An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals

Abstract

BackgroundSince the drastic reorganisation of the phylogeny of the animal kingdom into three major clades of bilaterians; Ecdysozoa, Lophotrochozoa and Deuterostomia, it became glaringly obvious that the selection of model systems with extensive molecular resources was heavily biased towards only two of these three clades, namely the Ecdysozoa and Deuterostomia. Increasing efforts have been put towards redressing this imbalance in recent years, and one of the principal phyla in the vanguard of this endeavour is the Annelida.ResultsIn the context of this effort we here report our characterisation of an Expressed Sequence Tag (EST) screen in the serpulid annelid, Pomatoceros lamarckii. We have sequenced over 5,000 ESTs which consolidate into over 2,000 sequences (clusters and singletons). These sequences are used to build phylogenetic trees to estimate relative branch lengths amongst different taxa and, by comparison to genomic data from other animals, patterns of gene retention and loss are deduced.ConclusionThe molecular phylogenetic trees including the P. lamarckii sequences extend early observations that polychaetes tend to have relatively short branches in such trees, and hence are useful taxa with which to reconstruct gene family evolution. Also, with the availability of lophotrochozoan data such as that of P. lamarckii, it is now possible to make much more accurate reconstructions of the gene complement of the ancestor of the bilaterians than was previously possible from comparisons of ecdysozoan and deuterostome genomes to non-bilaterian outgroups. It is clear that the traditional molecular model systems for protostomes (e.g. Drosophila melanogaster and Caenorhabditis elegans), which are restricted to the Ecdysozoa, have undergone extensive gene loss during evolution. These ecdysozoan systems, in terms of gene content, are thus more derived from the bilaterian ancestral condition than lophotrochozoan systems like the polychaetes, and thus cannot be used as good, general representatives of protostome genomes. Currently sequenced insect and nematode genomes are less suitable models for deducing bilaterian ancestral states than lophotrochozoan genomes, despite the array of powerful genetic and mechanistic manipulation techniques in these ecdysozoans. A distinct category of genes that includes those present in non-bilaterians and lophotrochozoans, but which are absent from ecdysozoans and deuterostomes, highlights the need for further lophotrochozoan data to gain a more complete understanding of the gene complement of the bilaterian ancestor.

Schistosome I/Lamides – A new family of bioactive helminth neuropeptides

“…While similar peptides (including –RLamides, -SIamides and -FVRIamides) have been described in other invertebrate phyla, including Annelida and Mollusca (Chen et al, 1995; Pedder et al, 2001; El Filali et al, 2006; Jekely et al, 2008; Takahashi et al, 2009), we could find no evidence for the presence of similar peptides in vertebrate host organisms. The NPP-1-like peptides reported here thus represent a group of novel helminth neuropeptides which, if they are absent from host species, and are functionally conserved across helminths, could represent particularly promising avenues for drug development.…”

Evolutionary crossroads in developmental biology: annelids

“…This conservative nature of annelids, or at least of the polychaete annelids examined, also extends to the less divergent nature of their gene sequences (Fig. 5B) and the retention of more ancestral gene organisations than are found in traditional invertebrate models Takahashi et al, 2009). A greater proportion of the introns that were present in the protostome-deuterostome ancestor (PDA; sometimes called the Urbilaterian ancestor) have been retained in P. dumerilii than in most other invertebrates examined .…”

“…The general picture is one of a greater degree of retention of genes in annelids that were present in the ancestral bilaterian than can be found in ecdysozoan model systems, such as fruit flies and nematodes (e.g. Prud'homme et al, 2002;Tessmar-Raible et al, 2007;Simionato et al, 2008;Takahashi et al, 2009;Cho et al, 2010;Shimeld et al, 2010) (Fig. 5A).…”

Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

“…These results suggest that Hydroides genome content has not evolved as quickly as the fruit fly and nematode genomes. Consistent with these findings, other annelids were found to possess relatively slowly evolving genomes (43,44), and D. melanogaster and C. elegans are documented to possess more derived genomes with extensive gene loss and higher rates of molecular evolution (45,46). Studying mechanisms that mediate bacteria-induced metamorphosis in Hydroides might provide a framework to understand bacteria-animal interactions in diverse animals.…”

“…S1). Previous studies also reported relatively slow evolutionary rates of annelids compared with the model ecdysozoans D. melanogaster and C. elegans (43)(44)(45)(46), suggesting that annelids might share more ancestral characteristics with distantly related model animals. Mechanisms underpinning the metamorphic response of Hydroides to bacterial inducers might therefore have conserved features present in other metazoans and serve as an example of how bacteria impact the development of an animal.…”