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MBE Advance Access published online on July 8, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn150
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© 2008 The Authors.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Research Article

Halogenase genes in two nonribosomal peptide synthetase gene clusters of Microcystis (Cyanobacteria): sporadic distribution and evolution

Sabrina Cadel-Six*, Catherine Dauga{dagger}, Anne Marie Castets*, Rosmarie Rippka*, Christiane Bouchier{dagger}{dagger}, Nicole Tandeau de Marsac*,{ddagger} and Martin Welker*,§,¶

* Institut Pasteur, Unité des Cyanobactéries; CNRS, URA 2172, F75015 Paris, France
{dagger} Institut Pasteur, Genopole® Ile de France - Plateforme 4, F75015 Paris, France
{dagger}{dagger} Institut Pasteur, Genopole® Ile de France - Plateforme 1, F75015 Paris, France
§ Technische Universität Berlin, Inst. Chemie, AG Biochemie & Molekulare Biologie, Franklinstr. 29, 10587 Berlin, Germany

{ddagger} Corresponding author: N. Tandeau de Marsac, Unité des Cyanobactéries, Département de Microbiologie, Institut Pasteur, 28 rue du Docteur Roux, 75724 Paris Cedex 15, France. E-mail address: ntmarsac{at}pasteur.fr. Tel: +33 (0)1 45 68 84 15; Fax: +33 (0)1 40 61 30 42.

Received for publication April 25, 2008. Revision received June 24, 2008. Accepted for publication July 3, 2008.

Cyanobacteria of the genus Microcystis are known to produce secondary metabolites of large structural diversity by nonribosomal peptide synthetase (NRPS) pathways. For a number of such compounds, halogenated congeners have been reported along with non-halogenated ones. In the present study, chlorinated cyanopeptolin and/or aeruginosin type peptides were detected by mass spectrometry in 17 out of 28 axenic strains of Microcystis. In these strains, a halogenase gene was identified between two genes coding for NRPS modules in respective gene clusters, while it was consistently absent when the strains produced only non-chlorinated corresponding congeners. Nucleotide sequences were obtained for 12 complete halogenase genes and 14 inter-module regions of gene clusters lacking a halogenase gene or containing only fragments of it. When a halogenase gene was found absent, a specific, identical excision pattern was observed for both synthetase gene clusters in most strains. A phylogenetic analysis including other bacterial halogenases showed that the NRPS related halogenases of Microcystis form a monophyletic group divided into two sub-groups, corresponding to either the cyanopeptolin or the aeruginosin peptide synthetases. The distribution of these peptide synthetase gene clusters, among the tested Microcystis strains, was found in relative agreement with their phylogeny reconstructed from 16S-23S rDNAs intergenic spacer sequences, while the distribution of the associated halogenase genes appears to be sporadic. The presented data suggest that in cyanobacteria these prevalent halogenase genes originated from an ancient horizontal gene transfer followed by duplication in the cyanobacterial lineage. We propose an evolutionary scenario implying repeated gene losses to explain the distribution of halogenase genes in two NRPS gene clusters that subsequently defines the seemingly erratic production of halogenated and non-halogenated aeruginosins and cyanopeptolins among Microcystis strains.

Key Words: halogenase • cyanopeptolin • aeruginosin • DNA rearrangement • secondary peptide metabolite • chlorination • internal transcribed spacer (ITS) • phylogeny

Present address: Anagnostec GmbH, Am Mühlenberg 11, 14476 Potsdam, Germany


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[Abstract] [Full Text] [PDF]


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