Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Recently, an active set of beta-lactam biosynthesis genes was reported in the genome of the arthropod springtail Folsomia candida (Collembola). Evidence was provided that these genes were acquired through horizontal gene transfer. However, successful integration of fungal- or bacterial-derived beta-lactam biosynthesis into the metabolism of an animal requires the beta-lactam precursor L-α-aminoadipic acid and a phosphopantetheinyl transferase for activation of the first enzymeof the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-Dvaline synthetase (ACVS). In this study, we characterized these supporting pathways and their transcriptional regulation in F. candida. We identified one phosphopantetheinyl transferase and three pathways for L-α-aminoadipic acid production, distinct from the pathways utilized by microorganisms. We found that after heat shock, the phosphopantetheinyl transferase was co-regulated with ACVS, confirming its role in activating ACVS. Two of the three L-α-aminoadipic acid production pathways were downregulated, while PIPOX, an enzyme participating in the pipecolate pathway, was slightly co-regulated with ACVS. This indicates that L-α-aminoadipic acid may not be a limiting factor in beta-lactam biosynthesis in F. candida, in contrast to microorganisms. In conclusion, we show that all components for L-α-aminoadipic acid synthesis are present and transcriptionally active in F. candida. This demonstrates how springtails could have recruited native enzymes to integrate a betalactam biosynthesis pathway into their metabolism after horizontal gene transfer.
Original languageEnglish
Number of pages18
JournalBiology open
DOIs
Publication statusE-pub ahead of print - 15 Nov 2016

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aminoadipic acid
Folsomia candida
beta-lactams
Candida
Biosynthesis
beta-Lactams
Collembola
biochemical pathways
biosynthesis
Acids
transferases
Gene transfer
Horizontal Gene Transfer
Genes
Metabolism
Microorganisms
microorganisms
metabolism
Arthropods
Enzymes

Cite this

@article{88912189627c4fac90a1bcb69cefec48,
title = "Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida",
abstract = "Recently, an active set of beta-lactam biosynthesis genes was reported in the genome of the arthropod springtail Folsomia candida (Collembola). Evidence was provided that these genes were acquired through horizontal gene transfer. However, successful integration of fungal- or bacterial-derived beta-lactam biosynthesis into the metabolism of an animal requires the beta-lactam precursor L-α-aminoadipic acid and a phosphopantetheinyl transferase for activation of the first enzymeof the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-Dvaline synthetase (ACVS). In this study, we characterized these supporting pathways and their transcriptional regulation in F. candida. We identified one phosphopantetheinyl transferase and three pathways for L-α-aminoadipic acid production, distinct from the pathways utilized by microorganisms. We found that after heat shock, the phosphopantetheinyl transferase was co-regulated with ACVS, confirming its role in activating ACVS. Two of the three L-α-aminoadipic acid production pathways were downregulated, while PIPOX, an enzyme participating in the pipecolate pathway, was slightly co-regulated with ACVS. This indicates that L-α-aminoadipic acid may not be a limiting factor in beta-lactam biosynthesis in F. candida, in contrast to microorganisms. In conclusion, we show that all components for L-α-aminoadipic acid synthesis are present and transcriptionally active in F. candida. This demonstrates how springtails could have recruited native enzymes to integrate a betalactam biosynthesis pathway into their metabolism after horizontal gene transfer.",
author = "Wouter Suring and Janine Marien and R.A. Broekman and {van Straalen}, N.M. and D. Roelofs",
year = "2016",
month = "11",
day = "15",
doi = "10.1242/bio.019620",
language = "English",
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Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida. / Suring, Wouter; Marien, Janine ; Broekman, R.A.; van Straalen, N.M.; Roelofs, D.

In: Biology open, 15.11.2016.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida

AU - Suring, Wouter

AU - Marien, Janine

AU - Broekman, R.A.

AU - van Straalen, N.M.

AU - Roelofs, D.

PY - 2016/11/15

Y1 - 2016/11/15

N2 - Recently, an active set of beta-lactam biosynthesis genes was reported in the genome of the arthropod springtail Folsomia candida (Collembola). Evidence was provided that these genes were acquired through horizontal gene transfer. However, successful integration of fungal- or bacterial-derived beta-lactam biosynthesis into the metabolism of an animal requires the beta-lactam precursor L-α-aminoadipic acid and a phosphopantetheinyl transferase for activation of the first enzymeof the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-Dvaline synthetase (ACVS). In this study, we characterized these supporting pathways and their transcriptional regulation in F. candida. We identified one phosphopantetheinyl transferase and three pathways for L-α-aminoadipic acid production, distinct from the pathways utilized by microorganisms. We found that after heat shock, the phosphopantetheinyl transferase was co-regulated with ACVS, confirming its role in activating ACVS. Two of the three L-α-aminoadipic acid production pathways were downregulated, while PIPOX, an enzyme participating in the pipecolate pathway, was slightly co-regulated with ACVS. This indicates that L-α-aminoadipic acid may not be a limiting factor in beta-lactam biosynthesis in F. candida, in contrast to microorganisms. In conclusion, we show that all components for L-α-aminoadipic acid synthesis are present and transcriptionally active in F. candida. This demonstrates how springtails could have recruited native enzymes to integrate a betalactam biosynthesis pathway into their metabolism after horizontal gene transfer.

AB - Recently, an active set of beta-lactam biosynthesis genes was reported in the genome of the arthropod springtail Folsomia candida (Collembola). Evidence was provided that these genes were acquired through horizontal gene transfer. However, successful integration of fungal- or bacterial-derived beta-lactam biosynthesis into the metabolism of an animal requires the beta-lactam precursor L-α-aminoadipic acid and a phosphopantetheinyl transferase for activation of the first enzymeof the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-Dvaline synthetase (ACVS). In this study, we characterized these supporting pathways and their transcriptional regulation in F. candida. We identified one phosphopantetheinyl transferase and three pathways for L-α-aminoadipic acid production, distinct from the pathways utilized by microorganisms. We found that after heat shock, the phosphopantetheinyl transferase was co-regulated with ACVS, confirming its role in activating ACVS. Two of the three L-α-aminoadipic acid production pathways were downregulated, while PIPOX, an enzyme participating in the pipecolate pathway, was slightly co-regulated with ACVS. This indicates that L-α-aminoadipic acid may not be a limiting factor in beta-lactam biosynthesis in F. candida, in contrast to microorganisms. In conclusion, we show that all components for L-α-aminoadipic acid synthesis are present and transcriptionally active in F. candida. This demonstrates how springtails could have recruited native enzymes to integrate a betalactam biosynthesis pathway into their metabolism after horizontal gene transfer.

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