The Analysis of Eight Transcriptomes from All Poriferan Classes Reveals Surprising Genetic Complexity in Sponges

Abstract

Sponges (Porifera) are among the earliest evolving metazoans. Their filter-feeding body plan based on choanocyte chambers organized into a complex aquiferous system is so unique among metazoans that it either reflects an early divergence from other animals prior to the evolution of features such as muscles and nerves, or that sponges lost these characters. Analyses of the Amphimedon and Oscarella genomes support this view of uniqueness-many key metazoan genes are absent in these sponges-but whether this is generally true of other sponges remains unknown. We studied the transcriptomes of eight sponge species in four classes (Hexactinellida, Demospongiae, Homoscleromorpha, and Calcarea) specifically seeking genes and pathways considered to be involved in animal complexity. For reference, we also sought these genes in transcriptomes and genomes of three unicellular opisthokonts, two sponges (A. queenslandica and O. carmela), and two bilaterian taxa. Our analyses showed that all sponge classes share an unexpectedly large complement of genes with other metazoans. Interestingly, hexactinellid, calcareous, and homoscleromorph sponges share more genes with bilaterians than with nonbilaterian metazoans. We were surprised to find representatives of most molecules involved in cell-cell communication, signaling, complex epithelia, immune recognition, and germ-lineage/sex, with only a few, but potentially key, absences. A noteworthy finding was that some important genes were absent from all demosponges (transcriptomes and the Amphimedon genome), which might reflect divergence from main-stem lineages including hexactinellids, calcareous sponges, and homoscleromorphs. Our results suggest that genetic complexity arose early in evolution as shown by the presence of these genes in most of the animal lineages, which suggests sponges either possess cryptic physiological and morphological complexity and/or have lost ancestral cell types or physiological processes.

Sterol and genomic analyses validate the sponge biomarker hypothesis

“…Isopropylcholesterols, for example, are most common in the order Halichondrida, but can be found sporadically across all major demosponge clades (4). Because A. queenslandica lacks C 30 sterols, we also analyzed the transcriptomes from six additional demosponges (Crella elegans, Ircinia fasciculata, Chondrilla nucula, Pseudospongosorites suberitoides, Spongilla lacustris, and Petrosia ficiformis) (20) as well as genomes from the homoscleromorph sponge Oscarella carmela and calcareous sponge Sycon ciliatum. This larger dataset includes sponges that produce rare C 29 and C 30 sterols (see Fig.…”

“…This suggests that one SMT gene is responsible for the first round of methylation of (B) Distribution of sterol synthesis genes across eukaryotes. This phylogeny represents a consensus tree based on previous phylogenetic studies (6,20,35). In some cases, multiple genes have been combined into one category based on shared enzymatic function.…”

“…This interpretation is also contradicted by significant research demonstrating that demosponges perform de novo sterol synthesis and side chain alkylation (23,26) and that sterol patterns do not differ dramatically within species collected from different locations or times (19). The protocols used to generate the transcriptomes involved the enrichment of eukaryotic mRNAs (20), meaning that genes from prokaryotic symbionts could have been lost. This is relevant because it has been suggested that a bacterial symbiont of demosponges (phylum Poribacteria) has an SMT (27).…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Now known to be unique to Metazoa [24 -26], a full complement of TGF-b signalling components (TGF-b and BMP ligands, their receptors, and numerous SMAD cofactors) has been found in cnidarians [27 -29], placozoans [15], sponges [30] and, most recently, the ctenophores Mnemiopsis leidyi [31] and Pleurobrachia bachei (table 1). Non-metazoan unikonts lack not only the ligands, receptors and SMAD cofactors [17,[24][25][26], but also most of the inhibitors. This pathway is a clear example of a metazoan innovation [25], and the presence of all elements together in ctenophores suggests that this system was actively transducing extracellular signals into transcriptional responses in the ancestral metazoan.…”

Early metazoan life: divergence, environment and ecology

“…Alternatively, if sponges are a single clade, we cannot rely upon inferences about the morphology of these nodes to infer the morphological and developmental attributes of the most basal metazoans. Several recent studies suggest that sponges are likely to be monophyletic rather than paraphyletic [8,9]. Earlier studies indicated that resolving the phylogenetic position of ctenophores was complicated by considerable long-branch attraction [10], but more recent studies have attempt to resolve these difficulties and support a basal position for the clade [4,5,11], but have also been criticized [12,13].…”