Evolutionary ecology of beta-lactam gene clusters in animals

Wouter Suring, Karen Meusemann, Alexander Blanke, Janine Mariën, Tim Schol, Valeria Agamennone, Anna Faddeeva-Vakhrusheva, Matty P Berg, Abraham Brouwer, Nico M van Straalen, Dick Roelofs, 1KITE Basal Hexapod consortium

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Beta-lactam biosynthesis was thought to occur only in fungi and bacteria, but we recently reported the presence of isopenicillin N synthase in a soil-dwelling animal, Folsomia candida. However, it has remained unclear whether this gene is part of a larger beta-lactam biosynthesis pathway and how widespread the occurrence of penicillin biosynthesis is among animals. Here, we analysed the distribution of beta-lactam biosynthesis genes throughout the animal kingdom and identified a beta-lactam gene cluster in the genome of F. candida (Collembola), consisting of isopenicillin N synthase (IPNS), δ-(L-α-aminoadipoyl)-L-cysteinyl-D-valine synthetase (ACVS), and two cephamycin C genes (cmcI and cmcJ) on a genomic scaffold of 0.76 Mb. All genes are transcriptionally active and are inducible by stress (heat shock). A beta-lactam compound was detected in vivo using an ELISA beta-lactam assay. The gene cluster also contains an ABC transporter which is coregulated with IPNS and ACVS after heat shock. Furthermore, we show that different combinations of beta-lactam biosynthesis genes are present in over 60% of springtail families, but they are absent from genome- and transcript libraries of other animals including close relatives of springtails (Protura, Diplura and insects). The presence of beta-lactam genes is strongly correlated with an euedaphic (soil-living) lifestyle. Beta-lactam genes IPNS and ACVS each form a phylogenetic clade in between bacteria and fungi, while cmcI and cmcJ genes cluster within bacteria. This suggests a single horizontal gene transfer event most probably from a bacterial host, followed by differential loss in more recently evolving species.

Original languageEnglish
Pages (from-to)3217-3229
Number of pages13
JournalMolecular Ecology
Volume26
Issue number12
DOIs
Publication statusPublished - Jun 2017

Keywords

  • Journal Article

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    Suring, W., Meusemann, K., Blanke, A., Mariën, J., Schol, T., Agamennone, V., ... 1KITE Basal Hexapod consortium (2017). Evolutionary ecology of beta-lactam gene clusters in animals. Molecular Ecology, 26(12), 3217-3229. https://doi.org/10.1111/mec.14109