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Research Article | Applied and Environmental Science

Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica

Kyle R. Pomraning, Erin L. Bredeweg, Eduard J. Kerkhoven, Kerrie Barry, Sajeet Haridas, Hope Hundley, Kurt LaButti, Anna Lipzen, Mi Yan, Jon K. Magnuson, Blake A. Simmons, Igor V. Grigoriev, Jens Nielsen, Scott E. Baker
Aaron P. Mitchell, Editor
Kyle R. Pomraning
aChemical & Biological Process Development Group, Pacific Northwest National Laboratory, Richland, Washington, USA
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Erin L. Bredeweg
bEnvironmental Molecular Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Eduard J. Kerkhoven
cDepartment of Biology and Biological Engineering, Chalmers University of Technology, Göteborg, Sweden
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Kerrie Barry
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Sajeet Haridas
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Hope Hundley
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Kurt LaButti
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Anna Lipzen
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Mi Yan
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Jon K. Magnuson
aChemical & Biological Process Development Group, Pacific Northwest National Laboratory, Richland, Washington, USA
eJoint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Blake A. Simmons
eJoint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Igor V. Grigoriev
dDOE Joint Genome Institute, Walnut Creek, California, USA
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Jens Nielsen
cDepartment of Biology and Biological Engineering, Chalmers University of Technology, Göteborg, Sweden
fNovo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark
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  • ORCID record for Jens Nielsen
Scott E. Baker
bEnvironmental Molecular Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
eJoint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Aaron P. Mitchell
Carnegie Mellon University
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DOI: 10.1128/mSphere.00541-18
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  • FIG 1
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    FIG 1

    Isolation of Y. lipolytica mutants that lack filamentous growth. Approximately 500,000 colonies were screened for smooth morphology with no visible hyphae. From strain FKP355, five mutant strains were isolated that exhibit growth only as yeast (FKP500 to FKP504). The leu2-270 mutation was complemented in strain FKP503 to construct FKP514 and confirm the phenotype in a prototrophic strain. Confocal microscopy confirmed yeast phase growth and lack of elongated cells or pseudohyphae in auxotrophic and prototrophic smooth strains.

  • FIG 2
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    FIG 2

    smooth strains have mutations in repetitive regions of the genome. Coverage from high-throughput 150-bp paired-end Illumina sequencing from strain FKP355 (wild type) and five smooth mutant strains. Colored bases indicate polymorphic loci where reads align with SNPs at a rate greater than that expected from incorrect base calls. (A) Regions with no coverage are detected in smooth-17, smooth-33, and smooth-43 mutants at the end of scaffold 14 after alignment to the FKP355 reference genome. (B) Raw PacBio reads with homology to the single-copy region at the end of scaffold 14 (from 1 to 12 kb) were reassembled and analyzed for mutations not detected from the curated genome assembly. An example of an alternative assembly of the region detects a deletion in smooth-19 not seen in the reference assembly. (C) All five smooth mutants exhibit a different polymorphism rate than the wild-type rate at a transition point between a high-copy-number transposon-containing region and a moderate-copy-number region of short, tandem repeats.

  • FIG 3
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    FIG 3

    smooth strains have reduced repetitive DNA content. (A) Illumina 150-bp sequencing reads from strain FKP355 were systematically analyzed for the presence of all possible tandem duplications with a repeat unit length of 1 to 75 bp and quantified. Identification of phased repeat units with similar coverage was used to infer arrays of tandem repeats longer than a simple duplication. Colors indicate overlapping sequence motifs found in similar repeat sequences. (B) The fraction of 150-bp sequencing reads from the wild-type and smooth strains containing high-frequency tandem duplications of 10, 12, 28, and 40 bp in length. (C) The fraction of 150-bp sequencing reads from the wild-type and smooth strains that align to the FKP355 rDNA repeat.

  • FIG 4
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    FIG 4

    Effect of smooth-33 on expression of genes with specific DNA motifs near their transcription start site. The number of ACGCG and CCCCT motifs on each strand of DNA was determined (from 0 to 2 sites) between the transcription start site (labeled 0) and a given distance. The given distances shown are 200 to 2,000 bp in 200-bp intervals, both up- and downstream of the transcription start site. For each interval, the average difference in expression between FKP514 (smooth-33) and FKP391 (wild type) during chemostat cultivation is shown. Note that the presence of more CCCCT motifs close to the transcription start site is generally associated with decreased expression in the smooth-33 mutant, while the presence of more than one ACGCG site very near and 3′ of the transcription start site is associated with increased expression in the smooth-33 mutant.

  • FIG 5
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    FIG 5

    Ylmsn2p and the MBP complex regulate formation of hyphae. Ylmsn2p is predicted to interact with CCCCT promoter motifs, while the MBF complex (composed of Ylswi6p and Ylmbp1p) is predicted to interact with ACGCG motifs. Ylmsn2 was overexpressed in a smooth-33 background and deleted in the parental hyphal background used for mutagenesis (FKP355). Conversely, Ylswi6 and Ylmbp1 were independently deleted in a smooth-33 background and overexpressed in the parental background. Strains were cultured on YNB agar for 3 days at 28°C prior to examination of hyphae formation and imaging. Detailed genotypes are listed in Table 4.

  • FIG 6
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    FIG 6

    Mutants with a hyphal reversion phenotype in smooth-33. FKP514 (smooth-33) was mutagenized, and colonies exhibiting a transition to hyphal growth were isolated and sequenced. Mutant strains were plated on YNB agar, and isolated single colonies were imaged after 48 h at 28°C. Gene names shown are based on orthologs from S. cerevisiae and C. albicans. Mutations shown are the highest likelihood candidate identified after sequencing of each mutant.

  • FIG 7
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    FIG 7

    Histidine kinases in Y. lipolytica. (A) Phylogenetic reconstruction of selected histidine kinases from ascomycete fungi. Protein sequences from the histidine kinases of Y. lipolytica with similarity to Sln1p (FKP355 JGI protein ID 128287, 113409, 109080, 128802, and 126630) were used as bait to BlastP search the proteomes of Y. lipolytica, S. cerevisiae, C. albicans, Lipomyces starkeyi, Schizosaccharomyces pombe, Taphrina deformans, Ascobolus immerses, Monacrosporium haptotylum, Aspergillus nidulans, Stagnospora nodorum, Cladonia grayi, Botrytis cinerea, Neurospora crassa, and Xylona heveae. The BlastP hits were aligned using MUSCLE and analyzed by the maximum likelihood method with 200 bootstrap replicates to define the relationships between the Y. lipolytica genes and those from other species. (B) Protein domains from Ylnik1p were predicted by InterProScan (90). The kinase domain in Ylnik1p is predicted to be an S/T protein kinase. Note that all the mutations recovered occur in the HAMP domain. The sites of mutations are indicated by asterisks.

  • FIG 8
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    FIG 8

    Ylchk1 regulates formation of hyphae. Ylchk1 was deleted in wild-type and smooth-33 genetic backgrounds by replacement with leu2. Ylchk1 is not required for the transition to hyphal growth morphology, but deletion results in limited reversion to hyphal morphology in smooth-33.

Tables

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  • TABLE 1

    Enriched Gene Ontology terms in the smooth-33 mutanta

    GO termFDR
    Upregulated in the smooth-33 mutant
        DNA repair1.2E−05
        Regulation of transcription from RNA polymerase II promoter5.7E−04
        DNA recombination5.8E−03
        DNA replication initiation1.7E−02
        Cell cycle process3.3E−02
        Mismatched DNA binding3.3E−02
        Nucleosome assembly4.2E−02
    Downregulated in the smooth-33 mutant
        Small-GTPase-mediated signal transduction1.8E−03
        Steroid biosynthetic process4.0E−03
        GTP catabolic process4.9E−03
        Cytokinesis1.7E−02
        Nucleocytoplasmic transport2.7E−02
        Cellular lipid metabolic process3.5E−02
        Oxygen transport3.6E−02
        Membrane raft organization3.6E−02
        Chitin metabolic process4.2E−02
        Response to toxic substance4.2E−02
        Regulation of molecular function4.5E−02
        Fungal-type cell wall organization4.5E−02
        Microtubule-based movement4.9E−02
    • ↵a Analysis of the top 1,000 up- and downregulated genes identified biological process Gene Ontology (GO) terms specifically overrepresented in the smooth-33 mutant (false-discovery rate [FDR] of <0.01).

  • TABLE 2

    Expression of Y. lipolytica genes predicted to regulate the smooth phenotypea

    JGI protein IDS. cerevisiae homolog(s)Log2 fold changeP value
    5′-CCCCT-3′ binding
        143137msn2, msn4, com2−2.633.46E−04
        121652rei10.904.68E−03
        110816rph1, gis10.614.76E−02
        129649usv1, rgm10.201.82E−01
    5-ACGCG-3′ binding
        13938swi60.842.98E−03
        129847swi4, mbp10.846.32E−03
    • ↵a Fold change and P values represent the change in expression level between the smooth-33 and wild-type strains during chemostat cultivation.

  • TABLE 3

    High-confidence genes involved in yeast-to-hyphae transitiona

    JGI protein IDS. cerevisiae BlastPbNo. of strainsPredicted mutations recovered
    113409sln1 (nik1)5E342G, S441T, I536M, G584S, M598K
    140296cts14K2*, W134*, G285E, G284V/E837D
    127631ssk23G1190D, P555H, R526P
    109080sln1 (chk1)2T1290M, E1415K
    122144pbs222 x G371R
    124736hog11S335*
    128138hym11L103P
    131882lrg11G938C
    129277mih11Y476*
    • ↵a Genes with mutations in independent mutant strains as well as genes found in only one strain but with few or no other nonsynonymous mutations. Eight mutant strains contained many nonsynonymous mutations in unique gene hits and are not shown.

    • ↵b Genes in parentheses represent the best BlastP hit from C. albicans.

  • TABLE 4

    Y. lipolytica strains used in this study

    StrainGenotypeReference
    FKP355matA leu2-270 xpr2-332 axp-2 ku70::hph+55
    FKP391matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+55
    FKP500matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-17This work
    FKP501matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-18This work
    FKP502matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-19This work
    FKP503matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33This work
    FKP504matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-43This work
    FKP514matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33This work
    FEB248matA leu2-270 xpr2-332 axp-2 ku70::hph+ msn2::leu2+This work
    FKP552matA leu2-270 xpr2-332 axp-2 ku70::hph+ exp1p-:leu2+This work
    FEB237matA leu2-270 xpr2-332 axp-2 ku70::hph+ exp1p-mbp1:leu2+This work
    FEB240matA leu2-270 xpr2-332 axp-2 ku70::hph+ exp1p-swi6:leu2+This work
    FKP640matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33 exp1p-:leu2+This work
    FEB242matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33 exp1p-msn2:leu2+This work
    FEB249matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33 mbp1::leu2+This work
    FEB252matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33 swi6::leu2+This work
    FKP672matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 mih1Y476*This work
    FKP673matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 lrg1G938CThis work
    FKP675matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 nik1E342GThis work
    FKP677matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 nik1S441TThis work
    FKP681matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 nik1I536MThis work
    FKP682matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 nik1G584SThis work
    FKP683matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 nik1M598KThis work
    FKP684matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 pbs2G371RThis work
    FKP686matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 ssk2G1190DThis work
    FKP687matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 hog1R335*This work
    FKP689matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 chk1T1290MThis work
    FKP690matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 ssk2P555HThis work
    FKP691matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 ssk2R526PThis work
    FKP694matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 chk1E1415KThis work
    FKP695matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 pbsG371RThis work
    FKP730matA leu2-270::leu2+ xpr2-332 axp-2 ku70::hph+ smooth-33 hym1L103PThis work
    FEB492matA leu2-270 xpr2-332 axp-2 ku70::hph+ chk1::leu2+This work
    FEB494matA leu2-270 xpr2-332 axp-2 ku70::hph+ smooth-33 chk1::leu2+This work
  • TABLE 5

    Primers used in this study

    PrimerSequence (5→3′)
    OKP443ACCCGTTGCTATCTCCACAC
    OKP444GTGCAGTCGCCAGCTTAAA
    OEB491ATATCTACAGCGGTACCCCCATGGACCTCGAATTGGAAAT
    OEB492CCGCCTCCGCCGATATCCCCCTAGTCCCGAGGATGCGTA
    OEB497ATATCTACAGCGGTACCCCCATGTCCATCTACAAAGCAAC
    OEB498CCGCCTCCGCCGATATCCCCCTATCTCTCTCCCTCAAGCA
    OEB503ATATCTACAGCGGTACCCCCATGCCCGACGTGAAACACGA
    OEB504CCGCCTCCGCCGATATCCCCTCATGCCTGCTGAGGAGGCT
    OEB544CTGATCGTACCTTGATGTCGACCCGTTGCTATCTCCACAC
    OEB545CGTACAGTTCGAGGATCGTAGTGCAGTCGCCAGCTTTAAA
    OEB487GGTTTTGAGTCTTGGGAGTGG
    OEB548CGACATCAAGGTACGATCAGATGGGCCAAAGTTAGTGGTG
    OEB549TACGATCCTCGAACTGTACGCCTTCTAGTCTCCGCTCCAT
    OEB490CCACAGCTGCTCTTATGACG
    OEB493GTAGTTTCGGTTGCCTCGTC
    OEB550CGACATCAAGGTACGATCAGTCGAGTTACCCTATGTGCTG
    OEB551TACGATCCTCGAACTGTACGGGGTCGGTCTAGGACGATGT
    OEB496GACACAAAGCTCATCGGTGG
    OEB499TGCAATCTCCTCCCAGATTT
    OEB552CGACATCAAGGTACGATCAGTGTCGTGAACGTCTTTGAGC
    OEB553TACGATCCTCGAACTGTACGCTCACGGTATGGGCTGTTCT
    OEB502TCTCCGAGGCCATCATTTAG
    OEB846TTGATCCTGATGGTCGTGAA
    OEB847CGACATCAAGGTACGATCAGATCAGCGGAGATGTTTCGTC
    OEB848TACGATCCTCGAACTGTACGGAATAAACCGTCAGCCCAGA
    OEB849GGCGACACAGTCAGAGCATA
    OEB4CGGAGATGATATCGCCAAAC
    OEB575GAGCTGCCATTGAGAAGGAG
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Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica
Kyle R. Pomraning, Erin L. Bredeweg, Eduard J. Kerkhoven, Kerrie Barry, Sajeet Haridas, Hope Hundley, Kurt LaButti, Anna Lipzen, Mi Yan, Jon K. Magnuson, Blake A. Simmons, Igor V. Grigoriev, Jens Nielsen, Scott E. Baker
mSphere Dec 2018, 3 (6) e00541-18; DOI: 10.1128/mSphere.00541-18

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Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica
Kyle R. Pomraning, Erin L. Bredeweg, Eduard J. Kerkhoven, Kerrie Barry, Sajeet Haridas, Hope Hundley, Kurt LaButti, Anna Lipzen, Mi Yan, Jon K. Magnuson, Blake A. Simmons, Igor V. Grigoriev, Jens Nielsen, Scott E. Baker
mSphere Dec 2018, 3 (6) e00541-18; DOI: 10.1128/mSphere.00541-18
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    • ABSTRACT
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KEYWORDS

Yarrowia
dimorphic
genomics
molecular genetics
morphology
signaling

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