Sporobolomyces lactucae sp. nov. (Pucciniomycotina, Microbotryomycetes, Sporidiobolales): An Abundant Component of Romaine Lettuce Phylloplanes

. 2022 Mar 16 ; 8 (3) : . [epub] 20220316

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35330304

Grantová podpora
8072-42000-077-00D Agricultural Research Service
1010662 National Institute of Food and Agriculture

Shifts in food microbiomes may impact the establishment of human pathogens, such as virulent lineages of Escherichia coli, and thus are important to investigate. Foods that are often consumed raw, such as lettuce, are particularly susceptible to such outbreaks. We have previously found that an undescribed Sporobolomyces yeast is an abundant component of the mycobiome of commercial romaine lettuce (Lactuca sativa). Here, we formally describe this species as Sporobolomyces lactucae sp. nov. (Pucciniomycotina, Microbotryomycetes, and Sporidiobolales). We isolated multiple strains of this yeast from commercial romaine lettuce purchased from supermarkets in Illinois and Indiana; additional isolates were obtained from various plant phylloplanes in California. S. lactucae is a red-pigmented species that is similar in appearance to other members of the genus Sporobolomyces. However, it can be differentiated by its ability to assimilate glucuronate and D-glucosamine. Gene genealogical concordance supports S. lactucae as a new species. The phylogenetic reconstruction of a four-locus dataset, comprising the internal transcribed spacer and large ribosomal subunit D1/D2 domain of the ribosomal RNA gene, translation elongation factor 1-α, and cytochrome B, places S. lactucae as a sister to the S. roseus clade. Sporobolomyces lactucae is one of the most common fungi in the lettuce microbiome.

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Kluyver A.J., van Niel C.B. Über Spiegelbilder erzeugende Hefearten und die neue Hefegattung Sporobolomyces. Centbl. Bakt. ParasitKde. 1924;63:19.

Hamamoto M., Boekhout T., Nakase T. Sporobolomyces Kluyver & van Niel (1924) In: Kurtzman C.P., Fell J.W., Boekhout T., editors. The Yeasts: A Taxonomic Study. 5th ed. Volume 3. Elsevier; Burlington, MA, USA: 2011. pp. 1929–1990.

Wang Q.-M., Yurkov A.M., Göker M., Lumbsch H.T., Leavitt S.D., Groenewald M., Theelen B., Liu X.-Z., Boekhout T., Bai F.-Y. Phylogenetic classification of yeasts and related taxa within Pucciniomycotina. Stud. Mycol. 2015;81:149–189. doi: 10.1016/j.simyco.2015.12.002. PubMed DOI PMC

Nyland G. Studies on Some Unusual Heterobasidiomycetes from Washington State. Mycologia. 1949;41:686–701. doi: 10.1080/00275514.1949.12017812. DOI

Valério E., Gadanho M., Sampaio J.P. Reappraisal of the Sporobolomyces roseus species complex and description of Sporidiobolus metaroseus sp. nov. Int. J. Syst. Evol. Microbiol. 2008;58:736–741. doi: 10.1099/ijs.0.65580-0. PubMed DOI

Aime M.C., Matheny P.B., Henk D.A., Frieders E.M., Nilsson R.H., Piepenbring M., McLaughlin D.J., Szabo L.J., Begerow D., Sampaio J.P., et al. An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia. 2006;98:896–905. doi: 10.1080/15572536.2006.11832619. PubMed DOI

Wang Q.-M., Groenewald M., Takashima M., Theelen B., Han P.-J., Liu X.-Z., Boekhout T., Bai F.-Y. Phylogeny of yeasts and related filamentous fungi within Pucciniomycotina determined from multigene sequence analyses. Stud. Mycol. 2015;81:27–53. doi: 10.1016/j.simyco.2015.08.002. PubMed DOI PMC

Haelewaters D., Peterson R.A., Nevalainen H., Aime M.C. Inopinatum lactosum gen. & comb. nov., the first yeast-like fungus in Leotiomycetes. Int. J. Syst. Evol. Microbiol. 2021;71:004862. doi: 10.1099/ijsem.0.004862. PubMed DOI

Aime M.C., Castlebury L.A., Abbasi M., Begerow D., Berndt R., Kirschner R., Marvanová L., Ono Y., Padamsee M., Scholler M., et al. Competing sexual and asexual generic names in Pucciniomycotina and Ustilaginomycotina (Basidiomycota) and recommendations for use. IMA Fungus. 2018;9:75–89. doi: 10.5598/imafungus.2018.09.01.06. PubMed DOI PMC

Lorenzini M., Zapparoli G., Azzolini M., Carvalho C., Sampaio J.P. Sporobolomyces agrorum sp. nov. and Sporobolomyces sucorum sp. nov., two novel basidiomycetous yeast species isolated from grape and apple must in Italy. Int. J. Syst. Evol. Microbiol. 2019;69:3385–3391. doi: 10.1099/ijsem.0.003626. PubMed DOI

Li A.-H., Yuan F.-X., Groenewald M., Bensch K., Yurkov A.M., Li K., Han P.-J., Guo L.-D., Aime M.C., Sampaio J., et al. Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species. Stud. Mycol. 2020;96:17–140. doi: 10.1016/j.simyco.2020.01.002. PubMed DOI PMC

Urbina H., Aime M.C. A closer look at Sporidiobolales: Ubiquitous microbial community members of plant and food biospheres. Mycologia. 2018;110:79–92. doi: 10.1080/00275514.2018.1438020. PubMed DOI

Kurtzman C.P., Fell J.W., Boekhout T. The Yeasts, a Taxonomic Study. 5th ed. Volume 3 Elsevier; Burlington, MA, USA: 2011.

Davoli P., Mierau V., Weber R.W.S. Carotenoids and Fatty Acids in Red Yeasts Sporobolomyces roseus and Rhodotorula glutinis. Appl. Biochem. Microbiol. 2004;40:392–397. doi: 10.1023/B:ABIM.0000033917.57177.f2. PubMed DOI

Mannazzu I., Landolfo S., da Silva T.L., Buzzini P. Red yeasts and carotenoid production: Outlining a future for non-conventional yeasts of biotechnological interest. World J. Microbiol. Biotechnol. 2015;31:1665–1673. doi: 10.1007/s11274-015-1927-x. PubMed DOI

Wei C., Wu T., Ao H., Qian X., Wang Z., Sun J. Increased torulene production by the red yeast, Sporidiobolus pararoseus, using citrus juice. Prep. Biochem. Biotechnol. 2020;50:66–73. doi: 10.1080/10826068.2019.1663533. PubMed DOI

McCormack P.J., Wildman H.G., Jeffries P. Production of antibacterial compounds by phylloplane-inhabiting yeasts and yeastlike fungi. Appl. Environ. Microbiol. 1994;60:927–931. doi: 10.1128/aem.60.3.927-931.1994. PubMed DOI PMC

Bashi E., Fokkema N.J. Environmental factors limiting growth of Sporobolomyces roseus, an antagonist of Cochliobolus sativus, on wheat leaves. Trans. Br. Mycol. Soc. 1977;68:17–25. doi: 10.1016/S0007-1536(77)80146-0. DOI

Di Menna M.E. Yeasts from the leaves of pasture plants. N. Z. J. Agric. Res. 1959;2:394–405. doi: 10.1080/00288233.1959.10420328. DOI

Hamamoto M., Nakase T. Ballistosporous yeasts found on the surface of plant materials collected in New Zealand. 1. Six new species in the genus Sporobolomyces. Antonie Van Leeuwenhoek. 1995;67:151–171. doi: 10.1007/BF00871210. PubMed DOI

Wang Q.-M., Bai F.-Y. Four new yeast species of the genus Sporobolomyces from plant leaves. FEMS Yeast Res. 2004;4:579–586. doi: 10.1016/j.femsyr.2003.11.002. PubMed DOI

Barata A., Malfeito-Ferreira M., Loureiro V. The microbial ecology of wine grape berries. Int. J. Food Microbiol. 2012;153:243–259. doi: 10.1016/j.ijfoodmicro.2011.11.025. PubMed DOI

Hunter P.J., Pink D.A.C., Bending G.D. Cultivar-level genotype differences influence diversity and composition of lettuce (Lactuca sp.) phyllosphere fungal communities. Fungal Ecol. 2015;17:183–186. doi: 10.1016/j.funeco.2015.05.007. DOI

Haelewaters D., Urbina H., Brown S., Newerth-Henson S., Aime M. Isolation and Molecular Characterization of the Romaine Lettuce Phylloplane Mycobiome. J. Fungi. 2021;7:277. doi: 10.3390/jof7040277. PubMed DOI PMC

Andrews J.H., Harris R.F. The Ecology and Biogeography of Microorganisms on Plant Surfaces. Annu. Rev. Phytopathol. 2000;38:145–180. doi: 10.1146/annurev.phyto.38.1.145. PubMed DOI

Nguyen-The C., Carlin F. The microbiology of minimally processed fresh fruits and vegetables. Crit. Rev. Food Sci. Nutr. 1994;34:371–401. doi: 10.1080/10408399409527668. PubMed DOI

Albu S., Toome M., Aime M.C. Violaceomyces palustris gen. et sp. nov. and a new monotypic lineage, Violaceomycetales ord. nov. in Ustilaginomycetes. Mycologia. 2015;107:1193–1204. doi: 10.3852/14-260. PubMed DOI

Suh S.-O., Zhang N., Nguyen N., Gross S., Blackwell M. Lab Manual for Yeast Study. Louisiana State University; Baton Rouge, LA, USA: 2008.

Kurtzman C.P., Fell J.W., Boekhout T., Robert V. Methods for Isolation, Phenotypic Characterization, and Maintenance of Yeasts. In: Kurtzman C.P., Fell J.W., Boekhout T., editors. The Yeasts: A Taxonomic Study. 5th ed. Elsevier; Burlington, MA, USA: 2011. pp. 87–110.

Online Auction Color Chart Co. The Online Auction Color Chart: The New Language of Color for Buyers and Sellers. Online Auction Color Chart Co.; Palo Alto, CA, USA: 2004.

White T.J., Bruns T.D., Lee S.B., Taylor J.W. PCR Protocols: A Guide to Methods and Applications. Academic Press; San Diego, CA, USA: 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phy-logenetics; pp. 315–322.

Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993;2:113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x. PubMed DOI

Vilgalys R., Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 1990;172:4238–4246. doi: 10.1128/jb.172.8.4238-4246.1990. PubMed DOI PMC

Hopple J.S., Jr. Ph.D. Thesis. Duke University; Durham, NC, USA: 1994. Phylogenetic Investigations in the Genus Coprinus Based on Morphological and Molecular Characters.

Rehner S.A., Buckley E. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: Evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia. 2005;97:84–98. doi: 10.3852/mycologia.97.1.84. PubMed DOI

Biswas S.K., Yokoyama K., Nishimura K., Miyaji M. Molecular phylogenetics of the genus Rhodotorula and related basidiomycetous yeasts inferred from the mitochondrial cytochrome b gene. Int. J. Syst. Evol. Microbiol. 2001;51:1191–1199. doi: 10.1099/00207713-51-3-1191. PubMed DOI

Toome M., Roberson R.W., Aime M.C. Meredithblackwellia eburnean gen. et sp. nov., Kriegeriaceae fam. nov. and Kriegeriales ord. nov.—Toward resolving higher-level classification in Microbotryomycetes. Mycologia. 2013;105:486–495. doi: 10.3852/12-251. PubMed DOI

Wang Q.M., Theelen B., Groenewald M., Bai F.-Y., Boekhout T. Moniliellomycetes and Malasseziomycetes, two new classes in Ustilaginomycotina. Persoonia-Mol. Phylogeny Evol. Fungi. 2014;33:41–47. doi: 10.3767/003158514X682313. PubMed DOI PMC

Wang Q.-M., Bai F.-Y. Molecular phylogeny of basidiomycetous yeasts in the Cryptococcus luteoluslineage (Tremellales) based on nuclear rRNA and mitochondrial cytochromebgene sequence analyses: Proposal of Derxomyces gen. nov. and Hannaella gen. nov., and description of eight novel Derxomyces species. FEMS Yeast Res. 2008;8:799–814. doi: 10.1111/j.1567-1364.2008.00403.x. PubMed DOI

Johnson M., Zaretskaya I., Raytselis Y., Merezhuk Y., McGinnis S., Madden T.L. NCBI BLAST: A better web interface. Nucleic Acids Res. 2008;36:W5–W9. doi: 10.1093/nar/gkn201. PubMed DOI PMC

Tan Y.P., Bishop-Hurley S.L., Marney T.S., Shivas R.G. Nomenclatural novelties. [(accessed on 27 January 2022)];Index Fungorum. 2021 503:1–8. Available online: http://www.indexfungorum.org/Publications/Index%20Fungorum%20no.503.pdf.

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; Proceedings of the 2010 Gateway Computing Environments Workshop (GCE); New Orleans, LA, USA. 14 November 2010; Piscataway, NJ, USA: Institute of Electrical and Electronics Engineers; 2010. pp. 1–8. DOI

Capella-Gutiérrez S., Silla-Martínez J.M., Gabaldón T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–1973. doi: 10.1093/bioinformatics/btp348. PubMed DOI PMC

Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Schoch C.L., Robbertse B., Robert V., Vu D., Cardinali G., Irinyi L., Meyer W., Nilsson R.H., Hughes K., Miller A.N., et al. Finding needles in haystacks: Linking scientific names, reference specimens and molecular data for Fungi. Database. 2014;2014:bau061. doi: 10.1093/database/bau061. PubMed DOI PMC

Takashima M., Nakase T. Four new species of the genus Sporobolomyces isolated from leaves in Thailand. Mycoscience. 2000;41:357–369. doi: 10.1007/BF02463949. DOI

Bai F.Y. Reclassification of the Sporobolomyces roseus and Sporidiobolus pararoseus complexes, with the description of Sporobolomyces phaffii sp. nov. Int. J. Syst. Evol. Microbiol. 2002;52:2309–2314. doi: 10.1099/ijs.0.02297-0. PubMed DOI

Vu D., Groenewald M., Szöke S., Cardinali G., Eberhardt U., Stielow B., de Vries M., Verkleij G.J.M., Crous P.W., Boekhout T., et al. DNA barcoding analysis of more than 9000 yeast isolates contributes to quantitative thresholds for yeast species and genera delimitation. Stud. Mycol. 2016;85:91–105. doi: 10.1016/j.simyco.2016.11.007. PubMed DOI PMC

Fell J.W., Scorzetti G., Statzell-Tallman A., Pinel N., Yarrow D. Recognition of the basidiomycetous yeast Sporobolomyces ruberrimus sp. nov. as a distinct species based on molecular and morphological analyses. FEMS Yeast Res. 2002;1:265–270. doi: 10.1111/j.1567-1364.2002.tb00044.x. PubMed DOI

Satoh K., Makimura K. Sporobolomyces koalae sp. nov., a basidiomycetous yeast isolated from nasal smears of Queensland koalas kept in a Japanese zoological park. Int. J. Syst. Evol. Microbiol. 2008;58:2983–2986. doi: 10.1099/ijs.0.2008/000307-0. PubMed DOI

Libkind D., Gadanho M., Van Broock M., Sampaio J.P. Sporidiobolus longiusculus sp. nov. and Sporobolomyces patagonicus sp. nov., novel yeasts of the Sporidiobolales isolated from aquatic environments in Patagonia, Argentina. Int. J. Syst. Evol. Microbiol. 2005;55:503–509. doi: 10.1099/ijs.0.63322-0. PubMed DOI

Maria J.S. Sporobolomyces marcillae nov. spec., isolated from the air. Arch Mikrobiol. 1958;32:29–31. doi: 10.1007/BF00409194. PubMed DOI

Taylor J.W., Jacobson D.J., Kroken S., Kasuga T., Geiser D.M., Hibbett D.S., Fisher M. Phylogenetic Species Recognition and Species Concepts in Fungi. Fungal Genet. Biol. 2000;31:21–32. doi: 10.1006/fgbi.2000.1228. PubMed DOI

Maddison W.P., Maddison D.R. Mesquite: A Modular System for Evolutionary Analysis, Version 3.61. 2019. [(accessed on 27 January 2022)]. Available online: https://www.mesquiteproject.org.

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., Von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Nguyen L.-T., Schmidt H.A., Von Haeseler A., Minh B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Chernomor O., Von Haeseler A., Minh B.Q. Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices. Syst. Biol. 2016;65:997–1008. doi: 10.1093/sysbio/syw037. PubMed DOI PMC

Hoang D.T., Chernomor O., Von Haeseler A., Minh B.Q., Vinh L.S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC

USDA . Agricultural Statistics 2020. National Agricultural Statistics Service; Washington, DC, USA: [(accessed on 13 April 2021)]. Available online: https://usda.library.cornell.edu/concern/publications/j3860694x?locale=en.

FDA . Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables. US Department of Health and Human Services; Washington, DC, USA: 1998.

Moulas C., Petsoulas C., Rousidou K., Perruchon C., Karas P., Karpouzas D.G. Effects of Systemic Pesticides Imidacloprid and Metalaxyl on the Phyllosphere of Pepper Plants. BioMed Res. Int. 2013;2013:969750. doi: 10.1155/2013/969750. PubMed DOI PMC

Martos F., Munoz F., Pailler T., Kottke I., Gonneau C., Selosse M.-A. The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol. Ecol. 2012;21:5098–5109. doi: 10.1111/j.1365-294X.2012.05692.x. PubMed DOI

Setati M.E., Jacobson D., Andong U.-C., Bauer F.F. The Vineyard Yeast Microbiome, a Mixed Model Microbial Map. PLoS ONE. 2012;7:e52609. doi: 10.1371/journal.pone.0052609. PubMed DOI PMC

Bourret T.B., Grove G.G., VanDeMark G.J., Henick-Kling T., Glawe D.A. Diversity and molecular determination of wild yeasts in a central Washington State vineyard. N. Am. Fungi. 2013;8:1–32. doi: 10.2509/naf2013.008.015. DOI

Jroundi F., González-Muñoz M.T., Sterflinger K., Piñar G. Molecular Tools for Monitoring the Ecological Sustainability of a Stone Bio-Consolidation Treatment at the Royal Chapel, Granada. PLoS ONE. 2015;10:e0132465. doi: 10.1371/journal.pone.0132465. PubMed DOI PMC

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