When you hear the word “sponge”, what comes to mind? Perhaps your favorite bath-time cleaning implement? It turns out that the humble sponge can do more than just scrub away dirt; it can provide researchers with a glimpse into the evolution of multicellular organisms. In a recent Nature paper (1), Mansi Srivastava et al. presented the genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef. What makes this paper interesting isn’t the sequence itself, but rather what we can learn from it.
Sponges are generally recognized as the oldest surviving Metazoan (i.e., multicellular member of the Animal Kingdom). Although sponges lack some of the basic features of the higher Eumetazoans (i.e., “true” animals) such as a gut and nervous system, they share a number of key genes involved in the six hallmarks of multicellular organisms: 1) regulation of cell cycle and growth, 2) programmed cell death, 3) cell-cell and cell-matrix adhesion, 4) developmental signaling and gene regulation, 5) allorecognition and innate immunity and 6) specialization of cell types. Thus, analysis of the sponge genome may provide valuable insight into which genes were required for the evolution of multicelluar organisms and the origin of those genes.
Srivastava et al. determined that the A. queenslandica genome exhibits significant conservation of gene structure and genome organization compared to the genome of other animals and has ~30,000 predicted protein-coding loci, of which 18,693 (63%) have identifiable homologs in other organisms. Many of these genes belong to one of the 1,286 metazoan-specific gene families, which emerged during the ~150- to 200-million-year period before sponges diverged from other animals (i.e., the metazoan stem; see Figure 1 of the Nature paper). During this time period, nearly 75% of these animal-specific gene families arose through gene duplication and divergence, and 235 animal-specific protein domains and 769 combinations of animal-specific domains evolved. Examples include homeodomain proteins and basic helix-loop-helix domains (2,3). Likewise, there was a significant expansion of proteins that contain the immunoglobulin-like domain and are involved in cellular recognition, binding or adhesion. The authors identified 218 predicted immunoglobulin-like domain-containing proteins in Amphimedon but only 5 in Monosiga brevicollis, a closely-related but nonmetazoan organism.
Some of these newly evolved animal-specific genes combined with more ancient gene products to provide novel functionalities or regulatory mechanisms. A good example illustrates the evolution of the p53-mediated apoptotic response to DNA damage: The p53/p63/p73 tumor suppressor family is found in organisms more primitive than metazoans; however, the homeodomain-interacting protein kinase that activates p53 in the presence of DNA breaks is metazoan-specific, and the MDM2 ubiquitin ligase that regulates p53 is eumetazoan-specific.
In addition, the ligands, receptors and transcription factors involved in signaling pathways that determine cellular identity and direct morphogenesis are all metazoan-specific. However, many of the cytosolic signal transducers pre-date metazoans. This suggests that new pathways arose through the interaction of novel ligands and receptors with existing signaling mechanisms.
The Amphimedon genome also revealed interesting clues about how and when certain tissues may have evolved. The presence of post-synaptic and proneural regulatory protein orthologs in Amphimedon implies the existence of an ancestral protoneuron. However, some key synaptic proteins are missing. Thus, although the metazoan ancestor possessed a complex sensory system, a complex nervous system was not possible until evolutionary advancements were made by the eumetazoans. Also, sponges do not have a mesoderm, and appropriately, the Amphimedon genome seems to lack transcription factors involved in mesoderm development. However, despite the lack of a neuromuscular system, sponges do have several transcription factors associated with determination or differentiation of nerves and muscle cells.
Finally, one last point that I found interesting: The Amphimedon genome encodes caspases, which are key cysteine proteases involved in both the intrinsic and extrinsic apoptosis pathways. The intrinsic apoptosis pathway, which involves permeabilization of the outer mitochondrial membrane, is likely the original mechanism for inducing apoptosis because some of the necessary components have more ancient origins and predate metazoans.
Thus, the lowly sponge can teach us a great deal about our own evolution and the evolution of other animals. How much more can we gleen from its DNA? Perhaps a lot, and some of that information could have important implications. Researchers have known for some time that many genes associated with multicellularity are also implicated in cancer and autoimmune disorders, which are nothing more than aberrant regulation of cell growth and immunity, respectively. It makes me wonder: How much more can we learn from the humble sponge?
- Srivastava M. et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature, 466, 720–7 PMID: 20686567
- Simionato, E. et al. (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: Insights from comparative genomics. BMC Evol. Biol. 7, 33.
- Larroux, C. et al. (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol. Biol. Evol. 25, 980–96.
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