Proc Natl Acad Sci U S A 113(35): 9882-9887

PMC: PMC5024638

PMID: 27535936

Comparative genomics of biotechnologically important yeasts

Tanya Long+30 authors

Supplementary Material

^{Department of Energy Joint Genome Institute, Walnut Creek, CA, 94598;}

^{University College Dublin Conway Institute, School of Medicine, University College Dublin, Dublin 4, Ireland;}

^{Laboratory of Genetics, Genetics/Biotechnology Center, University of Wisconsin–Madison, Madison, WI, 53706;}

^{Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil;}

^{Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin–Madison, Madison, WI, 53726;}

^{Deutsche Sammlung von Mikroorganismen und Zellkulturen German Collection of Microorganisms and Cell Cultures, Leibniz Institute, 38124 Braunschweig, Germany;}

^{Department of Biological Sciences, Vanderbilt University, Nashville, TN, 37235;}

^{Department of Bacteriology, University of Wisconsin–Madison, Madison, WI, 53706;}

^{US Department of Agriculture Forest Products Laboratory, Madison, WI, 53726;}

^{Xylome Corporation, Madison, WI, 53719;}

^{School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom;}

^{Department of Molecular Genetics and Biotechnology, Institute of Cell Biology, National Academy of Sciences of Ukraine, Lviv 79005, Ukraine;}

^{Department of Biotechnology and Microbiology, University of Rzeszow, Rzeszow 35-601, Poland;}

^{Department of Plant Pathology, Ohio State University, Columbus, OH, 43210;}

^{Centraalbureau voor Schimmelcultures Fungal Biodiversity Centre, Royal Netherlands Academy of Arts and Sciences, 3508 AD, Utrecht, The Netherlands;}

^{Agricultural Research Service, National Center for Agricultural Utilization Research, US Department of Agriculture, Peoria, IL, 61604;}

^{Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803;}

^{Department of Biological Sciences, University of South Carolina, Columbia, SC, 29208}

^{To whom correspondence may be addressed. Email:}vog.lbl@veirogirGVI or ude.csiw@irffejwt.

Edited by Chris R. Somerville, University of California, Berkeley, CA, and approved July 11, 2016 (received for review March 10, 2016)

Author contributions: A.L., C.P.K., M.B., I.V.G., and T.W.J. designed research; T.M.L., C.H.C., C.C., A.Y.C., S.D., S.J.H., H.-P.K., Y.P., A.A. Sibirny, J.B.S., C.P.K., and T.W.J. performed research; C.H.C. contributed new reagents/analytic tools; R.R., S.H., K.H.W., M.R.L., C.T.H., M.G., A.A. Salamov, J.H.W., A.L.A., K.W.B., A.C., A.P.D., K.M.L., A.L., E.A.L., A.M.L., J.P.M.-K., R.A.O., R.P.O., J.L.P., A.R., C.A.R., C.S., J.C.S., H.S., C.P.K., I.V.G., and T.W.J. analyzed data; R.R., S.H., K.H.W., C.T.H., M.G., C.P.K., M.B., I.V.G., and T.W.J. wrote the paper; and K.W.B., C.P.K., M.B., I.V.G., and T.W.J. coordinated the project.

^{Present address: Center for Algorithmic Biotechnology, St. Petersburg State University, St. Petersburg 199004, Russia.}

^{Present address: Microbiology, Department of Biology, Utrecht University, 3508, Utrecht, The Netherlands.}

Edited by Chris R. Somerville, University of California, Berkeley, CA, and approved July 11, 2016 (received for review March 10, 2016)

Significance

The highly diverse Ascomycete yeasts have enormous biotechnological potential. Collectively, these yeasts convert a broad range of substrates into useful compounds, such as ethanol, lipids, and vitamins, and can grow in extremes of temperature, salinity, and pH. We compared 29 yeast genomes with the goal of correlating genetics to useful traits. In one rare species, we discovered a genetic code that translates CUG codons to alanine rather than canonical leucine. Genome comparison enabled correlation of genes to useful metabolic properties and showed the synteny of the mating-type locus to be conserved over a billion years of evolution. Our study provides a roadmap for future biotechnological exploitations.

Keywords: genomics, bioenergy, biotechnological yeasts, genetic code, microbiology

Significance

Abstract

Ascomycete yeasts are metabolically diverse, with great potential for biotechnology. Here, we report the comparative genome analysis of 29 taxonomically and biotechnologically important yeasts, including 16 newly sequenced. We identify a genetic code change, CUG-Ala, in Pachysolen tannophilus in the clade sister to the known CUG-Ser clade. Our well-resolved yeast phylogeny shows that some traits, such as methylotrophy, are restricted to single clades, whereas others, such as l-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode many pathways of interest. Genomics can predict some biochemical traits precisely, but the genomic basis of others, such as xylose utilization, remains unresolved. Our data also provide insight into early evolution of ascomycetes. We document the loss of H3K9me2/3 heterochromatin, the origin of ascomycete mating-type switching, and panascomycete synteny at the MAT locus. These data and analyses will facilitate the engineering of efficient biosynthetic and degradative pathways and gateways for genomic manipulation.

Abstract

Yeasts are fungi that reproduce asexually by budding or fission and sexually without multicellular fruiting bodies (1, 2). Their unicellular, largely free-living lifestyle has evolved several times (3). Despite morphological similarities, yeasts constitute over 1,500 known species that inhabit many specialized environmental niches and associations, including virtually all varieties of fruits and flowers, plant surfaces and exudates, insects and other invertebrates, birds, mammals, and highly diverse soils (4). Biochemical and genomic studies of the model yeast Saccharomyces cerevisiae—essential for making bread, beer, and wine—have established much of our understanding of eukaryotic biology. However, in many ways, S. cerevisiae is an oddity among the yeasts, and many important biotechnological applications and highly divergent physiological capabilities of lesser-known yeast species have not been fully exploited (5). Various species can grow on methanol or n-alkanes as sole carbon and energy sources, overproduce vitamins and lipids, thrive under acidic conditions, and ferment unconventional carbon sources. Many features of yeasts make them ideal platforms for biotechnological processes. Their thick cell walls help them survive osmotic shock, and in contrast to bacteria, they are resistant to viruses. Their unicellular form is easy to cultivate, scale up, and harvest. The objective of this study was, therefore, to put yeasts with diverse biotechnological applications in a phylogenomic context and relate their physiologies to genomic features, so that their useful properties may be developed through genetic techniques. Backgrounds on 16 yeasts are given in SI Appendix.

Acknowledgments

We thank Marco A. Soares for computational advice. K.H.W. thanks G. Cagney, E. Dillon, and K. Wynne (University College Dublin Conway Institute Proteomics Core Facility) for help with MS. M.B. thanks Drs. S. O. Suh, H. Urbina, and N. H. Nguyen and numerous Louisiana State University undergraduates for their assistance. The work conducted by the US Department of Energy (DOE) Joint Genome Institute, a DOE Office of Science User Facility, is supported by Office of Science of the US DOE Contract DE-AC02-05CH11231. This material is based on work supported by National Science Foundation Grant DEB-1442148 (to C.T.H. and C.P.K.) and supported in part by DOE Great Lakes Bioenergy Research Center, DOE Office of Science Grant BER DE-FC02-07ER64494, and US Department of Agriculture (USDA) National Institute of Food and Agriculture Hatch Project 1003258. K.H.W. acknowledges European Research Council Grant 268893, Science Foundation Ireland Grant 13/IA/1910, and the Wellcome Trust. M.R.L. acknowledges a fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (process no. 7371/13-6). C.T.H. is a Pew Scholar in the Biomedical Sciences and an Alfred Toepfer Faculty Fellow, which are supported by the Pew Charitable Trusts and the Alexander von Humboldt Foundation, respectively. C.A.R. acknowledges support from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq. Funding from National Science Foundation Grants DEB-0072741 (to M.B.) and 0417180 (to M.B.) supported discovery and study of many new yeast strains that contributed to this study. T.W.J. acknowledges DOE Great Lakes Bioenergy Research Center DOE Office of Science Grant BER DE-FC02-07ER64494 and the USDA, Forest Products Laboratory for financial support.

Acknowledgments

Footnotes

Conflict of interest statement: C.H.C. and T.W.J. are employees of Xylome Corporation, which is developing nonconventional yeasts for biotechnological applications.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1603941113/-/DCSupplemental.

Footnotes

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Comparative genomics of biotechnologically important yeasts

Supplementary Material

Supplementary File

Supplementary File

Supplementary File

Supplementary File

Significance

Abstract

Acknowledgments

Footnotes

References