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Comparative Genomics of Biotechnologically Important Yeasts

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Comparative Genomics of Biotechnologically Important Yeasts Comparative genomics of biotechnologically important yeasts Robert Rileya, Sajeet Haridasa, Kenneth H. Wolfeb, Mariana R. Lopesc,d, Chris Todd Hittingerc,e, Markus Gökerf, Asaf A. Salamova, Jennifer H. Wisecaverg, Tanya M. Longh,i, Christopher H. Calveyj, Andrea L. Aertsa, Kerrie W. Barrya, Cindy Choia, Alicia Cluma, Aisling Y. Coughlanb, Shweta Deshpandea, Alexander P. Douglassb, Sara J. Hansonb, Hans-Peter Klenkf,k, Kurt M. LaButtia, Alla Lapidusa,1, Erika A. Lindquista, Anna M. Lipzena, Jan P. Meier-Kolthofff, Robin A. Ohma,2, Robert P. Otillara, Jasmyn L. Pangilinana, Yi Penga, Antonis Rokasg, Carlos A. Rosad, Carmen Scheunerf, Andriy A. Sibirnyl,m, Jason C. Slotn, J. Benjamin Stielowf,o, Hui Suna, Cletus P. Kurtzmanp, Meredith Blackwellq,r, Igor V. Grigorieva,3, and Thomas W. Jeffriesh,3 aDepartment of Energy Joint Genome Institute, Walnut Creek, CA 94598; bUniversity College Dublin Conway Institute, School of Medicine, University College Dublin, Dublin 4, Ireland; cLaboratory of Genetics, Genetics/Biotechnology Center, University of Wisconsin–Madison, Madison, WI 53706; dDepartamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil; eDepartment of Energy Great Lakes Bioenergy Research Center, University of Wisconsin–Madison, Madison, WI 53726; fDeutsche Sammlung von Mikroorganismen und Zellkulturen German Collection of Microorganisms and Cell Cultures, Leibniz Institute, 38124 Braunschweig, Germany; gDepartment of Biological Sciences, Vanderbilt University, Nashville, TN 37235; hDepartment of Bacteriology, University of Wisconsin–Madison, Madison, WI 53706; iUS Department of Agriculture Forest Products Laboratory, Madison, WI 53726; jXylome Corporation, Madison, WI 53719; kSchool of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom; lDepartment of Molecular Genetics and Biotechnology, Institute of Cell Biology, National Academy of Sciences of Ukraine, Lviv 79005, Ukraine; mDepartment of Biotechnology and Microbiology, University of Rzeszow, Rzeszow 35-601, Poland; nDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210; oCentraalbureau voor Schimmelcultures Fungal Biodiversity Centre, Royal Netherlands Academy of Arts and Sciences, 3508 AD, Utrecht, The Netherlands; pAgricultural Research Service, National Center for Agricultural Utilization Research, US Department of Agriculture, Peoria, IL 61604; qDepartment of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803; and rDepartment of Biological Sciences, University of South Carolina, Columbia, SC 29208 Edited by Chris R. Somerville, University of California, Berkeley, CA, and approved July 11, 2016 (received for review March 10, 2016) Ascomycete yeasts are metabolically diverse, with great potential for resistant to viruses. Their unicellular form is easy to cultivate, biotechnology. Here, we report the comparative genome analysis of scale up, and harvest. The objective of this study was, therefore, 29 taxonomically and biotechnologically important yeasts, including to put yeasts with diverse biotechnological applications in a 16 newly sequenced. We identify a genetic code change, CUG-Ala, in phylogenomic context and relate their physiologies to genomic 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 Significance as L-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode The highly diverse Ascomycete yeasts have enormous bio- many pathways of interest. Genomics can predict some biochemical technological potential. Collectively, these yeasts convert a broad traits precisely, but the genomic basis of others, such as xylose uti- range of substrates into useful compounds, such as ethanol, lization, remains unresolved. Our data also provide insight into early lipids, and vitamins, and can grow in extremes of temperature, evolution of ascomycetes. We document the loss of H3K9me2/3 het- salinity, and pH. We compared 29 yeast genomes with the goal erochromatin, the origin of ascomycete mating-type switching, and of correlating genetics to useful traits. In one rare species, we panascomycete synteny at the MAT locus. These data and analyses discovered a genetic code that translates CUG codons to alanine will facilitate the engineering of efficient biosynthetic and degrada- rather than canonical leucine. Genome comparison enabled cor- tive pathways and gateways for genomic manipulation. relation of genes to useful metabolic properties and showed the synteny of the mating-type locus to be conserved over a billion genomics | bioenergy | biotechnological yeasts | genetic code | years of evolution. Our study provides a roadmap for future microbiology biotechnological exploitations. Author contributions: A.L., C.P.K., M.B., I.V.G., and T.W.J. designed research; T.M.L., C.H.C., easts are fungi that reproduce asexually by budding or fission 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 Yand sexually without multicellular fruiting bodies (1, 2). research; C.H.C. contributed new reagents/analytic tools; R.R., S.H., K.H.W., M.R.L., C.T.H., Their unicellular, largely free-living lifestyle has evolved several 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., times (3). Despite morphological similarities, yeasts constitute over 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., 1,500 known species that inhabit many specialized environmental M.B., I.V.G., and T.W.J. coordinated the project. niches and associations, including virtually all varieties of fruits and Conflict of interest statement: C.H.C. and T.W.J. are employees of Xylome Corporation, flowers, plant surfaces and exudates, insects and other inverte- which is developing nonconventional yeasts for biotechnological applications. brates, birds, mammals, and highly diverse soils (4). Biochemical This article is a PNAS Direct Submission. — and genomic studies of the model yeast Saccharomyces cerevisiae Data deposition: The sequences reported in this paper have been deposited in the GenBank essential for making bread, beer, and wine—have established much database (accession nos. LWKO00000000, LYME00000000, LXTC00000000, LYBQ00000000, of our understanding of eukaryotic biology. However, in many ways, LYBR00000000, LWUO00000000, LSKT00000000, LTAD00000000, LXPE00000000, S. cerevisiae is an oddity among the yeasts, and many important AECK00000000, LSGR00000000, LXPB00000000, LZCH00000000, AEHA00000000, AEUO00000000,andLWUN00000000). biotechnological applications and highly divergent physiologi- 1Present address: Center for Algorithmic Biotechnology, St. Petersburg State University, cal capabilities of lesser-known yeast species have not been fully St. Petersburg 199004, Russia. exploited (5). Various species can grow on methanol or n-alkanes 2Present address: Microbiology, Department of Biology, Utrecht University, 3508, Utrecht, as sole carbon and energy sources, overproduce vitamins and The Netherlands. lipids, thrive under acidic conditions, and ferment unconventional 3To whom correspondence may be addressed. Email: [email protected] or twjeffri@ carbon sources. Many features of yeasts make them ideal platforms wisc.edu. for biotechnological processes. Their thick cell walls help them This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. survive osmotic shock, and in contrast to bacteria, they are 1073/pnas.1603941113/-/DCSupplemental. 9882–9887 | PNAS | August 30, 2016 | vol. 113 | no. 35 www.pnas.org/cgi/doi/10.1073/pnas.1603941113 Downloaded by guest on October 1, 2021 features, so that their useful properties may be developed through which may lower rates of leucylation (10), an Ser identity element genetic techniques. Backgrounds on 16 yeasts are given in in the variable loop, and a G discriminator base. Most CUG-Ser SI Appendix. clade species contained all three serylation features in their predicted tRNACAGs, indicating translation of CUG to Ser (SI Appendix, Results Fig. S7A). However, in the most basal taxa of this clade, not all of Organism Phylogeny. Genomes were sequenced and assembled as the features are present: M. bicuspidata lackstheSeridentityele- described in Materials and Methods (SI Appendix, Table S1). ment, and Babjeviella inositovora lacks the discriminator base. This Ser Using the predicted proteomes (SI Appendix, Fig. S1 and Table finding may reflect stepwise accumulation of tRNACAG features S2) of these plus an additional 13 ascomycete yeasts and 9 fungal in the evolution of alternative CUG translation. Species branching outgroups, we generated three phylogenomic data matrices: deeper in the tree do not show any of the three features. “full” (7,297 genes with four or more sequences), “MARE” To investigate CUG translation beyond CUG-Ser, we analyzed (1,559 genes from the full set filtered for informative quality), multiple alignments of 700 orthologous groups of proteins (SI and “core” (418 genes present in all organisms). The MARE-filtered Appendix). For each yeast, we identified its CUG-encoded positions supermatrix tree (6, 7) is shown (Fig. 1). The full
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