Abstract

Animals (metazoans) include some of the most complex living organisms on Earth, with regard to their multicellularity, numbers of differentiated cell types, and lifecycles. The metazoan extracellular matrix (ECM) is well-known to have major roles in the development of tissues during embryogenesis and in maintaining homoeostasis throughout life, yet insight into the ECM proteins which may have contributed to the transition from unicellular eukaryotes to multicellular animals remains sparse. Recent phylogenetic studies place either ctenophores or poriferans as the closest modern relatives of the earliest emerging metazoans. Here, we review the literature and representative genomic and transcriptomic databases for evidence of ECM and ECM-affiliated components known to be conserved in bilaterians, that are also present in ctenophores and/or poriferans. Whereas an extensive set of related proteins are identifiable in poriferans, there is a strikingly lack of conservation in ctenophores. From this perspective, much remains to be learnt about the composition of ctenophore mesoglea. The principal ECM-related proteins conserved between ctenophores, poriferans, and bilaterians include collagen IV, laminin-like proteins, thrombospondin superfamily members, integrins, membrane-associated proteoglycans, and tissue transglutaminase. These are candidates for a putative ancestral ECM that may have contributed to the emergence of the metazoans.

Introduction

Some of the most fascinating and mysterious steps in the evolution of life on earth involve the debut of multicellular organisms from single-celled ancestors. Modern multicellular lifeforms are present in both the bacterial and eukaryotic domains of life and there is evidence that multicellularity has emerged independently multiple times [1–5]. For eukaryotes, particularly the Metazoa (animals), the transition from unicellularity to multicellularity is complex to consider because ancestral forms are either not represented in the fossil record, or are extremely rare and difficult to identify. Genome and transcriptome sequencing projects offer new routes to consider these evolutionary transitions more systematically. For example, an analysis of genomic data from many modern prokaryotes to identify commonalities in protein-coding sequences allowed inference of the possible repertoire of proteins in a last common ancestral cell [6].

In considering central attributes of multicellular organisms, the evolution of stable mechanisms for organised cell-to-cell attachments is a key requirement of multicellularity. The most complex modern multicellular organisms, including between 3 and approximately 122 different cell types, are found among the Metazoa [5]. The single-celled eukaryotes most closely related to animals are the choanoflagellates [7] and filastereans such as Capsaspora owczarzaki [8,9]. From comparative studies of the transcriptomes and predicted proteomes of these protists, it has been deduced that the origin of metazoans probably involved the functional adaptation of pre-existing gene products, for example new or adapted roles of integrin and cadherin receptors, both of which have been identified in certain unicellular eukaryotes [10,11], as well as genetic rearrangement events that led to the origin of new types of gene products with novel functional capacities for cell interactions and intercellular communications [12].

A central mediator of metazoan multicellularity is the extracellular matrix (ECM), a structured extracellular network of collagens, glycoproteins, proteoglycans, and associated carbohydrates such as glycosaminoglycans. The secreted proteins that build the ECM appear to fall within the novel category of metazoan gene products, because many ECM proteins are highly conserved throughout animals and yet are not represented in choanoflagellates or filastereans [13,14]. Williams et al. [13] established that three species of these protists express distinct sets of predicted secreted proteins (identified by presence of an N-terminal secretory signal peptide and no transmembrane domain), none of which have a domain composition equivalent to a metazoan ECM protein, although individual domains common in ECM proteins are present. Specific examples are the separate domains of fibrillar collagens [15] or thrombospondins [16]. These data suggest that gene rearrangement and domain shuffling had an important role in the emergence of the large, multidomain, secreted proteins that characterise the metazoan ECM. In modern metazoans, the secretion and extracellular assembly of structural proteins of the ECM depends on many ECM-affiliated proteins, both intracellular and extracellular: for example, to effect post-translational modifications, proteolytic processing, or interactions with non-structural and matricellular proteins within the ECM [17,18]. Thus, consideration of the phylogeny of these affiliated proteins is also relevant to constructing models for the evolution of metazoan ECM.

The distinct domain architectures of secreted proteins of choanoflagellates and metazoans suggest that additional insights into metazoan ECM evolution could be ascertained from careful comparative analysis of ECM and affiliated proteins encoded in modern species from the earliest diverging metazoan phyla. By analogy with the analysis of a prokaryotic ancestral cell [6], proteins in common between extant species in the earliest diverging phyla would be candidates for membership of ‘ancestral ECM’. Of the early diverging metazoan phyla (Ctenophora (comb jellies), Porifera (sponges), Placozoa, and Cnidaria), cnidarians are, to date, by far the most-studied with regard to their ECM and cell-adhesion mechanisms. This relates to the lengthy history of Hydra as an experimental model [19], the phylogenetic position of cnidarians as the sister group to bilaterians, and the presence of a morphologically well-defined ECM, the mesoglea, that, in Hydra, can be isolated away from the cell layers of the body wall as an acellular structure and is thus suitable for biochemical study [20,21].

Knowledge of the ECM of the other early diverging phyla is much more sparse. Placozoa comprise an enigmatic phylum that to date includes only a few species and will not be considered further here [22]. A mesoglea between the epithelial cell layers is apparent in ctenophores, but information on its molecular composition is very limited (discussed further below). Sponges have biomineralised extracellular structures (spicules) embedded in a fibrillar meshwork, but most classes lack ECM as recognised morphologically in bilaterians. A limitation for the study of ctenophores and sponges until recent years has been a lack of laboratory model species or cell culture [23,24].

The limited knowledge is significant because both Porifera and Ctenophora are considered to be of earlier evolutionary origin than Cnidaria, as evidenced by the fossil record and molecular phylogeny reconstructions [25,26]. However, there remains considerable controversy over whether the sponges or the ctenophores are of earliest evolutionary origin, i.e., which phylum represents the sister group to all other animals. Historically, sponges were placed at the base of the animal evolutionary tree due to their simple morphological organisation, limited number of cell types, and the absence of recognisable nerve or muscle structures: both of the latter are present in ctenophores and cnidarians [27] (Figure 1A). With the expansion of molecular phylogenetics, several studies have surprisingly placed ctenophores as the sister group to all other animals (e.g. [28]) (Figure 1B), whereas others continue to support the traditional ‘poriferans-sister’ model (e.g. [29,30]). Genome sequencing of two species of ctenophores indicated major differences in the categories of encoded proteins in comparison with all other metazoans, with many proteins of bilaterians noted to be absent [31–,33]. Thus the ‘ctenophore first’ hypothesis remains under active discussion and investigation [34,35].

Ctenophores and Poriferans

Figure 1
Ctenophores and Poriferans

(A,B) Schematic evolutionary trees of the poriferan-first (A), or ctenophore-first (B), models of metazoan evolution. Choanoflagellates are included as the closest outgroup. (C) Morphology of a ctenophore, Pleurobrachia pileus. Internal organs are visible through the transparent mesoglea (asterisk). Key: mouth (mo); aboral neuro-sensory complex (nsc); comb rows (cr); tentacles (tcl); lateral branches of tentacles (tentillae), (tt); tentacle root (tr), and pharynx (ph). Scale bar: 1 cm (reproduced from [106] under CC-BY). (D) Schematic diagram of a ctenophore. Mesoglea is present within the tentacles and body wall (reproduced from [107] under CC-BY). (E) Morphology of a demosponge, Echinoclathria gibbosa (reproduced from [108] under CC-BY). (F) Diagram of the body wall and cell types of a sponge, (reproduced from [109] with automatic permission from Elsevier via STM Permissions). (G) Tree diagram of the four classes of extant sponges.

Figure 1
Ctenophores and Poriferans

(A,B) Schematic evolutionary trees of the poriferan-first (A), or ctenophore-first (B), models of metazoan evolution. Choanoflagellates are included as the closest outgroup. (C) Morphology of a ctenophore, Pleurobrachia pileus. Internal organs are visible through the transparent mesoglea (asterisk). Key: mouth (mo); aboral neuro-sensory complex (nsc); comb rows (cr); tentacles (tcl); lateral branches of tentacles (tentillae), (tt); tentacle root (tr), and pharynx (ph). Scale bar: 1 cm (reproduced from [106] under CC-BY). (D) Schematic diagram of a ctenophore. Mesoglea is present within the tentacles and body wall (reproduced from [107] under CC-BY). (E) Morphology of a demosponge, Echinoclathria gibbosa (reproduced from [108] under CC-BY). (F) Diagram of the body wall and cell types of a sponge, (reproduced from [109] with automatic permission from Elsevier via STM Permissions). (G) Tree diagram of the four classes of extant sponges.

The advent of genomic and transcriptomic sequencing projects for an increasing number of poriferan and ctenophore species has revolutionised the possibility to gain insight into ECM content in sponges and ctenophores, through analysis of the predicted proteomes of individual species. This article will review the published literature and discuss our findings from a recent detailed survey of public genomic and transcriptomic databases for ECM proteins in species representing three classes of sponges and three species of ctenophores.

Known components of ECM in ctenophores and poriferans

Ctenophores

The unique anatomy and ultrastructure of ctenophores has been studied by light and electron microscopy, with major interest in developmental processes, nerve and muscle tissues, and the specialised rows of locomotary ciliated combs (Figure 1C,D) [36,37]. Prey capture is carried out by specific colloblast cells on extensible tentacles (most species) or by direct engulfment (Beroe species, that lack tentacles) [28,38]. The mesoglea is typically described as transparent and jelly-like. From transmission electron microscopy studies of the tentacles of Euplokamis, the mesoglea was observed to contain networks of striated fibrils, interpreted as collagen fibrils, as well as muscle fibres, mesenchymal cells, and a network of nerve cells. Curious box-like, acellular, extracellular structures were also observed [39]. Later immunofluorescent staining studies of Pleurobrachia species or Beroe abyssicola also identified many cell types within the bodywall mesoglea, including networks of nerve cells, muscle, and other cell types [40–42]. Transmission electron microscopy has also provided views of a basement membrane-like layer that underlies ectodermal cells in Pleurobrachia bachei and B. ovata, but is not visible in Mnemiopsis leidyi [14]. There is very little direct knowledge of the composition of ctenophore mesoglea, but a phylogenetic study of the basement membrane proteoglycan, perlecan, concluded that perlecan is absent from M. leidyi [43]. Fidler et al. [14] detected collagen IV by immunohistochemistry as diffuse arrays in proximity to ectodermal cells in M. leidyi, and with more appearance of linear elements in Beroe and Pleurobrachia. Genomic and transcriptomic analyses identified many collagen IV paralogues, whereas small collagenous proteins (designated spongins from their initial identification in Porifera) were absent and a unique type of secreted protein, containing only a non-collagenous (NC) domain, was identified and designated NC1 protein [14].

Porifera

Adult sponges are sessile, vase-shaped animals with pores that filter water into the body cavity for food uptake by specialised choanocytes (Figure 1E) [44,45]. The body wall consists of an epithelial bilayer supported by mineralised spicules and a meshwork of extracellular fibrils termed the mesohyl (Figure 1F). Unlike ctenophores, overt cell–cell junctions are apparent between epithelial cells [46]. There are four extant classes of sponges (Figure 1G) and different classes have different processes of biomineralisation. In calcerous sponges, calcium carbonate-based spicules are assembled extracellularly through carbonic anhydrase activity and possibly in association with acidic extracellular proteins [47–49]. In siliceous sponges, silicon dioxide spicules are templated through intracellular and extracellular processes involving (in many species) the polymerising enzyme, silicatein, and frequently with templating on to collagen fibres [50–52]. Silicateins are related to the cathepsin family of intracellular processing and degrading enzymes and are thought to have arisen in the sponge lineage through ancestral gene duplication and point mutation of cathepsin L [53]. Chitin has also been identified as a spicule-associated, possible template in demosponges, and a glass sponge [54,55].

By electron microscopy, class Homoscleromorpha is distinguished by the presence of a basement membrane structure [56,57]. Indeed, a collagen IV cloned from a homoscleromorph sponge was shown to have a basement membrane-like localisation [56]. In addition, sponges (along with various other invertebrates) encode short-chain spongins that contribute to 10 nm microfibrils within the mesohyl. Spongins comprise approximately 79–100 Gly-Xaa-Yaa triplets and 3 non-collagenous regions, with the C-terminal non-collagenous regions having homology and a proposed shared evolutionary origin with the NC1 domain of collagen IV [58,59]. Collagen fibril structures have been identified by ultrastructural criteria in several sponge species [60–62] and molecular cloning has led the recognition of a diversity of molecular forms of collagens of the fibrillar or interrupted-triple-helix types in addition to spongins ([63–65] and reviewed by [66]).

Species-specific, carbohydrate-based cell-to-cell adhesion mechanisms have also been characterised functionally and biochemically in sponges. Sulphated polysaccharides have major roles in species-specific cell-to-cell adhesion, in conjunction with proteins termed aggregation factor complex, spongican, or glyconectins [67–72]. These proteins can adopt unusual, ring-like conformations and appear to be specific to the demosponge lineage [73,74]. Other mechanisms may involve C-type lectins and a calcium-dependent lectin, clathrilectin [75,76], as well as self-association of carbohydrates [77]. Chemically, the sulphated polysaccharides appear very varied, with varying amounts of sulphated galactose, fucose, arabinose, or hexuronic acid identified across species [78]. Examination of the structures of the acid-labile carbohydrates of glyconectins from several species identified these to include heterogeneous sulphated oligosaccharides with variable amounts of fucose, arabinose, or py(4,6)Galacatose residues, and thus distinct from the repeated disaccharide units of bilaterian glycosaminoglycans [79].

With regards to other mechanisms of cell–ECM associations, integrin subunits have been cloned from several sponge species [80–82]. Integrin(s) have been implicated functionally in autograft fusion in Geodia cydonium [83] and the response of Microciona prolifera cells to depletion of extracellular sulphate [84]. The identification of vinculin in Oscarella pearsei and the localisation of this protein to cell–cell and cell–ECM contact sites further supports that poriferan integrins are likely to function in adhesion and cell signaling, as in bilaterians [85]. Dystroglycan-like proteins with possible laminin-binding capacity have been recognised in several sponges in addition to the dystroglycans of cnidarians and bilaterians [86].

Insights from genomics and transcriptomics: a structured survey of ECM proteins encoded in poriferans and ctenophores

The sequencing of the genome of the demosponge Amphimedon queenslandica expanded the view on candidate ECM proteins of sponges. Analysis of the predicted proteins indicated that, even in the absence of overt basement membrane-like structures, laminin-like proteins are encoded [87,88]. Since 2010, transcriptomes for sponges of other classes and genomes and transcriptomes for several species of ctenophores have been published [32,33,89,90].

To obtain a wider view of ECM and ECM-associated proteins in ctenophores and poriferans, we surveyed sponge and ctenophore genome- and/or transcriptome-predicted proteins for selected ECM and ECM-affiliated proteins. The ECM proteins chosen for study are highly conserved in invertebrate and vertebrate bilaterians [91,92] and have known functional roles in the fibrils and meshworks of the ECM. A range of collagens were included as search tools to assist identification of possible disparate forms. Major glycoprotein and proteoglycan receptors that tether ECM proteins at cell surfaces and extracellular proteases important for ECM dynamics in bilaterians were also included (Figure 2A), along with intracellular proteins that are important for procollagen assembly, processing, and collagen fibril formation (Figure 2B) [93], or for the post-translational assembly of the core tetrasaccharide linker for glycosaminoglycan substitution on proteoglycan core proteins [94] (Figure 2C). Spongin and silicatein are not present in vertebrates but were included because of their known importance in poriferan ECM. The suite of 41 proteins analysed is listed in Supplementary Table S1. The sponges species included represent the classes Demospongiae (the most abundant in terms of species), Homoscleromorpha and Calcerea and the three species of ctenophores have sequenced genomes and/or a large transcriptome dataset.

The cell–ECM adhesion proteins included in our genomic and transcriptomic surveys

Figure 2
The cell–ECM adhesion proteins included in our genomic and transcriptomic surveys

(A) Schematic diagram of molecular processes involved in cell–ECM adhesion. (B) The major enzymes involved in procollagen processing and collagen fibril assembly. (C) The enzymes involved in O-linkage of the core tetrasaccharide for glycosaminoglycan addition.

Figure 2
The cell–ECM adhesion proteins included in our genomic and transcriptomic surveys

(A) Schematic diagram of molecular processes involved in cell–ECM adhesion. (B) The major enzymes involved in procollagen processing and collagen fibril assembly. (C) The enzymes involved in O-linkage of the core tetrasaccharide for glycosaminoglycan addition.

From initial BLASTP or TBLASTN searches, protein sequences of highest homology (determined by evalue <1e-30 and extensive % coverage of the query sequence) were compiled and validated by best-reciprocal Basic Local Alignment Search Tool (BLAST) search. Sequences passing this step were subjected to additional quality control analysis for secretory signal peptides, transmembrane domains, overall domain architecture and, where relevant, enzyme active site. The results obtained are summarised in Tables 1 and 2, respectively. The underlying data are presented in Supplementary Tables S2–S8.

Table 1

The ECM-related proteins conserved with bilaterians identified from the ctenophore species studied

ECM/ECM-affiliated protein Accession numbers of homologues identified in Ctenophore species 
 M. leidyi P. bachei H. californensis 
ADAMTS 
Agrin 
β-1,4-galactosyltransferase 1 
β-1,4-galactosyltransferase 2 
Bone morphogenetic protein 1 ML31401a PB3463711 GGLO01058316.1 
Bifunctional heparan sulphate N-deacetylase/N-sulphotransferase 
Collagen I 
Collagen IV ML034334a
ML034337a
ML18175a
ML17501a
ML034336a
ML18198a
ML16441a
ML25069a
ML18197a
ML18176a
ML17504a
ML17502a
ML034335a 
PB3460513
PB3460485
PB3479585
PB3460474
PB3479630 
GGLO01050633.1
GGLO01050605.1
GGLO01033148.1
GGLO01027773.1
GGLO01030859.1
GGLO01027525.1
GGLO01030860.1
GGLO01014639.1
GGLO01023628.1
GGLO01020933.1
GGLO01020934.1 
Collagen VI 
Collagen X 
Collagen XIV 
Collagen XVIII 
Collagen XXIII 
Collagen XXV 
Dystroglycan 
Fibrillin 
Fibulin 
Glucuronyl-transferase ML271519a ML073039a PB3467704 GGLO01045111.1 
Glypican ML14244a PB3464484 GGLO01048445.1 
Heparan sulphate 2-O-sulphotransferase 
Hsp47 (SERPINH1) 
Integrin α ML09514a
ML463513a
ML30811a
ML27362a 
PB3464239 GGLO01029506.1
GGLO01029505.1
GGLO01050007.1
GGLO01050010.1 
Integrin β ML068314a ML073028a ML04042a ML05098a PB3461633
PB3460305
PB3465728
PB3460908 
GGLO01026249.1
GGLO01070288.1 
Laminin α ML097515a GGLO01023715.1 
Laminin β GGLO01023769.1 
Laminin γ ML05951a ML035910a PB3460962
PB3479626 
GGLO01031685.1 
Lysyl hydroxylase 
Lysyl oxidase 
Matrix metalloproteinase ML030215a GGLO01044249.1 
Nidogen 
Perlecan 
Procollagen C-proteinase enhancer 
Prolyl 4-hydroxylase GFAT01094412.1, ML257632 PB3469803 (p) GGLO01022174 
Silicatein ML017310a
ML005020a
ML10109a
ML007332a 
PB3466562
PB3465824 
GGLO01072762.1
GGLO01008148.1
GGLO01041937.1
GGLO01007610.1+ 
SPARC 
Spongin 
Syndecan PB12832424 
Thrombospondin superfamily ML34222a PB11599022 (p) GGLO01050054(p) 
Tissue transglutaminase 2 ML03126a PB 3462531 GGLO01036061 
Xylosyl transferase 
ECM/ECM-affiliated protein Accession numbers of homologues identified in Ctenophore species 
 M. leidyi P. bachei H. californensis 
ADAMTS 
Agrin 
β-1,4-galactosyltransferase 1 
β-1,4-galactosyltransferase 2 
Bone morphogenetic protein 1 ML31401a PB3463711 GGLO01058316.1 
Bifunctional heparan sulphate N-deacetylase/N-sulphotransferase 
Collagen I 
Collagen IV ML034334a
ML034337a
ML18175a
ML17501a
ML034336a
ML18198a
ML16441a
ML25069a
ML18197a
ML18176a
ML17504a
ML17502a
ML034335a 
PB3460513
PB3460485
PB3479585
PB3460474
PB3479630 
GGLO01050633.1
GGLO01050605.1
GGLO01033148.1
GGLO01027773.1
GGLO01030859.1
GGLO01027525.1
GGLO01030860.1
GGLO01014639.1
GGLO01023628.1
GGLO01020933.1
GGLO01020934.1 
Collagen VI 
Collagen X 
Collagen XIV 
Collagen XVIII 
Collagen XXIII 
Collagen XXV 
Dystroglycan 
Fibrillin 
Fibulin 
Glucuronyl-transferase ML271519a ML073039a PB3467704 GGLO01045111.1 
Glypican ML14244a PB3464484 GGLO01048445.1 
Heparan sulphate 2-O-sulphotransferase 
Hsp47 (SERPINH1) 
Integrin α ML09514a
ML463513a
ML30811a
ML27362a 
PB3464239 GGLO01029506.1
GGLO01029505.1
GGLO01050007.1
GGLO01050010.1 
Integrin β ML068314a ML073028a ML04042a ML05098a PB3461633
PB3460305
PB3465728
PB3460908 
GGLO01026249.1
GGLO01070288.1 
Laminin α ML097515a GGLO01023715.1 
Laminin β GGLO01023769.1 
Laminin γ ML05951a ML035910a PB3460962
PB3479626 
GGLO01031685.1 
Lysyl hydroxylase 
Lysyl oxidase 
Matrix metalloproteinase ML030215a GGLO01044249.1 
Nidogen 
Perlecan 
Procollagen C-proteinase enhancer 
Prolyl 4-hydroxylase GFAT01094412.1, ML257632 PB3469803 (p) GGLO01022174 
Silicatein ML017310a
ML005020a
ML10109a
ML007332a 
PB3466562
PB3465824 
GGLO01072762.1
GGLO01008148.1
GGLO01041937.1
GGLO01007610.1+ 
SPARC 
Spongin 
Syndecan PB12832424 
Thrombospondin superfamily ML34222a PB11599022 (p) GGLO01050054(p) 
Tissue transglutaminase 2 ML03126a PB 3462531 GGLO01036061 
Xylosyl transferase 

Homologues of ECM and affiliated proteins of bilaterians identified in three species of ctenophores. Accession numbers are from M. leidyi genome browser [32], P. bachei transcriptome at Neurobase [33], and GenBank transcriptome shotgun assembly (TSA) for the H. californensis transcriptome [110].

Underlying BLAST results are reported in Supplementary Tables S2–S4.

Abbreviations: p, partial sequence. + BLASTP for silicatein in H. californiensis yielded >100 hits with many redundant sequences. Four top hits are included here.

Table 2

The ECM-related proteins conserved with bilaterians identified from the sponge species studied

ECM/ECM-affiliated protein Accession numbers of top homologues identified in poriferan species 
 O. carmella A. queenslandica L. complicata S. ciliatum 
ADAMTS g302.t1, g3943.t1, g5893.t1 XP_011406035.1 lcpid17910, lcgid3864
lcpid26189,lcgid1420
lcpid16435,lcgid3864
lcpid14744,lcgid48263
lcpid8832,lcgid1429 
scpid8465, scgid0298 scpid14367, scgid31153
scpid11730, scgid3308
scpid7699, scgid3308 scpid11197, scgid3308 
Agrin 
β-1,4-galactosyltransferase 1 g6154.t1
g11091.t1 
XP_003383478.3 lcpid72445, lcgid57516
lcpid108583, lcgid4190 
scpid62588, scgid16118
scpid83531, scgid23687 
β-1,4-galactosyltransferase 2 g11091 XP_003383478.3 lcpid72445, lcgid57516 scpid83531 
Bone morphogenetic protein 1 g3280.t1 XP_003387878.1 lcpid53711 scpid73058 
Bifunctional heparan sulphate N-deacetylase/N-sulphotransferase g9342.t1 XP_019854532.1 lcpid25736, lcgid12663
lcpid35336, lcgid53985
lcpid65133, lcgid5933 lcpid44097, lcgid5933 
scpid22021, scgid1378
scpid11705, scgid14663
scpid24542, scgid2276
scpid19876, scgid2276 scpid27630, scgid5678 
Fibrillar collagen-like g11085.t1
g426.t1
g10272.t1 
XP_003388783.2
XP_011405131.1
XP_011405304.1
XP_019864450.1 
lcpid17276, lcgid40511, lcpid13783, lcgid6124 scpid13476, scgid0358
scpid12346, scgid28066,
scpid10799, scgid31760, scpid12114, scgid35048 
Collagen IV g1079.t1
g10977.t1 
lcpid52947, lcgid75348
lcpid4786, lcgid64311
lcpid13694, lcgid38464
lcpid16924, lcgid10403 
scpid10989, scgid8635 scpid11320, scgid9595 scpid8958, scgid15448 
Dystroglycan g5213.t1 scpid43419, scgid4112 scpid78051, scgid4112 
Fibrillin g2667.t1
g3633.t1 
XP_019850772.1
XP_019859670 
lcpid4195, lcgid79342 scpid6157, scgid20153 
Fibulin 
Glypican g1352.t1 XP_003386976.1 XP_019852741.1 lcpid67857, lcgid45685
lcpid32714, lcgid59020 
Glucuronyl-transferase g2277.t1 XP_019851580.1
XP_019851583.1 
lcpid40065, lcgid0547 scpid33216, scgid11109 
Heparan sulphate 2-O-sulphotransferase g2593.t1 lcpid67263, lcgid13423 scpid75685, scgid31021
scpid39942, scgid12865 
Integrin α g1989.t1
g9424.t1
g551.t1
 
XP_019848674.1
XP_019864024.1
XP_019864028.1
XP_019855406.1
XP_019855408.1
XP_019856433.1
XP_019850770.1 
lcpid14662, lcgid5141
lcpid30951, lcgid20056
lcpid24895, lcgid25747
lcpid28736, scgid0236
lcpid24944, lcgid0796
lcpid38700, lcgid0796
lcpid25998, lcgid57014
lcpid29144, lcgid59731
lcpid53986, lcgid5141 
scpid27434, scgid16145
scpid34588, scgid4727
scpid23074, scgid2395
scpid12646, scgid0799
scpid27708, scgid2395
scpid23633, scgid1153
scpid26968, scgid0799
scpid13516, scgid3686
scpid25262, scgid3686
scpid47429, scgid3686
scpid17601, scgid24595
scpid19223, cgid26959 
Integrin β g9310.t1
g9748.t1 
XP_011409775.1
XP_003388422.1
XP_019851540.1
XP_019864033.1
XP_011403560.2
XP_011404206.1 
lcpid40636, lcgid16859
lcpid44623, lcgid59216
lcpid32340, lcgid73219
lcpid170227, lcgid60939 
scpid4557, scgid16671
scpid20168, scgid21580
scpid4556, scgid3103
scpid38528, scgid18306
scpid22880, scgid21705
scpid49462, scgid3434
scpid22880, scgid21705
scpid41506, scgid3434
scpid47976, scgid3144
scpid29534, scgid3083
scpid19946, scgid33446
scpid27672, scgid3144 
Laminin α g7319.t1 XP_019852585.1 lcpid6587, lcgid43813 scpid4187, scgid33329 
Laminin β XP_019854276.1
XP_019849782.1 
lcpid31379, lcgid51207 scpid4527, scgid23872 
Laminin γ g7968.t1
g4177.t1 
XP_019855647.1 lcpid13654, lcgid40757 scpid4187, scgid33329 
Lysyl hydroxylase g1142.t1 XP_019854114.1 lcpid37848, lcgid5516 scpid32678, scgid32033 
Lysyl oxidase g7137.t1 XP_003387025.1 lcpid22308, lcgid72170 lcpid23110, lcgid74733 scpid30388, scgid0815 scpid36618, cgid24646 scpid31988, scgid0815 
Matrix metalloproteinase 
Nidogen 
Perlecan 
Procollagen C-proteinase enhancer 
Prolyl 4-hydroxylase g1383.t1 XP_003383442.1 lcpid38875,lcgid64402 scpid58888|scgid3871
scpid40070, scgid33742 
Silicatein g4492.t1 g6175.t1 g6176.t1 XP_003383103.1 lcpid104541, lcgid12146
lcpid113056, lcgid19166 
scpid95074, scgid11171
scpid63063, scgid35043 
SPARC g4839.t1 lcpid126889, lcgid36337, lcpid74779, lcgid64875 
Spongin g1095.t1
g988.t1
g2075.t1
g3758.t1 
XP_011405650.1 
Syndecan lcpid156268, lcgid70156 
Thrombospondin superfamily m162353a/g.162353 XP_011406237.1 lcpid9057a, lcpid8282, lcpid36553 scpid30246, scpid2291a, scpid12552 
Tissue transglutaminase 2 XP_019853849.1 
Xylosyl transferase g25200.t1 XP_011404143.1 lcpid41679, lcgid69457 scpid26149, scgid20327 
ECM/ECM-affiliated protein Accession numbers of top homologues identified in poriferan species 
 O. carmella A. queenslandica L. complicata S. ciliatum 
ADAMTS g302.t1, g3943.t1, g5893.t1 XP_011406035.1 lcpid17910, lcgid3864
lcpid26189,lcgid1420
lcpid16435,lcgid3864
lcpid14744,lcgid48263
lcpid8832,lcgid1429 
scpid8465, scgid0298 scpid14367, scgid31153
scpid11730, scgid3308
scpid7699, scgid3308 scpid11197, scgid3308 
Agrin 
β-1,4-galactosyltransferase 1 g6154.t1
g11091.t1 
XP_003383478.3 lcpid72445, lcgid57516
lcpid108583, lcgid4190 
scpid62588, scgid16118
scpid83531, scgid23687 
β-1,4-galactosyltransferase 2 g11091 XP_003383478.3 lcpid72445, lcgid57516 scpid83531 
Bone morphogenetic protein 1 g3280.t1 XP_003387878.1 lcpid53711 scpid73058 
Bifunctional heparan sulphate N-deacetylase/N-sulphotransferase g9342.t1 XP_019854532.1 lcpid25736, lcgid12663
lcpid35336, lcgid53985
lcpid65133, lcgid5933 lcpid44097, lcgid5933 
scpid22021, scgid1378
scpid11705, scgid14663
scpid24542, scgid2276
scpid19876, scgid2276 scpid27630, scgid5678 
Fibrillar collagen-like g11085.t1
g426.t1
g10272.t1 
XP_003388783.2
XP_011405131.1
XP_011405304.1
XP_019864450.1 
lcpid17276, lcgid40511, lcpid13783, lcgid6124 scpid13476, scgid0358
scpid12346, scgid28066,
scpid10799, scgid31760, scpid12114, scgid35048 
Collagen IV g1079.t1
g10977.t1 
lcpid52947, lcgid75348
lcpid4786, lcgid64311
lcpid13694, lcgid38464
lcpid16924, lcgid10403 
scpid10989, scgid8635 scpid11320, scgid9595 scpid8958, scgid15448 
Dystroglycan g5213.t1 scpid43419, scgid4112 scpid78051, scgid4112 
Fibrillin g2667.t1
g3633.t1 
XP_019850772.1
XP_019859670 
lcpid4195, lcgid79342 scpid6157, scgid20153 
Fibulin 
Glypican g1352.t1 XP_003386976.1 XP_019852741.1 lcpid67857, lcgid45685
lcpid32714, lcgid59020 
Glucuronyl-transferase g2277.t1 XP_019851580.1
XP_019851583.1 
lcpid40065, lcgid0547 scpid33216, scgid11109 
Heparan sulphate 2-O-sulphotransferase g2593.t1 lcpid67263, lcgid13423 scpid75685, scgid31021
scpid39942, scgid12865 
Integrin α g1989.t1
g9424.t1
g551.t1
 
XP_019848674.1
XP_019864024.1
XP_019864028.1
XP_019855406.1
XP_019855408.1
XP_019856433.1
XP_019850770.1 
lcpid14662, lcgid5141
lcpid30951, lcgid20056
lcpid24895, lcgid25747
lcpid28736, scgid0236
lcpid24944, lcgid0796
lcpid38700, lcgid0796
lcpid25998, lcgid57014
lcpid29144, lcgid59731
lcpid53986, lcgid5141 
scpid27434, scgid16145
scpid34588, scgid4727
scpid23074, scgid2395
scpid12646, scgid0799
scpid27708, scgid2395
scpid23633, scgid1153
scpid26968, scgid0799
scpid13516, scgid3686
scpid25262, scgid3686
scpid47429, scgid3686
scpid17601, scgid24595
scpid19223, cgid26959 
Integrin β g9310.t1
g9748.t1 
XP_011409775.1
XP_003388422.1
XP_019851540.1
XP_019864033.1
XP_011403560.2
XP_011404206.1 
lcpid40636, lcgid16859
lcpid44623, lcgid59216
lcpid32340, lcgid73219
lcpid170227, lcgid60939 
scpid4557, scgid16671
scpid20168, scgid21580
scpid4556, scgid3103
scpid38528, scgid18306
scpid22880, scgid21705
scpid49462, scgid3434
scpid22880, scgid21705
scpid41506, scgid3434
scpid47976, scgid3144
scpid29534, scgid3083
scpid19946, scgid33446
scpid27672, scgid3144 
Laminin α g7319.t1 XP_019852585.1 lcpid6587, lcgid43813 scpid4187, scgid33329 
Laminin β XP_019854276.1
XP_019849782.1 
lcpid31379, lcgid51207 scpid4527, scgid23872 
Laminin γ g7968.t1
g4177.t1 
XP_019855647.1 lcpid13654, lcgid40757 scpid4187, scgid33329 
Lysyl hydroxylase g1142.t1 XP_019854114.1 lcpid37848, lcgid5516 scpid32678, scgid32033 
Lysyl oxidase g7137.t1 XP_003387025.1 lcpid22308, lcgid72170 lcpid23110, lcgid74733 scpid30388, scgid0815 scpid36618, cgid24646 scpid31988, scgid0815 
Matrix metalloproteinase 
Nidogen 
Perlecan 
Procollagen C-proteinase enhancer 
Prolyl 4-hydroxylase g1383.t1 XP_003383442.1 lcpid38875,lcgid64402 scpid58888|scgid3871
scpid40070, scgid33742 
Silicatein g4492.t1 g6175.t1 g6176.t1 XP_003383103.1 lcpid104541, lcgid12146
lcpid113056, lcgid19166 
scpid95074, scgid11171
scpid63063, scgid35043 
SPARC g4839.t1 lcpid126889, lcgid36337, lcpid74779, lcgid64875 
Spongin g1095.t1
g988.t1
g2075.t1
g3758.t1 
XP_011405650.1 
Syndecan lcpid156268, lcgid70156 
Thrombospondin superfamily m162353a/g.162353 XP_011406237.1 lcpid9057a, lcpid8282, lcpid36553 scpid30246, scpid2291a, scpid12552 
Tissue transglutaminase 2 XP_019853849.1 
Xylosyl transferase g25200.t1 XP_011404143.1 lcpid41679, lcgid69457 scpid26149, scgid20327 

Homologues of ECM and affiliated proteins of bilaterians identified in four species of poriferans. Accession numbers are from genomes and transcriptome-predicted proteins of O. carmela, S. ciliatum, and L. complicata [89] at Compagen [90], and GenBank entries of the A. queenslandica genome and transcriptome projects [87,88]. Apart from collagen IV-like collagens and spongins, the various collagens identified have been grouped as fibrillar-like collagens. Underlying BLAST results and validations are reported in Supplementary Tables S5-S8. Abbreviation: SPARC, small protein acidic and rich in cysteine.

Collectively, the data demonstrate dramatic differences in the profile of conserved proteins in ctenophores versus poriferans (Figure 3 and Tables 1 and 2). Many more proteins in common with bilaterian ECM are encoded in poriferans than in ctenophores. Nevertheless, the ctenophore list does include a repertoire for a basic cell–ECM adhesion system: cell-surface receptors, ECM proteins, a cross-linking enzyme, and a potential ECM-proteolytic enzyme (Figure 3). The proteins identified in ctenophores were for the most part present in all three species, with the exception of syndecan, identified only in P. bachei, and potential matrix metalloproteases, identified in M. leidyi and H. californensis. In agreement with Fidler et al. [14], many collagen IV-like paralogues were identified. Post-translational modifications of proline and lysine residues contribute to the stability of collagen triple helices in vertebrates, however only prolyl-4-hydroxylase and not pro-collagen lysine dioxygenase (lysine hydroxylase) was identified in these ctenophores (Table 1 and Figure 3). The encoding of multiple integrin α and β subunits (Table 1) indicates potential for diverse specificities of integrin-mediated cell adhesion, perhaps in line with the relatively large number of cell types now documented in ctenophores [95]. Silicatein-like proteins were identified in all three species; however, given the recognised general divergence of protein sequences in ctenophores [32,33], in-depth studies will be needed to determine the relationship of these to the cathepsin family (Table 1).

ECM and ECM-affiliated proteins of poriferans and ctenophores that are conserved with bilaterians, as identified by our survey

Figure 3
ECM and ECM-affiliated proteins of poriferans and ctenophores that are conserved with bilaterians, as identified by our survey

The Venn diagram includes all categories of proteins that were identified in at least one of the species studied. See Tables 1 and 2 and Supplementary Tables for details of the protein identifications.

Figure 3
ECM and ECM-affiliated proteins of poriferans and ctenophores that are conserved with bilaterians, as identified by our survey

The Venn diagram includes all categories of proteins that were identified in at least one of the species studied. See Tables 1 and 2 and Supplementary Tables for details of the protein identifications.

We examined the laminin-like proteins in more detail in view of the early evolution of collagen IV [14] and the central role of laminin in basement membrane assembly in bilaterians [96]. With the caveat that some of the identified sequences are incomplete, the laminin subunits identified present a complex picture. Although all are large proteins with many of the characteristic domains of laminins, many variations in domain organisation are apparent, including atypical domains such as thrombospondin or fibronectin III domains. Overall, the laminin proteins of sponges are more similar to those of bilaterians, yet distinctions between β and γ subunits are blurred at both the sequence and domain levels. Notably, the laminin N-domain is lacking from (apparently full-length) ctenophore proteins and two α-like subunits but no β- or γ-like subunits were identified in P. bachei (Figure 4). The numbers of α-like and β/γ-like subunits varied among species and the α-like subunits included at most three laminin-G domains. Biochemical experiments will be needed to determine if these proteins are capable of forming stable heterotrimers and undergoing extracellular polymerisation or integrin-binding. For the ctenophore proteins, it is of interest whether heteromers including two different α subunits can be assembled.

Domain architectures of the laminin-like proteins identified in the species studied

Figure 4
Domain architectures of the laminin-like proteins identified in the species studied

Domains were identified in InterProScan 5. Representative examples of human laminin α, β, and γ chains are shown at the top. The number of amino acids is given in small font at the C-terminus of each protein. Dashed lines indicate incomplete sequence. Accession numbers are given on the right-hand side, see Tables 1 and 2 for details. The IV-B domain (in coral) is specific to the β subunit. Abbreviations: EGF, epidermal growth factor-like domain, with numbers referring to the number of repeated domains; FNIII, fibronectin type III domain; G, laminin G domain; GFR, growth factor-cysteine-rich domain; IV, laminin domain IV (in blue); N, laminin N-terminal domain; SP, signal peptide; TSR, thrombospondin type 1 domain. The G domain is structurally related to the Concanavalin A domain (Con A), which was identified in some sequences. Not to scale.

Figure 4
Domain architectures of the laminin-like proteins identified in the species studied

Domains were identified in InterProScan 5. Representative examples of human laminin α, β, and γ chains are shown at the top. The number of amino acids is given in small font at the C-terminus of each protein. Dashed lines indicate incomplete sequence. Accession numbers are given on the right-hand side, see Tables 1 and 2 for details. The IV-B domain (in coral) is specific to the β subunit. Abbreviations: EGF, epidermal growth factor-like domain, with numbers referring to the number of repeated domains; FNIII, fibronectin type III domain; G, laminin G domain; GFR, growth factor-cysteine-rich domain; IV, laminin domain IV (in blue); N, laminin N-terminal domain; SP, signal peptide; TSR, thrombospondin type 1 domain. The G domain is structurally related to the Concanavalin A domain (Con A), which was identified in some sequences. Not to scale.

We also examined the tissue transglutaminase (TGM) 2 (TGM2)-like proteins. In vertebrates, TGM2 has major roles in cross-linking fibrillin or fibronectin molecules into extracellular fibrils via redox-dependent processes [97,98]. The TGM-like proteins identified in the ctenophores and A. queenslandica sponge each include all the major domains of TGM2 but have only 30–35% sequence identity to human TGM2. However, at the active site of TTG2, the identity is 65–80% and the cysteine residue is completely conserved (Figure 5A). Molecular models of the active site region for four of the sequences, constructed against secondary structure alignments of four TGM2 structures from Protein Database (4KTY_B, 1G0D_A, 1LM9_A, and 2Q3Z_A), are presented overlaid with the structure of human TGM2 (4PYG) that was not used for modelling (Figure 5B,C). The models demonstrate that residues around the active site cysteine align very well with the known structure (Figure 5B), as do the highly conserved residues at the active site (Figure 5C). We predict that the ctenophore and sponge proteins should be active TGMs.

Molecular modelling of the active sites of the predicted tissue TGMs identified in Ctenophores and a Sponge

Figure 5
Molecular modelling of the active sites of the predicted tissue TGMs identified in Ctenophores and a Sponge

(A) CLUSTAL sequence alignment of the active site of human TGM2 (Hs) with the homologous regions of the identified ctenophore (Ml, M. leidyi; Pb, P. bachei, and poriferan (Aq, A. queenslandica) TGMs. See Tables 1 and 2 for full accession numbers. (B) Structure of the active site of 4PYG.pdb (human TGM2) [97]. The helix is highlighted in yellow as orientation for the overlay models in (C). (C) Models were prepared by HHPRED and MODELLER [111] and are shown as Aq (pink), ML03126a (green), ML25826a (salmon), and Pb3462531 (silver) overlaid with the crystal structure of human TGM2 from 4PYG.pdb, (black, with the catalytic cysteine (C277) labelled). The overlays show high conservation of the side chains of residues within a 6-Angstrom radius around the catalytic cysteine.

Figure 5
Molecular modelling of the active sites of the predicted tissue TGMs identified in Ctenophores and a Sponge

(A) CLUSTAL sequence alignment of the active site of human TGM2 (Hs) with the homologous regions of the identified ctenophore (Ml, M. leidyi; Pb, P. bachei, and poriferan (Aq, A. queenslandica) TGMs. See Tables 1 and 2 for full accession numbers. (B) Structure of the active site of 4PYG.pdb (human TGM2) [97]. The helix is highlighted in yellow as orientation for the overlay models in (C). (C) Models were prepared by HHPRED and MODELLER [111] and are shown as Aq (pink), ML03126a (green), ML25826a (salmon), and Pb3462531 (silver) overlaid with the crystal structure of human TGM2 from 4PYG.pdb, (black, with the catalytic cysteine (C277) labelled). The overlays show high conservation of the side chains of residues within a 6-Angstrom radius around the catalytic cysteine.

ECM-related proteins not found in the ctenophores raise other intriguing questions about the biochemical nature of ctenophore mesoglea. It was previously noted that core proteins of secreted proteoglycans of bilaterians are not conserved in early diverging metazoans [20,91]. However, carbohydrate has been reported as <1% of dry weight of ctenophores [99].

With the exception of glucuronyl-transferase, homologues of the bilaterian enzymes for addition of the core O-linked saccharides (Figure 2C), are not identifiable (Table 1 and Figure 3). Whether this pathway mechanism evolved later or has been lost through lineage-specific gene losses in ctenophores is unclear. With regard to ECM structure, no fibrillar-like collagens were identified and the collagen cross-linking enzyme lysyl oxidase was also absent, raising questions over the nature of observed striated fibrils in ctenophore mesoglea [39]. However, bone morphogenetic protein 1 (BMP1), which cleaves the C-propeptide of fibrillar procollagen [100] (Figure 2B), was present. In bilaterians, BMP1 has many other substrates including a laminin γ chain [100] and it may be expected that the ctenophore protein can target other substrates. In agreement with [14], spongin was not identified.

In contrast, poriferans were confirmed to encode a wider repertoire of ECM proteins including fibrillar-like collagens of various domain architectures and fibrillin, as well as small protein acidic and rich in cysteine (SPARC) and one or more thrombospondin superfamily members (see [16] for details of the thrombospondin superfamily). Collagen IV proteins were apparent in the calcerous sponges as well as (as expected) in the homoscleromorph sponge. The encoding of lysyl oxidase is in agreement with the detection of striated collagen fibrils in sponges [60–62]. Notwithstanding the unusual carbohydrate structures reported in sponges (see section above), the suite of carbohydrate-addition enzymes encoded indicate potential for addition of the O-linked core tetrasaccharide of glycosaminoglycans (Table 2 and Figure 3). Other aspects of ECM in common with bilaterian ECM include the encoding of A Disintegrin and Metalloproteinase with Thrombospondin motifs (ADAMTS) proteases and a wider repertoire of cell–ECM attachment receptor types, including membrane-bound proteoglycan core proteins, dystroglycan, and integrin subunits. Spongins were identified in A. queenslandica and O. carmela, but not in the calcerous sponges. Silecateins were identified as expected in the demosponge A. queenslandica and also in the other species examined (Table 2).

Perspective

Current laboratory experiments and analyses of genome-predicted proteins indicate that ctenophore ECM has a very different protein composition to other metazoans. This cannot be interpreted as a result of the early phylogenetic emergence of this phylum because poriferans, traditionally considered the earliest diverging metazoans, are found to have an array of ECM and ECM-affiliated proteins that is clearly closer to the conserved repertoire of cnidarians and bilaterians. The difference in ECM might be considered an indication that ctenophores evolved prior to poriferans, in which case the limited set of proteins conserved between ctenophores, poriferans and bilaterians can be taken to represent a prototypic ‘toolkit’ for a minimal metazoan ECM [101]. The combination of collagen IV, laminin-like proteins, and thrombospondin superfamily members is of great interest, as the concept of coordinated function of these three proteins within ECM has received little consideration.

However, other factors also need to be taken into consideration. There are estimated to be approximately 5000 species of extant poriferans, yet only approximately 150 known species of ctenophores. This may reflect that the deep-sea lifestyle of many ctenophores makes it difficult to identify the true number of species, or alternatively could indicate very different evolutionary histories of poriferans and ctenophores. Sponges and ctenophores evolved when oxygen levels on Earth were far lower than at present [102]. Indeed, members of both phyla lack hypoxia-inducible factor α (HIF) indicating that oxygen availability does not drive gene expression through the HIF pathway as in cnidarians and bilaterians [103]. In a ‘poriferan-first’ evolutionary scenario, the limited repertoire of known ECM proteins in ctenophores would represent secondary gene losses, leading to a proposal of a relatively complex ECM in the metazoan ancestor. Many ctenophores live in the deep sea and the environment of low oxygen and sparse food sources [102,104], and high hydrostatic pressure may have driven selection for a unique form of ECM. Clearly, the anatomy of ctenophores does include a mesoglea and, to date, to our knowledge, an unbiased study of ctenophore mesoglea by proteomic methods has not been carried out. Only through this type of approach with a clear view of ctenophore mesoglea composition be gained. A limitation of focusing on the ECM proteins conserved with bilaterians is that possible ctenophore- or poriferan-specific ECM proteins remain undisclosed. As discussed by others, it is very likely that a considerable ‘hidden biology’ of ctenophores and poriferans remains to be discovered [105]. Nevertheless, the positive identification of certain ECM proteins conserved between these early emerging phyla and other metazoans increases the precision of models for an ancestral metazoan ECM.

Summary

  • Ctenophores and poriferans have distinct sets of ECM-related proteins in comparison with the most highly conserved ECM and ECM-affiliated proteins of bilaterians.

  • In particular, ctenophores lack many of the structural ECM proteins and enzymes for addition of the core O-linked tetrasaccharide that is characteristic of bilaterian glycosaminoglycan substitutions.

  • Proteomic studies are needed to gain more comprehensive views of the composition of ECM in ctenophores and poriferans.

  • The very limited set of conserved ECM and ECM-affiliated proteins in ctenophores may represent a minimal toolkit that reflects the earliest emerging form of metazoan ECM. Given the current controversies over the relative phylogenetic placements of ctenophores and poriferans it cannot be excluded that this apparent simplicity may result from secondary gene losses that are specific to the evolution of the ctenophore lineage.

Competing Interests

The authors declare that there are no competing interests associated with the manuscript.

Abbreviations

     
  • BMP1

    bone morphogenetic protein 1

  •  
  • ECM

    extracellular matrix

  •  
  • HIF

    hypoxia-inducible factor

  •  
  • TGM

    transglutaminase

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Supplementary data