Comparative morphogenesis and gene expression during gut development in marine annelids

All life forms share a fundamental requirement to supply their cells with chemical energy. In multicellular animals, this requirement is satisfied by feeding and digestive systems, making the gut one of the most essential metazoan organs. With the evolution of a through gut, digestive systems became regionalized along the gut tube to accommodate food capture, digestion, absorption and removal of waste. Despite the diversity of animal body plans across Metazoa, gut regionalization is relatively conserved. Therefore, molecular mechanisms that specify cells and tissues of an ancient organ system may also be conserved among a broad range of taxa. FoxA and GATA456 transcription factors show similar patterns of expression along the gut tube in Deuterostomia and Ecdysozoa, but few studies have compared those patterns with Lophotrochozoa. This investigation examines the relationship of gut development and gene expression in three lophotrochozoan marine worms with contrasting life history modes and gut architectures, Capitella teleta (Annelida), Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). C. teleta develops a lecithotrophic metatrochophore larva with a 'dorsal pharynx,' the first description of this organ type in a marine polychaete. Chaetopterus develops a planktotrophic larva with a tripartite gut, and T. lageniformis develops a lecithotrophic pelagosphera larva with a U-shaped gut. Both FoxA and GATA456 orthologs were recovered from each worm. In all three species, FoxA is expressed in foregut and hindgut regions, and GATA456 subclass members are expressed in midgut endoderm and visceral mesoderm. Species-specific expression patterns indicate that there are important molecular differences in gut regionalization among lophotrochozoans. Four additional Fox factors were characterized in C. teleta , and their expression patterns are consistent with possible roles in foregut and midgut development when compared with other animals. Overall, FoxA and GATA456 factors show a conserved trend of complementary, regionalized expression along the gut tube in annelid and sipunculan worms, similar to the expression patterns in deuterostome and ecdysozoan models. The significance of this study is that both genes may be core components of a gut-specific, gene regulatory network in lophotrochozoans, and were likely deployed during early evolution of the metazoan through gut.