1887

Abstract

Wild flowers, and in particular, nectar of flowers, have been shown to be a rich reservoir of yeast biodiversity. In a taxonomic study of yeasts recovered from floral nectar in Morocco, nine strains were found to represent a novel species. Morphological and physiological characteristics and sequence analyses of the D1/D2 region of the large subunit rRNA gene as well as the internal transcribed spacer region showed that the novel species belonged to the genus . The name f.a., sp. nov. (EBDCdVMor24-1=CBS 15053=NRRL Y-63972) is proposed to accommodate this new species. was isolated from floral nectar of , and . The ascosporic state of the novel species was not found. was phylogenetically distinct from any currently recognized species and forms a well-supported subclade (bootstrap value 81 %) containing species associated with flowers and flower-visiting insects, including , and . The close genealogical relationship of with the clade is also consistent with the striking similarity of their ‘aeroplane’ cells morphologies and the lack of utilization of the α-glucoside trehalose. The ecology of these novel species and its probable endemicity are discussed.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.002784
2018-06-01
2019-12-12
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/68/6/2028.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.002784&mimeType=html&fmt=ahah

References

  1. Brysch-Herzberg M. Ecology of yeasts in plant-bumblebee mutualism in Central Europe. FEMS Microbiol Ecol 2004;50:87–100 [CrossRef][PubMed]
    [Google Scholar]
  2. Lachance MA. Yeast biodiversity: How many and how much?. In Rosa CA, Peter G. (editors) The Yeast Handbook: Biodiversity and Ecophysiology of Yeasts Berlin, Germany: Springer–Verlag; 2006; pp.1–9
    [Google Scholar]
  3. Pozo MI, Herrera CM, Bazaga P. Species richness of yeast communities in floral nectar of southern Spanish plants. Microb Ecol 2011;61:82–91 [CrossRef][PubMed]
    [Google Scholar]
  4. Canto A, Herrera CM, Rodriguez R. Nectar-living yeasts of a tropical host plant community: diversity and effects on community-wide floral nectar traits. PeerJ 2017;5:e3517 [CrossRef][PubMed]
    [Google Scholar]
  5. Lachance MA, Rosa CA, Starmer WT, Schlag-Edler B, Barker JS et al. Wickerhamiella australiensis, Wickerhamiella cacticola, Wickerhamiella occidentalis, Candida drosophilae and Candida lipophila, five new related yeast species from flowers and associated insects. Int J Syst Bacteriol 1998;48:1431–1443 [CrossRef][PubMed]
    [Google Scholar]
  6. Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JS et al. Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 2001;1:1–8 [CrossRef][PubMed]
    [Google Scholar]
  7. Lachance MA. Yeasts South–East England, UK: John Wiley & Sons; 2011;[Crossref]
    [Google Scholar]
  8. Lachance MA, Kurtzman CP. Wickerhamiella van der Walt (1973). In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts: A Taxonomic Study, 5th ed.vol. 2 San Diego, CA: Elsevier; 2011; pp.891–897[Crossref]
    [Google Scholar]
  9. de Vega C, Guzmán B, Lachance MA, Steenhuisen SL, Johnson SD et al. Metschnikowia proteae sp. nov., a nectarivorous insect-associated yeast species from Africa. Int J Syst Evol Microbiol 2012;62:2538–2545 [CrossRef][PubMed]
    [Google Scholar]
  10. de Vega C, Herrera CM. Microorganisms transported by ants induce changes in floral nectar composition of an ant-pollinated plant. Am J Bot 2013;100:792–800 [CrossRef][PubMed]
    [Google Scholar]
  11. de Vega C, Guzmán B, Steenhuisen SL, Johnson SD, Herrera CM et al. Metschnikowia drakensbergensis sp. nov. and Metschnikowia caudata sp. nov., endemic yeasts associated with Protea flowers in South Africa. Int J Syst Evol Microbiol 2014;64:3724–3732 [CrossRef][PubMed]
    [Google Scholar]
  12. de Oliveira Santos AR, Perri AM, Andrietta MG, Rosa CA, Lachance MA. The expanding large-spored Metschnikowia clade: Metschnikowia matae sp. nov., a yeast species with two varieties from the Brazilian Atlantic forest. Antonie van Leeuwenhoek 2015;108:753–763 [CrossRef][PubMed]
    [Google Scholar]
  13. Alimadadi N, Soudi MR, Wang SA, Wang QM, Talebpour Z et al. Starmerella orientalis f.a., sp. nov., an ascomycetous yeast species isolated from flowers. Int J Syst Evol Microbiol 2016;66:1476–1481 [CrossRef][PubMed]
    [Google Scholar]
  14. de Vega C, Albaladejo RG, Guzmán B, Steenhuisen SL, Johnson SD et al. Flowers as a reservoir of yeast diversity: description of Wickerhamiella nectarea f.a. sp. nov., and Wickerhamiella natalensis f.a. sp. nov. from South African flowers and pollinators, and transfer of related Candida species to the genus Wickerhamiella as new combinations. FEMS Yeast Res 2017;17:fox054 [CrossRef]
    [Google Scholar]
  15. Herrera CM, Canto A, Pozo MI, Bazaga P. Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc Biol Sci 2010;277:747–754 [CrossRef][PubMed]
    [Google Scholar]
  16. de Vega C, Herrera CM. Relationships among nectar-dwelling yeasts, flowers and ants: patterns and incidence on nectar traits. Oikos 2012;121:1878–1888 [CrossRef]
    [Google Scholar]
  17. Schaeffer RN, Irwin RE. Yeasts in nectar enhance male fitness in a montane perennial herb. Ecology 2014;95:1792–1798 [CrossRef][PubMed]
    [Google Scholar]
  18. Manson JS, Lachance MA, Thomson JD. Candida gelsemii sp. nov., a yeast of the Metschnikowiaceae clade isolated from nectar of the poisonous Carolina jessamine. Antonie van Leeuwenhoek 2007;92:37–42 [CrossRef][PubMed]
    [Google Scholar]
  19. Nicolson S, Thornburg RW. Nectar chemistry. In Pacini E, Nepi M, Nicolson S. (editors) Nectaries and Nectar Dordrecht, The Netherlands: Springer; 2007; pp.215–263[Crossref]
    [Google Scholar]
  20. Ruivo CC, Lachance MA, Rosa CA, Bacci M, Pagnocca FC. Candida heliconiae sp. nov., Candida picinguabensis sp. nov. and Candida saopaulonensis sp. nov., three ascomycetous yeasts from Heliconia velloziana (Heliconiaceae). Int J Syst Evol Microbiol 2006;56:1147–1151 [CrossRef][PubMed]
    [Google Scholar]
  21. Alvarez-Pérez S, Herrera CM. Composition, richness and nonrandom assembly of culturable bacterial-microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiol Ecol 2013;83:685–699 [CrossRef][PubMed]
    [Google Scholar]
  22. Golonka AM, Vilgalys R. Nectar inhabiting yeasts in virginian populations of Silene latifolia (Caryophyllaceae) and coflowering species. Am Midl Nat 2013;169:235–258 [CrossRef]
    [Google Scholar]
  23. Guzmán B, Lachance MA, Herrera CM. Phylogenetic analysis of the angiosperm-floricolous insect-yeast association: have yeast and angiosperm lineages co-diversified?. Mol Phylogenet Evol 2013;68:161–175 [CrossRef][PubMed]
    [Google Scholar]
  24. Mittelbach M, Yurkov AM, Nocentini D, Nepi M, Weigend M et al. Nectar sugars and bird visitation define a floral niche for basidiomycetous yeast on the Canary Islands. BMC Ecol 2015;15:2 [CrossRef][PubMed]
    [Google Scholar]
  25. Starmer WT, Lachance MA. Yeast ecology. In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts, 5th ed. Amsterdam, The Netherlands: Elsevier; 2011; pp.65–83[Crossref]
    [Google Scholar]
  26. Lachance MA. Metschnikowia: half tetrads, a regicide and the fountain of youth. Yeast 2016;33:563–574 [CrossRef][PubMed]
    [Google Scholar]
  27. Lachance MA, Hurtado E, Hsiang T. A stable phylogeny of the large-spored Metschnikowia clade. Yeast 2016;33:261–275 [CrossRef][PubMed]
    [Google Scholar]
  28. Stefanini I. Yeast-insect associations: it takes guts. Yeast 2018;35:315–330 [CrossRef][PubMed]
    [Google Scholar]
  29. Rosa CA, Lachance MA, Teixeira LC, Pimenta RS, Morais PB. Metschnikowia cerradonensis sp. nov., a yeast species isolated from ephemeral flowers and their nitidulid beetles in Brazil. Int J Syst Evol Microbiol 2007;57:161–165 [CrossRef][PubMed]
    [Google Scholar]
  30. Lachance MA, Ewing CP, Bowles JM, Starmer WT. 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 2005;55:1369–1377 [CrossRef][PubMed]
    [Google Scholar]
  31. Kurtzman CP, Fell JW, Boekhout T, Robert V. Methods for the isolation, phenotypic characterization and maintenance of yeasts. In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts: A Taxonomic Study, 5th ed.vol. 1 Amsterdam, The Netherlands: Elsevier; 2011; pp.87–110[Crossref]
    [Google Scholar]
  32. Kurtzman CP, Robnett CJ. Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 1998;73:331–371 [CrossRef][PubMed]
    [Google Scholar]
  33. Lachance MA, Bowles JM, Starmer WT, Barker JS. Kodamaea kakaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 1999;45:172–177 [CrossRef][PubMed]
    [Google Scholar]
  34. Baleiras Couto MM, Reizinho RG, Duarte FL. Partial 26S rDNA restriction analysis as a tool to characterise non-Saccharomyces yeasts present during red wine fermentations. Int J Food Microbiol 2005;102:49–56 [CrossRef][PubMed]
    [Google Scholar]
  35. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Gelfand DH, Sninsky JJ, White JW. (editors) PCR Protocols. A Guide to Methods And applications New York, NY: Academic press; 1990; pp.315–322
    [Google Scholar]
  36. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  37. Lachance MA. Metschnikowia. In Kurtzman CP, Fell JW, Boekhout T. (editors) The Yeasts: A Taxonomic Study, 5th ed.vol. 2 Amsterdam, The Netherlands: Elsevier; 2011; pp.575–620[Crossref]
    [Google Scholar]
  38. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406–425 [CrossRef][PubMed]
    [Google Scholar]
  39. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  40. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980;16:111–120 [CrossRef][PubMed]
    [Google Scholar]
  41. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783–791 [CrossRef][PubMed]
    [Google Scholar]
  42. Giménez-Jurado G. Metschnikowia gruessii sp. nov., the teleomorph of Nectaromyces reukaufii but not of Candida reukaufii. Syst Appl Microbiol 1992;15:432–438 [CrossRef]
    [Google Scholar]
  43. Giménez-Jurado G, Kurtzman CP, Starmer WT, Spencer-Martins I. Metschnikowia vanudenii sp. nov. and Metschnikowia lachancei sp. nov., from flowers and associated insects in North America. Int J Syst Evol Microbiol 2003;53:1665–1670 [CrossRef][PubMed]
    [Google Scholar]
  44. McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W et al. International Code of Nomenclature for Algae, Fungi and Plants (Melbourne Code) Koenigstein: Koelz Scientific Books; 2012
    [Google Scholar]
  45. Lachance MA. In defense of yeast sexual life cycles: the forma asexualis – an informal proposal. Yeast Newsletter 2012;61:24–25
    [Google Scholar]
  46. Duarte AW, Passarini MR, Delforno TP, Pellizzari FM, Cipro CV et al. Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environ Microbiol Rep 2016;8:874–885 [CrossRef][PubMed]
    [Google Scholar]
  47. Kurtzman CP, Droby S. Metschnikowia fructicola, a new ascosporic yeast with potential for biocontrol of postharvest fruit rots. Syst Appl Microbiol 2001;24:395–399 [CrossRef][PubMed]
    [Google Scholar]
  48. Suh SO, Gibson CM, Blackwell M. Metschnikowia chrysoperlae sp. nov., Candida picachoensis sp. nov. and Candida pimensis sp. nov., isolated from the green lacewings Chrysoperla comanche and Chrysoperla carnea (Neuroptera: Chrysopidae). Int J Syst Evol Microbiol 2004;54:1883–1890 [CrossRef][PubMed]
    [Google Scholar]
  49. Xue ML, Zhang LQ, Wang QM, Zhang JS, Bai FY. Metschnikowia sinensis sp. nov., Metschnikowia zizyphicola sp. nov. and Metschnikowia shanxiensis sp. nov., novel yeast species from jujube fruit. Int J Syst Evol Microbiol 2006;56:2245–2250 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.002784
Loading
/content/journal/ijsem/10.1099/ijsem.0.002784
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error