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

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-...

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Main Authors: Wouter Suring, Janine Mariën, Rhody Broekman, Nico M. van Straalen, Dick Roelofs
Format: Article
Language:English
Published: The Company of Biologists 2016-12-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/5/12/1784
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spelling doaj-d702b804455647f8970cba8187c4aecd2021-06-02T19:22:37ZengThe Company of BiologistsBiology Open2046-63902016-12-015121784178910.1242/bio.019620019620Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candidaWouter Suring0Janine Mariën1Rhody Broekman2Nico M. van Straalen3Dick Roelofs4 Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085-1087, Amsterdam 1081 HV, The Netherlands Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085-1087, Amsterdam 1081 HV, The Netherlands Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085-1087, Amsterdam 1081 HV, The Netherlands Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085-1087, Amsterdam 1081 HV, The Netherlands Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085-1087, Amsterdam 1081 HV, The Netherlands 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 enzyme of the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-D-valine 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 beta-lactam biosynthesis pathway into their metabolism after horizontal gene transfer.http://bio.biologists.org/content/5/12/1784Beta-lactamL-α-aminoadipateHeat shockCollembolaGene expression
collection DOAJ
language English
format Article
sources DOAJ
author Wouter Suring
Janine Mariën
Rhody Broekman
Nico M. van Straalen
Dick Roelofs
spellingShingle Wouter Suring
Janine Mariën
Rhody Broekman
Nico M. van Straalen
Dick Roelofs
Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
Biology Open
Beta-lactam
L-α-aminoadipate
Heat shock
Collembola
Gene expression
author_facet Wouter Suring
Janine Mariën
Rhody Broekman
Nico M. van Straalen
Dick Roelofs
author_sort Wouter Suring
title Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
title_short Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
title_full Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
title_fullStr Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
title_full_unstemmed Biochemical pathways supporting beta-lactam biosynthesis in the springtail Folsomia candida
title_sort biochemical pathways supporting beta-lactam biosynthesis in the springtail folsomia candida
publisher The Company of Biologists
series Biology Open
issn 2046-6390
publishDate 2016-12-01
description 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 enzyme of the pathway, δ-(L-α-aminoadipoyl)-L-cysteinyl-D-valine 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 beta-lactam biosynthesis pathway into their metabolism after horizontal gene transfer.
topic Beta-lactam
L-α-aminoadipate
Heat shock
Collembola
Gene expression
url http://bio.biologists.org/content/5/12/1784
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