Extra-and intracellular lactose catabolism in Penicillium chrysogenum: Phylogenetic and expression analysis of the putative permease and hydrolase genes

Ágota Jónás, E. Fekete, M. Flipphi, E. Sándor, Szilvia Jäger, Ákos P. Molnár, A. Szentirmai, L. Karaffa

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4 Citations (Scopus)

Abstract

Penicillium chrysogenum is used as an industrial producer of penicillin. We investigated its catabolism of lactose, an abundant component of whey used in penicillin fermentation, comparing the type strain NRRL 1951 with the high producing strain AS-P-78. Both strains grew similarly on lactose as the sole carbon source under batch conditions, exhibiting almost identical time profiles of sugar depletion. In silico analysis of the genome sequences revealed that P. chrysogenum features at least five putative β-galactosidase (bGal)-encoding genes at the annotated loci Pc22g14540, Pc12g11750, Pc16g12750, Pc14g01510 and Pc06g00600. The first two proteins appear to be orthologs of two Aspergillus nidulans family 2 intracellular glycosyl hydrolases expressed on lactose. The latter three P. chrysogenum proteins appear to be distinct paralogs of the extracellular bGal from A. niger, LacA, a family 35 glycosyl hydrolase. The P. chrysogenum genome also specifies two putative lactose transporter genes at the annotated loci Pc16g06850 and Pc13g08630. These are orthologs of paralogs of the gene encoding the high-affinity lactose permease (lacpA) in A. nidulans for which P. chrysogenum appears to lack the ortholog. Transcript analysis of Pc22g14540 showed that it was expressed exclusively on lactose, whereas Pc12g11750 was weakly expressed on all carbon sources tested, including D-glucose. Pc16g12750 was co-expressed with the two putative intracellular bGal genes on lactose and also responded on L-arabinose. The Pc13g08630 transcript was formed exclusively on lactose. The data strongly suggest that P. chrysogenum exhibits a dual assimilation strategy for lactose, simultaneously employing extracellular and intracellular hydrolysis, without any correlation to the penicillin-producing potential of the studied strains.

Original languageEnglish
Pages (from-to)489-497
Number of pages9
JournalJournal of Antibiotics
Volume67
Issue number7
DOIs
Publication statusPublished - 2014

Fingerprint

Penicillium chrysogenum
Membrane Transport Proteins
Hydrolases
Lactose
Genes
Penicillins
Aspergillus nidulans
Carbon
Galactosidases
Genome
Arabinose
Computer Simulation
Fermentation
Sequence Analysis
Proteins
Hydrolysis
Glucose

Keywords

  • beta-galactosidase
  • D-galactose
  • L-arabinose
  • lactose
  • Penicillium chrysogenum
  • permease

ASJC Scopus subject areas

  • Pharmacology
  • Drug Discovery

Cite this

@article{a72e8ae6444f4e35a1cae6acd4ca8ed0,
title = "Extra-and intracellular lactose catabolism in Penicillium chrysogenum: Phylogenetic and expression analysis of the putative permease and hydrolase genes",
abstract = "Penicillium chrysogenum is used as an industrial producer of penicillin. We investigated its catabolism of lactose, an abundant component of whey used in penicillin fermentation, comparing the type strain NRRL 1951 with the high producing strain AS-P-78. Both strains grew similarly on lactose as the sole carbon source under batch conditions, exhibiting almost identical time profiles of sugar depletion. In silico analysis of the genome sequences revealed that P. chrysogenum features at least five putative β-galactosidase (bGal)-encoding genes at the annotated loci Pc22g14540, Pc12g11750, Pc16g12750, Pc14g01510 and Pc06g00600. The first two proteins appear to be orthologs of two Aspergillus nidulans family 2 intracellular glycosyl hydrolases expressed on lactose. The latter three P. chrysogenum proteins appear to be distinct paralogs of the extracellular bGal from A. niger, LacA, a family 35 glycosyl hydrolase. The P. chrysogenum genome also specifies two putative lactose transporter genes at the annotated loci Pc16g06850 and Pc13g08630. These are orthologs of paralogs of the gene encoding the high-affinity lactose permease (lacpA) in A. nidulans for which P. chrysogenum appears to lack the ortholog. Transcript analysis of Pc22g14540 showed that it was expressed exclusively on lactose, whereas Pc12g11750 was weakly expressed on all carbon sources tested, including D-glucose. Pc16g12750 was co-expressed with the two putative intracellular bGal genes on lactose and also responded on L-arabinose. The Pc13g08630 transcript was formed exclusively on lactose. The data strongly suggest that P. chrysogenum exhibits a dual assimilation strategy for lactose, simultaneously employing extracellular and intracellular hydrolysis, without any correlation to the penicillin-producing potential of the studied strains.",
keywords = "beta-galactosidase, D-galactose, L-arabinose, lactose, Penicillium chrysogenum, permease",
author = "{\'A}gota J{\'o}n{\'a}s and E. Fekete and M. Flipphi and E. S{\'a}ndor and Szilvia J{\"a}ger and Moln{\'a}r, {{\'A}kos P.} and A. Szentirmai and L. Karaffa",
year = "2014",
doi = "10.1038/ja.2014.26",
language = "English",
volume = "67",
pages = "489--497",
journal = "Journal of Antibiotics",
issn = "0021-8820",
publisher = "Japan Antibiotics Research Association",
number = "7",

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TY - JOUR

T1 - Extra-and intracellular lactose catabolism in Penicillium chrysogenum

T2 - Phylogenetic and expression analysis of the putative permease and hydrolase genes

AU - Jónás, Ágota

AU - Fekete, E.

AU - Flipphi, M.

AU - Sándor, E.

AU - Jäger, Szilvia

AU - Molnár, Ákos P.

AU - Szentirmai, A.

AU - Karaffa, L.

PY - 2014

Y1 - 2014

N2 - Penicillium chrysogenum is used as an industrial producer of penicillin. We investigated its catabolism of lactose, an abundant component of whey used in penicillin fermentation, comparing the type strain NRRL 1951 with the high producing strain AS-P-78. Both strains grew similarly on lactose as the sole carbon source under batch conditions, exhibiting almost identical time profiles of sugar depletion. In silico analysis of the genome sequences revealed that P. chrysogenum features at least five putative β-galactosidase (bGal)-encoding genes at the annotated loci Pc22g14540, Pc12g11750, Pc16g12750, Pc14g01510 and Pc06g00600. The first two proteins appear to be orthologs of two Aspergillus nidulans family 2 intracellular glycosyl hydrolases expressed on lactose. The latter three P. chrysogenum proteins appear to be distinct paralogs of the extracellular bGal from A. niger, LacA, a family 35 glycosyl hydrolase. The P. chrysogenum genome also specifies two putative lactose transporter genes at the annotated loci Pc16g06850 and Pc13g08630. These are orthologs of paralogs of the gene encoding the high-affinity lactose permease (lacpA) in A. nidulans for which P. chrysogenum appears to lack the ortholog. Transcript analysis of Pc22g14540 showed that it was expressed exclusively on lactose, whereas Pc12g11750 was weakly expressed on all carbon sources tested, including D-glucose. Pc16g12750 was co-expressed with the two putative intracellular bGal genes on lactose and also responded on L-arabinose. The Pc13g08630 transcript was formed exclusively on lactose. The data strongly suggest that P. chrysogenum exhibits a dual assimilation strategy for lactose, simultaneously employing extracellular and intracellular hydrolysis, without any correlation to the penicillin-producing potential of the studied strains.

AB - Penicillium chrysogenum is used as an industrial producer of penicillin. We investigated its catabolism of lactose, an abundant component of whey used in penicillin fermentation, comparing the type strain NRRL 1951 with the high producing strain AS-P-78. Both strains grew similarly on lactose as the sole carbon source under batch conditions, exhibiting almost identical time profiles of sugar depletion. In silico analysis of the genome sequences revealed that P. chrysogenum features at least five putative β-galactosidase (bGal)-encoding genes at the annotated loci Pc22g14540, Pc12g11750, Pc16g12750, Pc14g01510 and Pc06g00600. The first two proteins appear to be orthologs of two Aspergillus nidulans family 2 intracellular glycosyl hydrolases expressed on lactose. The latter three P. chrysogenum proteins appear to be distinct paralogs of the extracellular bGal from A. niger, LacA, a family 35 glycosyl hydrolase. The P. chrysogenum genome also specifies two putative lactose transporter genes at the annotated loci Pc16g06850 and Pc13g08630. These are orthologs of paralogs of the gene encoding the high-affinity lactose permease (lacpA) in A. nidulans for which P. chrysogenum appears to lack the ortholog. Transcript analysis of Pc22g14540 showed that it was expressed exclusively on lactose, whereas Pc12g11750 was weakly expressed on all carbon sources tested, including D-glucose. Pc16g12750 was co-expressed with the two putative intracellular bGal genes on lactose and also responded on L-arabinose. The Pc13g08630 transcript was formed exclusively on lactose. The data strongly suggest that P. chrysogenum exhibits a dual assimilation strategy for lactose, simultaneously employing extracellular and intracellular hydrolysis, without any correlation to the penicillin-producing potential of the studied strains.

KW - beta-galactosidase

KW - D-galactose

KW - L-arabinose

KW - lactose

KW - Penicillium chrysogenum

KW - permease

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U2 - 10.1038/ja.2014.26

DO - 10.1038/ja.2014.26

M3 - Article

C2 - 24690910

AN - SCOPUS:84904974407

VL - 67

SP - 489

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JO - Journal of Antibiotics

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SN - 0021-8820

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