Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica View Full Text


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Article Info

DATE

2016-02-25

AUTHORS

Kyle R. Pomraning, Young-Mo Kim, Carrie D. Nicora, Rosalie K. Chu, Erin L. Bredeweg, Samuel O. Purvine, Dehong Hu, Thomas O. Metz, Scott E. Baker

ABSTRACT

BackgroundYarrowia lipolytica is an oleaginous ascomycete yeast that stores lipids in response to limitation of nitrogen. While the enzymatic pathways responsible for neutral lipid accumulation in Y. lipolytica are well characterized, regulation of these pathways has received little attention. We therefore sought to characterize the response to nitrogen limitation at system-wide levels, including the proteome, phosphoproteome and metabolome, to better understand how this organism regulates and controls lipid metabolism and to identify targets that may be manipulated to improve lipid yield.ResultsWe found that ribosome structural genes are down-regulated under nitrogen limitation, during which nitrogen containing compounds (alanine, putrescine, spermidine and urea) are depleted and sugar alcohols and TCA cycle intermediates accumulate (citrate, fumarate and malate). We identified 1219 novel phosphorylation sites in Y. lipolytica, 133 of which change in their abundance during nitrogen limitation. Regulatory proteins, including kinases and DNA binding proteins, are particularly enriched for phosphorylation. Within lipid synthesis pathways, we found that ATP-citrate lyase, acetyl-CoA carboxylase and lecithin cholesterol acyl transferase are phosphorylated during nitrogen limitation while many of the proteins involved in β-oxidation are down-regulated, suggesting that storage lipid accumulation may be regulated by phosphorylation of key enzymes. Further, we identified short DNA elements that associate specific transcription factor families with up- and down-regulated genes.ConclusionsIntegration of metabolome, proteome and phosphoproteome data identifies lipid accumulation in response to nitrogen limitation as a two-fold result of increased production of acetyl-CoA from excess citrate and decreased capacity for β-oxidation. More... »

PAGES

138

References to SciGraph publications

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  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/s12864-016-2471-2

    DOI

    http://dx.doi.org/10.1186/s12864-016-2471-2

    DIMENSIONS

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    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/26911370


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    35 schema:description BackgroundYarrowia lipolytica is an oleaginous ascomycete yeast that stores lipids in response to limitation of nitrogen. While the enzymatic pathways responsible for neutral lipid accumulation in Y. lipolytica are well characterized, regulation of these pathways has received little attention. We therefore sought to characterize the response to nitrogen limitation at system-wide levels, including the proteome, phosphoproteome and metabolome, to better understand how this organism regulates and controls lipid metabolism and to identify targets that may be manipulated to improve lipid yield.ResultsWe found that ribosome structural genes are down-regulated under nitrogen limitation, during which nitrogen containing compounds (alanine, putrescine, spermidine and urea) are depleted and sugar alcohols and TCA cycle intermediates accumulate (citrate, fumarate and malate). We identified 1219 novel phosphorylation sites in Y. lipolytica, 133 of which change in their abundance during nitrogen limitation. Regulatory proteins, including kinases and DNA binding proteins, are particularly enriched for phosphorylation. Within lipid synthesis pathways, we found that ATP-citrate lyase, acetyl-CoA carboxylase and lecithin cholesterol acyl transferase are phosphorylated during nitrogen limitation while many of the proteins involved in β-oxidation are down-regulated, suggesting that storage lipid accumulation may be regulated by phosphorylation of key enzymes. Further, we identified short DNA elements that associate specific transcription factor families with up- and down-regulated genes.ConclusionsIntegration of metabolome, proteome and phosphoproteome data identifies lipid accumulation in response to nitrogen limitation as a two-fold result of increased production of acetyl-CoA from excess citrate and decreased capacity for β-oxidation.
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    42 ConclusionsIntegration
    43 DNA
    44 DNA elements
    45 ResultsWe
    46 TCA cycle intermediates
    47 Y. lipolytica
    48 Yarrowia
    49 abundance
    50 accumulation
    51 acetyl-CoA carboxylase
    52 acyl transferase
    53 alcohol
    54 analysis
    55 ascomycete yeasts
    56 attention
    57 capacity
    58 carboxylase
    59 cholesterol acyl transferase
    60 citrate
    61 compounds
    62 control lipid metabolism
    63 cycle intermediates
    64 elements
    65 enzymatic pathways
    66 enzyme
    67 excess citrate
    68 factor family
    69 family
    70 genes
    71 intermediates
    72 key enzyme
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    74 lecithin cholesterol acyl transferase
    75 levels
    76 limitation of nitrogen
    77 limitations
    78 lipid accumulation
    79 lipid metabolism
    80 lipid synthesis pathway
    81 lipid yield
    82 lipids
    83 lipolytica
    84 little attention
    85 lyase
    86 metabolism
    87 metabolome
    88 multi-omics analysis
    89 neutral lipid accumulation
    90 nitrogen
    91 nitrogen limitation
    92 novel phosphorylation sites
    93 organisms
    94 pathway
    95 phosphoproteome
    96 phosphorylation
    97 phosphorylation sites
    98 production
    99 protein
    100 proteome
    101 regulation
    102 regulator
    103 regulatory proteins
    104 response
    105 results
    106 short DNA elements
    107 sites
    108 specific transcription factor family
    109 storage lipid accumulation
    110 structural gene
    111 sugar alcohols
    112 synthesis pathway
    113 system-wide level
    114 target
    115 transcription factor family
    116 transferase
    117 two-fold result
    118 yeast
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    121 schema:name Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica
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