Environmental Microbiology (2006) 8(8), 1460–1470 doi:10.1111/j.1462-2920.2006.01040.x
© 2006 The Authors
Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd
Blackwell Publishing LtdOxford, UKEMIEnvironmental Microbiology 1462-2912© 2006 The Authors; Journal compilation © 2006 Society for Applied Microbiology and Blackwell Publishing Ltd ? 20068814601470Original Article
Polyketide synthase diversity of sponge symbiontsT. K. Kim and J. A. Fuerst
Received 4 November, 2005; accepted 17 February, 2006. *For
correspondence. E-mail j.fuerst@mailbox.uq.edu.au; Tel. (+1) 617
3365 4643; Fax (+1) 617 3365 4699.
Diversity of polyketide synthase genes from bacteria
associated with the marine sponge Pseudoceratina
clavata : culture-dependent and culture-independent
approaches
Tae Kyung Kim and John A. Fuerst*
School of Molecular and Microbial Sciences, University of
Queensland, Brisbane, Qld 4072, Australia.
Summary
Diverse ketosynthase (KS) genes were retrieved from
the microbial community associated with the Great
Barrier Reef sponge Pseudoceratina clavata . Bacterial
isolation and metagenomic approaches were
employed. Phylogenetic analysis of 16S rRNA of cul-
turable sponge-associated bacterial communities
comprised eight groups over four phyla. Ten KS
domains were amplified from four genera of isolates
and phylogenetics demonstrated that these KS
domains were located in three clusters (actinobacte-
rial, cyanobacterial and trans -AT type). Metagenomic
DNA of the sponge microbial community was
extracted to explore community KS genes by two
approaches: direct amplification of KS domains and
construction of fosmid libraries for KS domain screen-
ing. Five KS domains were retrieved from polymerase
chain reaction (PCR) amplification using sponge
metagenome DNA as template and five fosmid clones
containing KS domains found using multiplex PCR
screening. Analysis of selected polyketide synthase
(PKS) from one fosmid showed that the PKS consists
of two modules. Open reading frames located up- and
downstream of the PKS displayed similarity with mem-
brane synthesis-related proteins such as cardiolipin
synthase. Metagenome approaches did not detect KS
domains found in sponge isolates. All KS domains
from both metagenome approaches formed a single
cluster with KS domains originating from metage-
nomes derived from other sponge species from other
geographical regions.
Introduction
Marine sponges have been used as a major source of
new natural bioactive compounds for decades. The origin
of bioactive compounds in marine sponges has been pro-
posed to be from either the sponge itself, their symbiotic
microorganisms, or a cooperative interaction between
sponge and symbiotic microorganisms (Faulkner et al .,
1993; Uriz et al ., 1996; Flowers et al ., 1998). These den-
sity gradient centrifugation-based studies have failed to
establish the location of the source of bioactive com-
pounds with respect to different cell types or regions within
the sponge. In situ hybridization techniques for targeting
biosynthesis genes of interest have been introduced and
have provided strong evidence for the bacterial origin of
marine invertebrate bioactive compounds and expression
of related genes for their synthesis (Davidson et al ., 2001;
Flatt et al ., 2005). In addition, the increasing data regard-
ing bacterial diversity associated with marine sponges
enhances the possibility of finding novel compounds and
their related genes or gene clusters from the marine
sponge-associated bacterial communities (Webster et al .,
2001; Hentschel et al ., 2002; Kim et al ., 2005; Montalvo
et al ., 2005). Both cultural and direct gene retrieval
approaches may be needed to explore the diversity of the
bacteria associated with sponges. Approaches which iso-
late biosynthetic genes or gene clusters from such micro-
bial communities with the aim of eventually providing
symbiont-generated bioactive compounds under con-
trolled conditions have been proposed (Hildebrand et al .,
2004).
Polyketides are well-studied and include many commer-
cially produced biopharmaceuticals. The diversity of their
structures includes macrolides and polyenes and the
diversity of applications includes antibiotics, antitumour
agents, immunosuppressants and the statin class of cho-
lesterol-controlling agents. Type I (modular) polyketide
synthases (PKSs) have been of special interest for their
modularity and suitability for the creation of customized
polyketides (Hopwood, 1997; Pfeifer et al ., 2001;
McDaniel et al ., 2005). A multiplasmid approach employ-
ing plasmids carrying type I PKS genes has a potential to
create thousands of combinations of PKS modules to
produce novel polyketides (Xue et al ., 1999). Recent
advances using synthetic PKS modules have indicated
the importance of a wide database of PKS sequences