Transcriptome Changes during the Life Cycle of the Red Sponge, Mycale phyllophila (Porifera, Demospongiae, Poecilosclerida)

Abstract

Sponges are an ancient metazoan group with broad ecological, evolutionary, and biotechnological importance. As in other marine invertebrates with a biphasic life cycle, the developing sponge undergoes a significant morphological, physiological, and ecological transformation during settlement and metamorphosis. In this study, we compare new transcriptome datasets for three life cycle stages of the red sponge (Mycale phyllophila) to test whether gene expression (as in the model poriferan, Amphimedon queenslandica) also varies more after settlement and metamorphosis. In contrast to A. queenslandica, we find that the transcriptome of M. phyllophila changes more during the earlier pre-competent larva/post-larva transition that spans these defining events. We also find that this transition is marked by a greater frequency of significantly up-regulated Gene Ontology terms including those for morphogenesis, differentiation, and development and that the transcriptomes of its pre-competent larvae and adult are distinct. The life cycle transcriptome variation between M. phyllophila and A. queenslandica may be due to their long separate evolutionary histories and corresponding differences in developmental rates and timing. This study now calls for new transcriptome datasets of M. phyllophila and other sponges, which will allow for tests of the generality of our life cycle expression differences and for the greater exploitation of poriferans in both basic and applied research.

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…Qiu et al 2015, Glöckner et al 2016, Ricci et al 2016. Therefore, to test the accuracy of GO methods, I characterized each list of DEGs using three independently generated GO annotations …”

“…Qiu et al 2015, Reyes-Bermudez et al 2016 were differentially present in each of the three annotation methods, denote highly specific regulatory information, and some of them are vertebrate-specific (e.g. the sponge has no heart, therefore an enrichment in WSP involved in heart development is either spurious or reflects gene pleiotropy between species).…”

“…GO has been widely applied to a variety of studies focusing on previously uncharacterized species (e.g. Glöckner et al 2016, Ricci et al 2016, including developmental RNA-Seq studies seeking to understand the role of genes expressed at a particular life cycle stage or transition (Reyes-Bermudez et al 2009a, Fiedler et al 2010, Heyland et al 2011, Conaco et al 2012, Du et al 2012, Vaughn et al 2012, Qiu et al 2015.…”

“…However, because the GO database is largely derived from a handful of well-characterized model bilaterians, these in silico methods of gene annotation are potentially unreliable in non-model species (e.g. Reyes-Bermudez et al 2009b, Fiedler et al 2010, Heyland et al 2011, Conaco et al 2012b, Du et al 2012, Vaughn et al 2012, Ventura et al 2013, Qiu et al 2015. This may be particularly pronounced in more distantly related taxa, such as non-bilaterian animals (i.e.…”

“…sponges, ctenophores, placozoans and cnidarians; e.g. Putnam et al 2007, Srivastava et al 2008, Shinzato et al 2011, Conaco et al 2012b, Fortunato et al 2012, Ryan et al 2013, Moroz et al 2014, Qiu et al 2015 and non-metazoan eukaryotes (e.g. choanoflagellates, plants, and fungi -excluding model systems such as Arabidopsis and yeast; Galagan et al 2003, Dean et al 2005, King et al 2008, Martinez et al 2009, Collén et al 2013, Suga et al 2013, Fairclough et al 2013).…”