisolithus tinctorius. For Sci 21:245–254CrossRefGoogle Scholar
  28. Mclean CB, Anthony J, Collins RA, Steinke E, Lawrie A (1998) First synthesis of ericoid mycorrhizas in the Epacridaceae under axenic conditions. New Phytol 139:589–593CrossRefGoogle Scholar
  29. McLean C, Cunnington J, Lawrie A (1999) Molecular diversity within and between ericoid endophytes from the Ericaceae and Epacridaceae. New Phytol 144:351–358CrossRefGoogle Scholar
  30. Midgley DJ, Chambers SM, Cairney JWG (2002) Spatial distribution of fungal endophyte genotypes in a Woollsia pungens (Ericaceae) root system. Aust J Bot 50:559–565CrossRefGoogle Scholar
  31. Midgley DJ, Chambers SM, Cairney JWG (2004a) Distribution of ericoid mycorrhizal endophytes and root-associated fungi in neighbouring Ericaceae plants in the field. Plant Soil 259:137–151. doi: 10.1023/B:PLSO.0000020947.13655.9f CrossRefGoogle Scholar
  32. Midgley DJ, Chambers SM, Cairney JWG (2004b) Inorganic and organic substrates as sources of nitrogen and phosphorus for multiple genotypes of two ericoid mycorrhizal fungal taxa from Woollsia pungens and Leucopogon parviflorus (Ericaceae). Aust J Bot 52:63–71CrossRefGoogle Scholar
  33. Midgley DJ, Chambers SM, Cairney JWG (2004c) Utilisation of carbon substrates by multiple genotypes of ericoid mycorrhizal fungal endophytes from eastern Australian Ericaceae. Mycorrhiza 14:245–251. doi: 10.1007/s00572-003-0262-5 CrossRefPubMedGoogle Scholar
  34. Midgley DJ, Jordan LA, Saleeba JA, McGee PA (2006) Utilisation of carbon substrates by orchid and ericoid mycorrhizal fungi from Australian dry sclerophyll forests. Mycorrhiza 16:175–182. doi: 10.1007/s00572-005-0029-2 CrossRefPubMedGoogle Scholar
  35. Palmer J, Horton B, Allaway W, Ashford A (2007) Growth stimulation of Woollsia pungens by a natural ericoid mycorrhizal fungal endophyte. Australas Mycol 26:1–8Google Scholar
  36. Peretto R, Bettini V, Bonfante P (1993) Evidence of two polygalacturonases produced by a mycorrhizal ericoid fungus during its saprophytic growth. FEMS Microbiol Lett 114:85–91. doi: 10.1111/j.1574-6968.1993.tb06555.x CrossRefGoogle Scholar
  37. Perotto S, Peretto R, Faccio A, Schubert A, Bonfante P, Varma A (1995) Ericoid mycorrhizal fungi: cellular and molecular bases of their interactions with the host plant. Can J Bot 73:557–568. doi: 10.1139/b95-296 CrossRefGoogle Scholar
  38. Perotto S, Coisson JD, Perugini I, Cometti V, Bonfante P (1997) Production of pectin-degrading enzymes by ericoid mycorrhizal fungi. New Phytol 135:151–162CrossRefGoogle Scholar
  39. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. doi: 10.1038/nmeth.1701 CrossRefPubMedGoogle Scholar
  40. Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, Dordrecht, 519 pCrossRefGoogle Scholar
  41. Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374CrossRefGoogle Scholar
  42. Rice AV, Currah RS (2006) Oidiodendron maius: saprobe in Sphagnum peat, mutualist in ericaceous roots? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer Berlin / Heidelberg, Berlin, pp 227–246CrossRefGoogle Scholar
  43. Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata—the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563CrossRefGoogle Scholar
  44. Vrålstad T, Schumacher T, Taylor AFS (2002) Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–152. doi: 10.1046/j.0028-646X.2001.00290.x CrossRefGoogle Scholar
  45. Williams AF, Chambers SM, Davies PW, Mclean CB, Cairney JWG (2004) Molecular investigation of sterile root-associated fungi from Epacris microphylla R. Br. (Ericaceae) and other epacrids at alpine, subalpine and coastal heathland sites. Australas Mycol 23:94–104Google Scholar
  46. Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451. doi: 10.1093/nar/gks479 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • David J. Midgley
    • 1
  • Carly P. Rosewarne
    • 1
  • Paul Greenfield
    • 1
  • Dongmei Li
    • 2
  • Cassandra J. Vockler
    • 1
  • Catherine J. Hitchcock
    • 3
  • Nicole A. Sawyer
    • 4
  • Robyn Brett
    • 5
  • Jacqueline Edwards
    • 5
  • John I. Pitt
    • 1
  • Nai Tran-Dinh
    • 1
  1. 1.CSIROSydneyAustralia
  2. 2.Plant Health and Environment LaboratoryMinistry for Primary Industries, Manatū Ahu MatuaAucklandNew Zealand
  3. 3.NSW Forensic and Analytical Science ServiceLidcombeAustralia
  4. 4.Douglass Hanly Moir Pathology, Molecular GeneticsNorth RydeAustralia
  5. 5.Biosciences Research, Department of Economic Development, Jobs, Transport and Resources, AgriBioLa Trobe UniversityBundooraAustralia

Personalised recommendations