Evolutionary ecology of beta-lactam gene clusters in animals.
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.
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Wouter
W
Suring
Department of Evolutionary Biology and Evolution, Institute for Biology I, University of Freiburg, Hauptstr. 1, D-79104, Freiburg (Brsg.), Germany.|Australian National Insect Collection, CSIRO National Research Collections Australia, Clunies Ross Street, Acton, ACT2601, Canberra, ACT, Australia.|Center for Molecular Biodiversity Research, Zoological Research Museum A. Koenig, Adenauerallee 160, D-53113, Bonn, Germany.
Karen
K
Meusemann
Medical and Biological Engineering Research Group, School of Engineering, University of Hull, Hull, HU6 7RX, UK.
Alexander
A
Blanke
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Janine
J
Mariën
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Tim
T
Schol
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Valeria
V
Agamennone
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Anna
A
Faddeeva-Vakhrusheva
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.|Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands.
Matty P
MP
Berg
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.|BioDetection Systems B.V., Science Park 406, 1098 XH, Amsterdam, The Netherlands.
Abraham
A
Brouwer
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Nico M
NM
van Straalen
Department of Ecological Science, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands.
Dick
http://orcid.org/0000-0003-3954-3590
D
Roelofs
D000818:Animals; D060829:Arthropod Proteins / Q000235:genetics*; D001181:Arthropods / Q000201:enzymology / Q000235:genetics*; D002513:Cephamycins; D005810:Multigene Family; D010088:Oxidoreductases / Q000235:genetics; D010453:Peptide Synthases / Q000235:genetics; D010802:Phylogeny; D047090:beta-Lactams
D060829:Arthropod Proteins; D002513:Cephamycins; D047090:beta-Lactams; D010088:Oxidoreductases; C038370:isopenicillin N synthetase; D010453:Peptide Synthases; C095368:alpha-aminoadipyl-cysteinyl-valine synthetase; C024925:cephamycin C
Collembola; antibiotic biosynthesis; gene expression; horizontal gene transfer