Conserved expression of vertebrate microvillar gene homologs in choanocytes of freshwater sponges.

Jesús F Peña,Daniel J Richter,Lingyu Wang,Scott A Nichols,Noriko Funayama,Alexandre Alié

doi:10.1186/s13227-016-0050-x

Abstract

BackgroundThe microvillus is a versatile organelle that serves important functions in disparate animal cell types. However, from a molecular perspective, the microvillus has been well studied in only a few, predominantly vertebrate, contexts. Little is known about how differences in microvillar structure contribute to differences in function, and how these differences evolved. We sequenced the transcriptome of the freshwater sponge, Ephydatia muelleri, and examined the expression of vertebrate microvillar gene homologs in choanocytes—the only microvilli-bearing cell type present in sponges. Sponges offer a distant phylogenetic comparison with vertebrates, and choanocytes are central to discussions about early animal evolution due to their similarity with choanoflagellates, the single-celled sister lineage of modern animals.ResultsWe found that, from a genomic perspective, sponges have conserved homologs of most vertebrate microvillar genes, most of which are expressed in choanocytes, and many of which exhibit choanocyte-specific or choanocyte-enriched expression. Possible exceptions include the cadherins that form intermicrovillar links in the enterocyte brush border and hair cell stereocilia of vertebrates and cnidarians. No obvious orthologs of these proteins were detected in sponges, but at least four candidate cadherins were identified as choanocyte-enriched and might serve this function. In contrast to the evidence for conserved microvillar structure in sponges and vertebrates, we found that choanoflagellates and ctenophores lack homologs of many fundamental microvillar genes, suggesting that microvillar structure may diverge significantly in these lineages, warranting further study.ConclusionsThe available evidence suggests that microvilli evolved early in the prehistory of modern animals and have been repurposed to serve myriad functions in different cellular contexts. Detailed understanding of the sequence by which different microvilli-bearing cell/tissue types diversified will require further study of microvillar composition and development in disparate cell types and lineages. Of particular interest are the microvilli of choanoflagellates, ctenophores, and sponges, which collectively bracket the earliest events in animal evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0050-x) contains supplementary material, which is available to authorized users.

Highlights

The microvillus is a versatile organelle that serves important functions in disparate animal cell types
If HU was applied 90–120 h post-germination, no developmental defects were detected and choanocyte chambers fully formed. We modified this approach to apply HU just prior to choanocyte differentiation. We found that this approach minimized developmental defects and that HU-treated sponges developed all observable features of the untreated control sponges, except that they lacked choanocytes
The six remaining cadherins have no obvious orthology to known microvillar cadherins. We found that both classical cadherin homologs had relatively low, but similar expression levels in E. fluviatilis choanocytes, but that one was significantly enriched in E. fluviatilis choanocytes and showed greater than 12-fold lower expression in HU-treated E. muelleri samples than in controls

Summary

Introduction

The microvillus is a versatile organelle that serves important functions in disparate animal cell types. Specialized feeding cells of sponges, called choanocytes (Fig. 1), are central to discussions about animal cell type evolution due to their similarities with choanoflagellates, the unicellular/colonial sister group of animals [1,2,3,4,5] Both cell types (generally described as “collar cells”) have an apical ring of actin-cored microvilli that surround a microtubule-cored flagellum—features that both lineages use for feeding on bacteria. Open questions remain about how differences in their molecular composition contribute to differences in their function, about how variations in their structure and organization (i.e., length, number) are regulated and, from an evolutionary perspective, how different cell types with microvilli are related—did they evolve through a vertical sequence of descent with modification, or can the microvillus be deployed de novo through activation of a conserved regulatory switch in otherwise unrelated cell types?

Methods

Results

Discussion

Conclusion