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-...
Main Authors: | , , , , |
---|---|
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 |
id |
doaj-d702b804455647f8970cba8187c4aecd |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT woutersuring biochemicalpathwayssupportingbetalactambiosynthesisinthespringtailfolsomiacandida AT janinemarien biochemicalpathwayssupportingbetalactambiosynthesisinthespringtailfolsomiacandida AT rhodybroekman biochemicalpathwayssupportingbetalactambiosynthesisinthespringtailfolsomiacandida AT nicomvanstraalen biochemicalpathwayssupportingbetalactambiosynthesisinthespringtailfolsomiacandida AT dickroelofs biochemicalpathwayssupportingbetalactambiosynthesisinthespringtailfolsomiacandida |
_version_ |
1721401886056120320 |