The Physiology and Molecular Biology of Sponge Tissues

Abstract

Sponges have become the focus of studies on molecular evolution and the evolution of animal body plans due to their ancient branching point in the metazoan lineage. Whereas our former understanding of sponge function was largely based on a morphological perspective, the recent availability of the first full genome of a sponge (Amphimedon queenslandica), and of the transcriptomes of other sponges, provides a new way of understanding sponges by their molecular components. This wealth of genetic information not only confirms some long-held ideas about sponge form and function but also poses new puzzles. For example, the Amphimedon sponge genome tells us that sponges possess a repertoire of genes involved in control of cell proliferation and in regulation of development. In vitro expression studies with genes involved in stem cell maintenance confirm that archaeocytes are the main stem cell population and are able to differentiate into many cell types in the sponge including pinacocytes and choanocytes. Therefore, the diverse roles of archaeocytes imply differential gene expression within a single cell ontogenetically, and gene expression is likely also different in different species; but what triggers cells to enter one pathway and not another and how each archaeocyte cell type can be identified based on this gene knowledge are new challenges. Whereas molecular data provide a powerful new tool for interpreting sponge form and function, because sponges are suspension feeders, their body plan and physiology are very much dependent on their physical environment, and in particular on flow. Therefore, in order to integrate new knowledge of molecular data into a better understanding the sponge body plan, it is important to use an organismal approach. In this chapter, we give an account of sponge body organization as it relates to the physiology of the sponge in light of new molecular data. We focus, in particular, on the structure of sponge tissues and review descriptive as well as experimental work on choanocyte morphology and function. Special attention is given to pinacocyte epithelia, cell junctions, and the molecules present in sponge epithelia. Studies describing the role of the pinacoderm in sensing, coordination, and secretion are reviewed. A wealth of recent work describes gene presence and expression patterns in sponge tissues during development, and we review this in the context of the previous descriptions of sponge morphology and physiology. A final section addresses recent findings of genes involved in the immune response. This review is far from exhaustive but intends rather to revisit for non-specialists key aspects of sponge morphology and physiology in light of new molecular data as a means to better understand and interpret sponge form and function today.

Introduction

Sponges are unusual animals which, due to their ancient heritage, can shed light on fundamental questions such as the origin of multicellularity, the evolution of tissues, signaling pathways, body polarity, and coordination systems. Sponge body plans are so different from those of other animals that it is difficult to compare even basic features, yet their molecular framework—which was revealed with the first full sponge genome from Amphimedon queenslandica (Srivastava et al., 2010), as well as from transcriptomic and other gene data from other sponges (Nichols et al., 2006, Harcet et al., 2010)—shows that they have a very similar complement of genes and gene pathways to those in other animals. Although at the time of this review we have only one full sponge genome on which to base our comparison, it appears that some of the molecules that may underlie important morphological innovations in animals might be missing in sponges. Examples are the absence of sodium channels from the A. queenslandica genome and yet their presence in choanoflagellates, the closest unicellular ancestor to animals (Liebeskind et al., 2011), and the presence of most components of the post-synaptic density in the sponge genome, including the ligand binding sites, but the absence of the ligands (Sakaraya et al., 2007, Alie and Manuel, 2010). This, together with the suggestion that ctenophores might be basal to sponges (Dunn et al., 2008), implies that sponges may not be ‘witnesses to the pre-history’ of animal systems as was suggested earlier by Pavans de Ceccatty (1974a) but may instead have lost complex animal characters, even neurons, however, unusual that might seem. Increasingly, it becomes clear that we need to revisit the morphology and physiology of sponges in order to better understand the relationship between gene and protein, and between cell and tissue function.

Sponges are suspension feeders, with a body plan designed to process as much water as possible, or needed, for feeding and respiration. Thus, the evolution of the sponge body plan can be seen as being guided by the fluid environment: sponges in low food environments find ways to process more water (use passive flow, e.g. Maldonado and Young, 1998, Leys et al., 2011) or eat different food as in the case of carnivorous sponges (e.g. Vacelet and Boury-Esnault, 1995); sponges in high food environments, or which have formed symbioses with microbes, may need to process less water (Weisz et al., 2008).

Since the sponge is essentially a piping system, whose pressure differences are essential to generate the proper flow rates over the filter, at the cellular level modifications to a canal filtration system require constant readjustments, and therefore, cells and tissues should have the flexibility to adjust and modify the canal system in response to changes in flow to maintain the correct pressure differential. This dependence on flow penetrating all regions of the animal means that regional specialization is less evident than in other animals. In carnivorous sponges, where the tissues are freed up from that dependence, regionalization is often overt with distinct spatial separation of food capture regions and reproductive regions, separation of male and female gametes; where they are still present, choanocyte (feeding) chambers are also segregated to a small region of the sponge body. But all sponges have some regionalization of tissues, and in many groups, skeletal types are regionalized, while in others, reproductive structures are separated from choanosomal feeding tissues. Despite the commonality of the aquiferous system, there are many ways of building it, and the millennia during which sponges have been doing this have generated enough variations on the theme that interpretation of regions as tissues that carry out a common function requires a good understanding of the cell type, origin, and function. Today, molecular expression data can help fill in the picture.

Simpson's ‘The cell biology of sponges’ (1984) is an invaluable comprehensive resource on the structure and function of sponges. It covers a period of research that used ultrastructure to study the fine details of sponge cell function, associations, and lineage, and highlights several areas of uncertain knowledge. Some of these areas we now know more about by the use of new techniques, in particular scanning electron microscopy and immunocytochemistry, but also X-ray microtomography, new physiological approaches, and new molecular data. In order to understand what genes and their products do in sponges, we need to have a good idea of sponge cell biology and physiology. The aim of this review is to re-evaluate aspects of sponge structure and function upon which molecular and physiological data have shed new light. We are selective in our approach and do not intend to try to match Simpson's scope, but rather touch on topics in which new advances have been made with respect to our understanding of sponge tissues, tissue function, differentiation, and patterning. We first provide an overview of sponge body organization and then discuss new interpretations of the cell biology and physiology of sponges, highlighting, where relevant, new knowledge yielded by the study of gene expression.