The Skeleton Forming Proteome of an Early Branching Metazoan: A Molecular Survey of the Biomineralization Components Employed by the Coralline Sponge Vaceletia Sp.

Abstract

The ability to construct a mineralized skeleton was a major innovation for the Metazoa during their evolution in the late Precambrian/early Cambrian. Porifera (sponges) hold an informative position for efforts aimed at unraveling the origins of this ability because they are widely regarded to be the earliest branching metazoans, and are among the first multi-cellular animals to display the ability to biomineralize in the fossil record. Very few biomineralization associated proteins have been identified in sponges so far, with no transcriptome or proteome scale surveys yet available. In order to understand what genetic repertoire may have been present in the last common ancestor of the Metazoa (LCAM), and that may have contributed to the evolution of the ability to biocalcify, we have studied the skeletal proteome of the coralline demosponge Vaceletia sp. and compare this to other metazoan biomineralizing proteomes. We bring some spatial resolution to this analysis by dividing Vaceletia’s aragonitic calcium carbonate skeleton into “head” and “stalk” regions. With our approach we were able to identify 40 proteins from both the head and stalk regions, with many of these sharing some similarity to previously identified gene products from other organisms. Among these proteins are known biomineralization compounds, such as carbonic anhydrase, spherulin, extracellular matrix proteins and very acidic proteins. This report provides the first proteome scale analysis of a calcified poriferan skeletal proteome, and its composition clearly demonstrates that the LCAM contributed several key enzymes and matrix proteins to its descendants that supported the metazoan ability to biocalcify. However, lineage specific evolution is also likely to have contributed significantly to the ability of disparate metazoan lineages to biocalcify.

The Holo-Transcriptome of a Calcified Early Branching Metazoan

“…In order to better understand how Vaceletia sp. manages its microbial community, with the prospect of understanding how this relationship may influence the construction of its highly calcified skeleton (Germer et al, 2015), we also surveyed and characterized some components of Vaceletia's innate immune system.…”

“…They have a widespread distribution and are important members of benthic communities. Due to their position on the metazoan tree of life sponges can be used to test hypotheses regarding the evolution of a variety of important traits such as biologically controlled biomineralisation (Jackson et al, 2007(Jackson et al, , 2011Germer et al, 2015), signaling pathways and gene regulation (Fernandez-Valverde and Degnan, 2016;Levin et al, 2016), gastrulation and mesoderm formation (Nakanishi et al, 2014), and genome evolution.…”

“…species. We previously generated this sequence resource to assist a proteomic survey of Vaceletia's calcified skeleton (Germer et al, 2015). Due to the high abundance and diversity of microbes in this sponge, we reason that interactions between the sponge and its microbial community may also play some role in fabricating its calcified skeleton.…”

New non-bilaterian transcriptomes provide novel insights into the evolution of coralskeletomes

“…As for galaxin-related proteins, collagen IV appears either ubiquitous or absent in different sponge classes, while a patchy distribution can be observed among groups of Demospongiae. Within Heteroscleromorpha presence of type IV collagen appears however, as previously hypothesized by Riesgo et al (2014), associated with the freshwater environment, but among keratose sponges it could be related to the collagenous framework of their organic skeletons (Junqua et al 1974;Germer et al 2015).…”

How evolution made the matrix punch at the multicellularity party

“…found in the coralline sponge Vaceletia, one of the earliest branching metazoans, also making a pre-or early-metazoan origin for this enzyme feasible (8). Darris et al (9) add to this body of work by looking into the evolutionary origin of GPBP.…”