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Widespread Occurrence and Genomic Context of Unusually Small Polyketide Synthase Genes in Microbial Consortia Associated with Marine Sponges

Lars Fieseler,^1, Ute Hentschel,¹ Lubomir Grozdanov,¹ Andreas Schirmer,² Gaiping Wen,³ Matthias Platzer,³ Sinia Hrvatin,^4, Daniel Butzke,^4, Katrin Zimmermann,⁴ and Jörn Piel^4*

Research Center for Infectious Diseases, University of Würzburg, Röntgenring 11, 97070 Würzburg, Germany,¹ Kosan Biosciences, Inc., Hayward, California 94545,² Genome Analysis, Leibniz Institute for Age Research-Fritz Lipmann Institute, Beutenbergstr. 11, Beutenberg Campus, 07745 Jena, Germany,³ Kekulé Institute of Organic Chemistry and Biochemistry, University of Bonn, Gerhard-Domagk-Str. 1, 53121 Bonn, Germany⁴

Received 25 September 2006/ Accepted 1 February 2007

Numerous marine sponges harbor enormous amounts of as-yet-uncultivated bacteria in their tissues. There is increasing evidence that these symbionts play an important role in the synthesis of protective metabolites, many of which are of great pharmacological interest. In this study, genes for the biosynthesis of polyketides, one of the most important classes of bioactive natural products, were systematically investigated in 20 demosponge species from different oceans. Unexpectedly, the sponge metagenomes were dominated by a ubiquitously present, evolutionarily distinct, and highly sponge-specific group of polyketide synthases (PKSs). Open reading frames resembling animal fatty acid genes were found on three corresponding DNA regions isolated from the metagenomes of Theonella swinhoei and Aplysina aerophoba. Their architecture suggests that methyl-branched fatty acids are the metabolic product. According to a phylogenetic analysis of housekeeping genes, at least one of the PKSs belongs to a bacterium of the Deinococcus-Thermus phylum. The results provide new insights into the chemistry of sponge symbionts and allow inference of a detailed phylogeny of the diverse functional PKS types present in sponge metagenomes. Based on these qualitative and quantitative data, we propose a significantly simplified strategy for the targeted isolation of biomedically relevant PKS genes from complex sponge-symbiont associations.

Published ahead of print on 9 February 2007.

Present address: Institute of Food Science and Nutrition, Food Microbiology, Swiss Federal Institute of Technology (ETH) Zurich, Schmelzbergstrasse 7, CH-8092 Zurich, Switzerland.

Present address: Harvard College, 8 Garden St., Cambridge, MA 02138.

Present address: Institut für Chemie und Biochemie der Freien Universität Berlin, Thielallee 63, 14195 Berlin, Germany.