Advertisement

Antonie van Leeuwenhoek

, Volume 111, Issue 10, pp 1935–1953 | Cite as

Metschnikowia mating genomics

  • Dong Kyung Lee
  • Tom Hsiang
  • Marc-André Lachance
Original Paper
  • 134 Downloads

Abstract

Genes involved in mating type determination and recognition were examined in Metschnikowia and related species, to gather insights on factors affecting mating compatibility patterns among haplontic, heterothallic yeast species of the genus. We confirmed the universality of the special mating locus organisation found in Clavispora lusitaniae across and exclusive to the family Metschnikowiaceae (i.e., Metschnikowia and Clavispora). Timing of the divergence between idiomorphs was confirmed to coincide with the origin of the larger (CUG-ser) clade comprising the Debaryomycetaceae and the Metschnikowiaceae, exclusive of Cephaloascus fragrans. The sequence of the a mating pheromone is highly conserved within the large-spored Metschnikowia species, including Metschnikowia orientalis and Metschnikowia hawaiiana, but not Metschnikowia drosophilae or Metschnikowia torresii, which have a pattern of their own, as do other clades in the genus. In contrast, variation in α pheromones shows a more continuous, although imperfect correlation with phylogenetic distance as well as with in vivo mating compatibility.

Keywords

Yeast Metschnikowia Metschnikowiaceae Mating type locus Mating pheromones 

Notes

Acknowledgements

Funding from the Natural Science and Engineering Research Council of Canada is gratefully acknowledged. Thanks are extended to K. Bensch for her assistance in obtaining the MycoBank numbers and to A. Spera for early contributions to exploration of the mating type locus.

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1084_MOESM1_ESM.pptx (537 kb)
Supplementary material 1 (PPTX 536 kb)
10482_2018_1084_MOESM2_ESM.docx (27 kb)
Supplementary material 2 (DOCX 27 kb)

References

  1. Adhikari H, Cullen PJ (2015) Role of phosphatidylinositol phosphate signaling in the regulation of the filamentous-growth mitogen-activated protein kinase pathway. Eukaryot Cell 14:427–440CrossRefGoogle Scholar
  2. Audhya A, Foti M, Emr SD (2000) Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth and organelle membrane dynamics. Mol Biol Cell 11:2673–2689CrossRefGoogle Scholar
  3. Beh CT, McMaster CR, Kozminski KG, Menon AK (2012) A detour for yeast oxysterol binding proteins. J Biol Chem 287:11481–11488CrossRefGoogle Scholar
  4. Bennett RJ, Turgeon BG (2016) Fungal sex: the ascomycota. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.FUNK-0005-2016 CrossRefPubMedGoogle Scholar
  5. Butler G, Rasmussen MD, Lin MF et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662CrossRefGoogle Scholar
  6. Cevheroglu O, Kumas G, Melinda G, Becker JM, Son CD (2017) The yeast Ste2p G protein-coupled receptor dimerizes on the cell plasma membrane. Biochim Biophys Acta 1859:698–711CrossRefGoogle Scholar
  7. Dignard D, El-Naggar AL, Logue ME, Butler G, Whiteway M (2007) Identification and characterization of MFA1, the gene encoding Candida albicans a-factor pheromone. Eukaryot Cell 6:487–494CrossRefGoogle Scholar
  8. Gastaldi S, Zamboni M, Bolasco G, Di Segni G, Tocchini-Valentini GP (2016) Analysis of random PCR-originated mutants of the yeast Ste2 and Ste3 receptors. Microbiologyopen 5:670–686CrossRefGoogle Scholar
  9. Gonçalves-Sá J, Murray A (2011) Asymmetry in sexual pheromones is not required for ascomycete mating. Curr Biol 21:1337–1346CrossRefGoogle Scholar
  10. Guzmán B, Lachance MA, Herrera CM (2013) Phylogenetic analysis of the angiosperm-floricolous insect-yeast association: have yeast and angiosperm lineages co-diversified? Mol Phlogenet Evol 68:61–175Google Scholar
  11. Hull CM, Johnson AD (1999) Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285:1271–1275CrossRefGoogle Scholar
  12. Jones SK Jr, Bennett RJ (2011) Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48:668–676CrossRefGoogle Scholar
  13. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  14. Kozakov D, Hall DR, Xia B, Porter KA, Padhorny D, Yueh C, Beglov D, Vajda S (2017) The ClusPro web server for protein-protein docking. Nat Protoc 12:255–278CrossRefGoogle Scholar
  15. Kurtzman CP (2003) Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora. FEMS Yeast Res 4:233–245CrossRefGoogle Scholar
  16. Kurtzman CP (2011) Discussion of teleomorphic and anamorphic ascomycetous yeasts and yeast-like taxa. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, vol 2. Elsevier, Amsterdam, pp 293–307CrossRefGoogle Scholar
  17. Kurtzman CP, Robnett CJ (2013) Relationships among genera of the Saccharomycotina (Ascomycota) from multigene phylogenetic analysis of type species. FEMS Yeast Res 13:23–33CrossRefGoogle Scholar
  18. Lachance MA (2011) Metschnikowia Kamienski (1899). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts, a taxonomic study, vol 2. Elsevier, Amsterdam, pp 575–620CrossRefGoogle Scholar
  19. Lachance MA (2012) In defense of yeast sexual life cycles: the forma asexualis, an informal proposal. Yeast Newsl 61:24–25Google Scholar
  20. Lachance MA (2016) Paraphyly and (yeast) classification. Int J Syst Evol Microbiol 66:4924–4929CrossRefGoogle Scholar
  21. Lachance MA, Bowles JM (2004) Metschnikowia similis sp. nov. and Metschnikowia colocasiae sp. nov., two ascomycetous yeasts isolated from Conotelus spp. (Coleoptera: Nitidulidae) in Costa Rica. Stud Mycol 50:69–76Google Scholar
  22. Lachance MA, Ewing CP, Bowles JM, Starmer WT (2005) Metschnikowia hamakuensis sp. nov., Metschnikowia kamakouana sp. nov. and Metschnikowia mauinuiana sp. nov., three endemic yeasts from Hawaiian nitidulid beetles. Int J Syst Evol Microbiol 55:1369–1377CrossRefGoogle Scholar
  23. Lachance MA, Collens JD, Peng XF, Wardlaw AM, Bishop L, Hou LY, Starmer WT (2016a) Spatial scale, genetic structure, and speciation of Hawaiian endemic yeasts. Pac Sci 70:389–408CrossRefGoogle Scholar
  24. Lachance MA, Hurtado E, Hsiang T (2016b) A stable phylogeny of the large-spored Metschnikowia clade. Yeast 33:261–275CrossRefGoogle Scholar
  25. Marinoni G (2003) Sexual cycle and speciation in the giant-spored Metschnikowia species. Dissertation, University of Western OntarioGoogle Scholar
  26. Marinoni G, Lachance MA (2004) Speciation in the large-spored Metschnikowia clade and establishment of a new species, Metschnikowia borealis comb. nov. FEMS Yeast Res 4:587–596CrossRefGoogle Scholar
  27. McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K et al (2012) International code of nomenclature for algae, fungi, and plants (Melbourne Code). Regnum Veg 154. ARG Gantner Verlag, KoenigsteinGoogle Scholar
  28. Merlini L, Dudin O, Martin SG (2013) Mate and fuse: how yeast cells do it. Open Biol 3:130008CrossRefGoogle Scholar
  29. Michaelis S, Barrowman J (2012) Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease. Microbiol Mol Biol Rev 76:626–651CrossRefGoogle Scholar
  30. Raicu V, Stoneman MR, Fung R, Melnichuk M, Jasnma DB, Pisterzi LF, Rath S, Fox M, Wells JW, Saldin DK (2009) Determination of supramolecular structure and spatial distribution of protein complexes in living cells. Nat Photonics 3:107–113CrossRefGoogle Scholar
  31. Reedy JL, Floyd AM, Heitman J (2009) Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Curr Biol 19:891–899CrossRefGoogle Scholar
  32. Riley R, Haridas S, Wolfe KH, Lopes MR, Hittinger CT, Göker M, Salamov AA, Wisecaver JH, Long TM, Calvey CH, Aerts AL, Barry KW, Choi C, Clum A, Coughlan AY, Deshpande S, Douglass AP, Hanson SJ, Klenk HP, LaButti KM, Lapidus A, Lindquist EA, Lipzen AM, Meier-Kolthoff JP, Ohm RA, Otillar RP, Pangilinan JL, Peng Y, Rokas A, Rosa CA, Scheuner C, Sibirny AA, Slot JC, Stielow JB, Sun H, Kurtzman CP, Blackwell M, Grigoriev IV, Jeffries TW (2016) Comparative genomics of biotechnologically important yeasts. Proc Natl Acad Sci USA 113:9882–9887CrossRefGoogle Scholar
  33. Robles LM, Millan-Pacheco C, Pastor N, Del Rio G (2017) Structure-function studies of the alpha pheromone receptor from yeast. Rev Esp Cienc Quim Biol 20:16–26Google Scholar
  34. Rogers DW, McConnel E, Greig D (2012) Molecular quantification of Saccharomyces cerevisiae α-pheromone secretion. FEMS Yeast Res 12:668–674CrossRefGoogle Scholar
  35. Rogers DW, Denton JA, McConnell E, Greig D (2015) Experimental evolution of species recognition. Curr Biol 25:1753–1758CrossRefGoogle Scholar
  36. Sengupta P, Cochran BH (1990) The PRE and PQ box are functionally distinct yeast pheromone response elements. Mol Cell Biol 10:6809–6812CrossRefGoogle Scholar
  37. Shen Y, Maupetit J, Derreumaux P, Tuffery P (2014) Improved PEP-FOLD approach for peptide and miniprotein structure prediction. J Chem Theor Comput 10:4745–4758CrossRefGoogle Scholar
  38. Sherwood RK, Scaduto CM, Torres SE, Bennett RJ (2014) Convergent evolution of a fused sexual cycle promotes the haploid lifestyle. Nature 506:387CrossRefGoogle Scholar
  39. Soll DR, Daniels KJ (2016) Plasticity of Candida albicans biofilms. Microbiol Mol Biol Rev 80:565–595CrossRefGoogle Scholar
  40. Srikantha T, Daniels KJ, Pujol C, Sahni N, Yi S, Soll DR (2012) Nonsex genes in the mating type locus of Candida albicans play roles in a/α biofilm formation, including impermeability and fluconazole resistance. PLoS Pathog 8:e1002476CrossRefGoogle Scholar
  41. Stoneman MR, Paprocki JD, Biener G, Yokoi K, Shevade A, Kuchin S, Raicu V (2017) Quaternary structure of the yeast pheromone receptor Ste2 in living cells. Biochim Biophys Acta 1859:1456–1464CrossRefGoogle Scholar
  42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  43. Uddin MS, Hauser M, Naider F, Becker JM (2016) The N-terminus of the yeast G protein-coupled receptor Ste2p plays critical roles in surface expression, signaling and negative regulation. Biochim Biophys Acta 1858:715–724CrossRefGoogle Scholar
  44. Umanah GKE, Huang L, Ding F, Arshava B, Farley AR, Link AJ, Naider F, Becker JM (2010) Identification of residue to residue contact between a peptide ligand and its G protein-coupled receptor using periodate-mediated dihydroxyphenylalanine cross-linking and mass spectrometry. J Biol Chem 285:39425–39436CrossRefGoogle Scholar
  45. Wolfe KH, Butler G (2017) Evolution of mating in the Saccharomycotina. Annu Rev Microbiol 71:197–214CrossRefGoogle Scholar
  46. Wolfe KH, Armisén D, Proux-Wera E, ÓhÉigeartaigh SS, Azam H, Gordon JL, Byme KP (2015) Clade- and species-specific features of genome evolution in the Saccharomycetaceae. FEMS Yeast Res 15:fov035CrossRefGoogle Scholar
  47. Wu CI (2001) The genic view of the process of speciation. J Evol Biol 14:851–865CrossRefGoogle Scholar
  48. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER suite: protein structure and function prediction. Nat Methods 12:7–8CrossRefGoogle Scholar
  49. Yi S, Sahni N, Daniels KJ, Lu KL, Srikantha T, Huang G, Garnaas AM, Soll DR (2011) Alternative mating type configurations (a/α versus a/a or α/α) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol 9:e1001117CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Dong Kyung Lee
    • 1
  • Tom Hsiang
    • 2
  • Marc-André Lachance
    • 1
  1. 1.Department of BiologyUniversity of Western OntarioLondonCanada
  2. 2.School of Environmental SciencesUniversity of GuelphGuelphCanada

Personalised recommendations