Linking Chemical and Microbial Diversity in Marine Sponges: Possible Role for Poribacteria as Producers of Methyl‐Branched Fatty Acids

Abstract

Many marine sponges contain massive numbers of largely uncultivated, phylogenetically diverse bacteria that seem to be important contributors to the chemistry of these animals. Insights into the diversity, origin, distribution, and function of their metabolic gene communities are crucial to dissect the chemical ecology and biotechnological potential of sponge symbionts. This study reveals a sharp dichotomy between high and low microbial abundance sponges with respect to polyketide synthase (PKS) gene content, the presence of methyl-branched fatty acids, and the presence of members of the symbiotic candidate phylum "Poribacteria". For the symbiont-rich sponge Cacospongia mycofijiensis, a source of the tubulin-inhibiting fijianolides (=laulimalides), near-exhaustive large-scale sequencing of PKS gene-derived PCR amplicons was conducted. Although these amplicons exhibit high diversity at the sequence level, almost all of them belong to a single, architecturally unique group of PKSs present in "Poribacteria" and are proposed to synthesize methyl-branched fatty acids. Three components of this PKS were studied in vitro, providing initial insight into its biochemistry.

Deep sequencing of non-ribosomal peptide synthetases and polyketide synthases from the microbiomes of Australian marine sponges

“…In this study, sup KS domains were detected in abundance within the sponge R. odorabile, along with a small number of cis-KS domains phylogenetically affiliated with actinobacteria. This co-occurrence of these two domain types was also observed from the sponge Cacospongia mycofijiensis (Fieseler et al, 2007;Hochmuth et al, 2010), which belongs to the same order as R. odorabile. The occurrence of these sup type KS domains in R. odorabile coincided with the detection of poribacteria (Fan et al, 2012), which are known to harbour the sup biosynthetic gene cluster (Siegl and Hentschel, 2010;Siegl et al, 2011).…”

“…The majority of these compounds exhibit structural features indicative of bacterial biosynthetic routes and microorganisms have been isolated that are capable of producing sponge-associated metabolites (Boot et al, 2006). Previous molecular studies, utilising vector-dependent approaches, identified a lack of functional diversity among some sponge species due to the dominance of sponge-specific polyketide synthases (PKSs) (Piel et al, 2004b;Schirmer et al, 2005;Fieseler et al, 2007;Hochmuth et al, 2010). This has since led to the development of assays that amplify specific ketosynthase (KS) groups involved in the biosynthesis of complex secondary metabolites (Piel et al, 2004a;Fisch et al, 2009).…”

“…Traditional methods, involving exhaustive extractions of sponge, do not reveal the chemical diversity produced by these rare biosphere representatives, or pathways that are inactive within the native host (Chiang et al, 2010). Harnessing this potentially novel chemistry is, therefore, dependent on the ability of molecular approaches to identify where this diversity exists (Fieseler et al, 2007;Hochmuth et al, 2010;Trindade-Silva et al, 2012), to provide access to the genetic basis of biosynthesis (Piel et al, 2004a;Fisch et al, 2009;Banik and Brady, 2010;Brady et al, 2010) and ultimately to facilitate production of these molecules through heterologous expression within a suitable host (Fu et al, 2008;Craig et al, 2010).…”

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

“…Additionally, certain sponge symbionts produce secondary metabolites that might be involved in the chemical defense of their hosts (Kennedy et al, 2007;Siegl and Hentschel 2010;Thomas et al, 2010a). Genomic information is currently being used to further characterize features of symbiosis and physiological properties and the lifestyle of sponge symbionts (Hochmuth et al, 2010;Thomas et al, 2010b;Siegl et al, 2011).…”

Contemporary molecular tools in microbial ecology and their application to advancing biotechnology

“…Although terrestrial organisms are supposed to be the richest source of natural products, marine ecosystems might also prove to be an important domain for bioprospecting (Putz and Proksch 2010) due to the fact that over 70% of the earth is covered by oceans and large parts of these oceans still remain unexplored or inaccessible. Marine sponges, in this context, are well known for their vast chemical and microbial diversity (Hochmuth, Niederkruger et al 2010, Hentschel, Piel et al 2012 and are an important source of useful bioactive compounds (Noro, Kalaitzis et al 2012). It has long been thought that the host synthesizes these products, but recent findings suggest bacterial origins for many (Piel 2002, Piel, Hofer et al 2004, Zimmermann, Engeser et al 2009 symbioses, but also enables the possibility of biotechnological production of natural products in heterologous hosts.…”