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Chapter 31
Marine Collagens
of the three fibrillar collagen clades (A, B, and C) occurred before the eumetazoan
radiation. Interestingly, only the B clade fibrillar collagens preserved their character-
istic modular structure from sponge to human. This observation is compatible with
the suggested primordial function of type V/XI fibrillar collagens in the initiation of
the formation of the collagen fibrils.
In the 1970s through 1980s, academics and commercial researchers began to
use collagen as a biomaterial in a variety of connective tissue applications because
of its excellent biocompatibility; low antigenicity; high biodegradability; and good
mechanical, hemostatic, and cell-binding properties (Stenzel et al. 1974). Recently,
Uzel and Buechler (2009) make a link between biochemical parameters (amino acid
sequence) and the associated biologically relevant functional properties (elasticity,
stiffness, energy storage capacity) of collagen. The key insight reported in their work
is that the type of amino acid motif that defines the tropocollagen molecule has
significant effects on its mechanical properties. Therefore, it can be hypothesized
that diversity of collagen polyforms determined the futures of their function, even
within the same organism.
The relative complexity of the marine invertebrate collagens and the difficulty
in their purification and characterization has hindered continued progress in their
research. However, there are more than enough examples for inspiring materials
scientists, practically in each order of marine invertebrates. Thus, here I will try to
represent and discuss the most spectacular events that are useful for biomimetic and
materials science, starting with sponges as the lowest marine invertebrates.
Fig. 31.1 AFM images: nanotopography of C. reniformis collagen fibers (a, b, c) (images courtesy
Sascha Heinemann)
The anthozoan collagens differ from other invertebrate collagens in the propor-
tions of hydroxylated proline and lysine, the total of basic amino acids, and the lower
total of imino acids (Young 1971) These differences may be true of all coelenterate
collagens if the studies of Piez and Gross (1959) on the float of the siphonophore
Physalia and of Chapman (1973) on the mesoglea of the hydroid Corynactis are
representative of other coelenterate groups.
The axial skeletal rod of Veretillum cynomorium was the subject of an exten-
sive study by Franc et al. (1974). These authors demonstrated that the organic
phase of this calcified structure is at least partly collagenous in structure, as earlier
X-ray diffraction studies (Marks et al. 1949) had shown for two other pennatulid
species.
Ultrastructural investigations of the fibrillar matrix showed that although some
banded fibrils were present, the most abundant fibril type only rarely showed a
transverse banding and therefore could not be unequivocally identified with the
physicochemically identified collagen. However, the collagenous nature of these
fibrils has since been confirmed by negative staining, which reveals a distinct band-
ing in isolated fibrils, and by electron diffraction of frozen hydrated fibrils, which
gives a diffraction pattern comparable to that of vertebrate collagen. The axial rod of
Veretillum is the only authenticated example of a collagenous matrix calcified with
calcite, as fibrillar collagen previously thought to be present in sponge and echino-
derm skeletons (Travis et al. 1967) was undoubtedly extraskeletal in origin (Ledger
and Jones 1977; Wilbur 1976). The axis is thus of immediate interest as a naturally
occurring contrast to the collagen–hydroxyapatite association typical of vertebrate
mineralized tissues (Ledger and Franc 1978).
Octocoral axes are composed of a limited number of structural elements.
Principally they contain variable amounts of flexible collagen fibers, embedded in
a pliant, proteinaceous matrix, and minerals that exist in a variety of crystal forms
and aggregate shapes (Kingsley and Watabe 1984).
Usually the major component of the axial skeleton of gorgonians (Coelencerata:
Octocorallia) is the gorgonin, composed mainly of collagen fibers in a proteina-
ceous matrix (Leversee 1969). The protein matrix is largely uncharacterized, but the
collagen, though modified, (Goldberg 1974) is characterized as collagen (see also
Chapter 14).
Unlike vertebrate osseous tissues that consist of hydroxyapatite and collagen,
collagen has not been associated with the formation of invertebrate calcium car-
bonate structures. However, decalcification of the calcareous spicules from the
gorgonian Leptogorgia virgulata reveals an organic matrix that may be divided
into water insoluble and soluble fractions. As reported by Kingsley et al. (1990),
the insoluble fraction displays characteristics typical of collagen, which is an
unusual component of an invertebrate calcium carbonate structure. This matrix
fraction exhibits a collagenous amino acid profile and behavior upon SDS-PAGE.
Furthermore, the reducible cross-link, dihydroxylysinonorleucine (DHLNL), is
detected in this fraction. The composition of the matrix varies seasonally; i.e., the
collagenous composition is most prevalent in the summer. These results indicate
that the insoluble matrix is a dynamic structure.
432 31 Marine Collagens
Of course, it very hard to believe that there are some correlations between coe-
lenterates collagen and climate changes, but in the case of giant jellyfish species
Nemopilema nomurai, it is true (Pauly et al. 2009; Purcell et al. 2007). According
to excellent review recently published by Richardson et al. (2009), human-induced
stresses of overfishing, eutrophication, climate change, translocation, and habitat
modification appear to be promoting jellyfish (pelagic cnidarian and ctenophore)
blooms to the detriment of other marine organisms. Mounting evidence suggests
that the structure of pelagic ecosystems can change rapidly from one that is dom-
inated by fish (that keep jellyfish in check through competition or predation) to
a less desirable gelatinous state, with lasting ecological, economic, and social
consequences.
Jellyfish is a well-known source of collagen and especially of edible collagen.
Regardless of their size or shape, most jellyfish are very fragile and contain more
than 95% of water, with more than 40% of the dry weight of the edible jelly-
fish being collagen (Miura and Kimura 1985; Nagai et al. 1999). Edible jellyfish
comprise five to seven species, including Lobonema smithi, Lobonemoides gra-
cilis, Rhopilema esculentum, Stomolophus meleagris, and N. nomurai (Nishimoto
et al. 2008). A large portion of the body, called the umbrella, is composed of both
mesogloea and outer skin and the latter is separated into outer and inner membranes,
known as exumbrella and subumbrella, respectively (Nagai et al. 1999). Different
polymorphs of collagen can be isolated from exumbrella and subumbrella.
Jellyfishes have been eaten by humans since 300 AD in China, and about
425,000 tonnes/year are harvested globally (1996–2005) for human consumption
in Southeast Asia. Jellyfish fisheries exist in 15 countries, including China, India,
Indonesia, Japan, Malaysia, and the Philippines, with export industries in Australia
and the USA (Richardson et al. 2009).
The giant jellyfish N. nomurai is a large Scyphozoan that is capable of attaining
a bell diameter of up to 1.5 m (Fig. 31.2). It mainly inhabits the Bohai Sea, Yellow
Sea, and northern East China Sea and was only rarely reported in the Japanese
sea area during the twentieth century. However, each year between 2002 and 2007,
dense aggregations of this jellyfish have been reported in the seas surrounding Japan
(Honda et al. 2005, 2009; Honda and Watanabe 2007; Iizumi 2004). If consider-
able amounts of collagen were obtainable from such jellyfish, which can weigh
up to 200 kg, they would have potential as an important source for collagen and
development of this unutilized resource would follow.
Jellyfish processing is carried out as follows (Hsieh et al. 2001).
Fresh jellyfish readily spoil at ambient temperature. Therefore, processing of jel-
lyfish is carried out preferably within a few hours of capture, while the animals are
still alive. The body of jellyfish consists of a hemispherical transparent umbrella.
The mouth is on the undersurface of the umbrella and is protected by fused oral
arms, commonly known as “legs.” The umbrella and oral arms of jellyfish are sep-
arated immediately after catching. Jellyfish are cleaned with seawater, scraped to
remove mucus membranes and gonadal material. Both umbrella and oral arms are
used in processing. Traditional methods of processing involve a stepwise reduction
of the water content using salt (NaCl) and alum (AlK[SO4 ]2 ·12H2 O). A salt mix
31.2 Coelenterates Collagens 433
Fig. 31.2 The “living collagen bomb” Nemopilema nomurai (a, b) is a large jellyfish that is
capable of attaining a bell diameter of up to 1.5 m (c) (images courtesy Naoto Honda)
containing about 10% alum is used for initial salting of jellyfish, using about 1 kg
salt–alum mix for 8–10 kg of jellyfish. Salted jellyfish are then left in the brine
for 3–4 days, followed by several transfers to another container salted with a fresh
mix containing a smaller amount of alum. The salted jellyfish can then be heaped
and left to dry on a draining rack at room temperature for 2 days and the heap is
turned upside down several times during that period to allow excess water to drain
out through compression from its own weight. The entire process requires 20–40
days to produce a salted final product with 60–70% moisture and 16–25% salt. The
processed jellyfish has a yield of about 7–10% of the raw weight depending on the
species and processing formula.
Preservation of jellyfish in a mixture of salt and alum is necessary to obtain
products of desirable structure and texture. Alum reduces pH, acts as a disinfectant
and a hardening agent, giving and maintaining a firm texture by precipitating pro-
tein. Salt aids in reducing the water content and in keeping the product microbially
stable. Cured jellyfish has a special crunchy and crispy texture that makes it unique.
The salted jellyfish has a stable shelf life of up to 1 year at room temperature. The
shelf life can be increased to more than 2 years if the product is kept cool; how-
ever, freezing spoils the product, which dries out completely and becomes covered
with wrinkles (Hsieh et al. 2001). Numerous modern separation and purification
technologies for jellyfish collagen have also been recently reported (Jin 2008; Shen
et al. 2009).
Except use as a food, jellyfish collagen has been investigated for application in
tissue engineering. Thus, Song et al. (2006) reported on porous scaffolds composed
434 31 Marine Collagens
Among the invertebrates, the molluscs exhibit a wide evolutionary history and pos-
sess connective tissues typical of vertebrates, which define the shape of the body
(Bairati 1985). Different types of collagens were isolated and described from bivalve
molluscs (Mizuta et al. 2004, 2005) as well as from cephalopods (Bairati et al. 1989,
31.4 Echinoderm Collagens 435
1999; Mizuta et al. 1994a, 1994b, 2009; Nagai et al. 2001; Rigo and Bairati 1998,
2002; Shadwick 1985; Sivakumar and Chandrakasan 1998; Sivakumar et al. 2003).
The cephalopods have evolved along the same lines as that of the fast mov-
ing predatory aquatic vertebrates and share substantial structural similarities with
vertebrates, which include the development of a complex nervous system, a brain
protected by a cartilaginous case, and an image-perceiving eye. For these rea-
sons, the cephalopod connective tissue is ideal to understand collagen in relation
to structure–function and evolution (Sivakumar et al. 2003).
Different polymorphic collagen chains have been described for various repre-
sentatives of Cephalopoda. Thus, it was reported the presence of a heterotrimeric
collagen in cranial cartilage of the cuttlefish, Sepia officinalis, and its possible sim-
ilarity to vertebrate minor collagens (Sivakumar and Chandrakasan 1998). Very
unusual collagen was also isolated by Rigo and Bairati (2002) from the extracellular
matrix of S. officinalis cartilage.
Recently, two genetically distinct types of collagen have been identified in the
mantle muscle and skin of the common squid Todarodes pacificus by Mizuta and co-
workers (Mizuta et al. 2009). The major collagen type, based on quantity, has been
denoted Type SQ-I and accounts for about 90% of the total collagen in the common
squid. This collagen type shows properties similar to those of vertebrate Type I
collagen, while the relatively minor collagen type, denoted Type SQ-II, resembles
vertebrate Type V collagen in terms of solubility and chemical composition. Both
SQ-I and SQ-II were isolated from pepsin-solubilized collagen preparations and
found to possess heterotrimeric chain compositions, i.e., [α1(SQI)]2α2(SQ-I) and
[α1(SQ-II)]2α2(SQ-II), respectively.
In contrast to acid-based isolation of collagens from jellyfish (Nishimoto et al.
2008), the same procedure using cephalopods has been carried out with alkali
extraction. For example, the mantle muscles of five cephalopod species, T. pacificus,
Photololigo edulis, Sepioteuthis lessoniana, Sepia esculenta, and Sepia longipes,
were extracted with 0.1 M NaOH to prepare crude collagen fiber, called the “residue
after alkali extraction” (RS-AL) (Mizuta et al. 2009). The collagens showed a
similar tendency in solubility, which gradually increased depending on the treat-
ing temperature, and the values at 40–90◦ C were constantly less than 47% for all
the species examined. In addition, the collagens were estimated to denature in the
approximate temperature range of 37.5–42.5◦ C. These results suggest that the col-
lagens in RS-AL from these species may have relatively high resistance to hot water
extraction even after their denaturation.
coasts. Among them, over 20 species are edible (Saito et al. 2002). In general, the
body wall of uncooked sea cucumber that is utilized as a vinegared dish is very hard
to masticate. After cooking, however, it becomes as tender as jelly. The body wall of
Stichopus japonicus is enjoyed by people in Japan and China as a hors d’oeuvre or
a main dish, owing to its unique elasticity and palatability. S. japonicus has a strong
potential for commercial use, because it is easily obtainable, inexpensive, and easy
to cook.
The intestine of S. japonicus is also consumed as one of the fermented seafoods,
called konowata in Japanese. Moreover, the boiled-dried sea cucumber, called iriko
in Japanese, is produced as a preserved food. The major component of these edible
portions is a collagenous fiber (Bailey et al. 1982; Cui et al. 2007; Matsumura 1974),
but little is known about the chemical properties and subunit structure of the collagen
molecule because of its extreme insolubility. Features of the collagens isolation and
solubilization from such representatives of echinoderms as starfish Asterias amuren-
sis (Kimura et al. 1993) or purple sea urchin (Anthocidaris crassispina) test (Nagai
and Suzuki 2000) have also been reported.
The second direction that is related to materials properties of echinoderms
collagens is dominated by scientists from the USA and Europe.
Echinoderms have the ability to change the mechanical properties of their col-
lagen fibrillar networks in a way that is interfaced with their neural systems over
physiologically relevant timescales. As recently reviewed by Eppell et al. (2006), the
major difference between echinoderm collagen fibrils and other animals is therefore
at the systemic level (Thurmond and Trotter 1996; Trotter et al. 1994).
Sea cucumber fibrils are similar to those found in vertebrates having the same
length, assembling with the same repeat period, possessing the same gap/overlap
ratio (Trotter et al. 1994) and possessing the same cross-linking chemistry (Butler
et al. 1987). The habit of echinoderm fibrils is spindle shaped, rather than cylin-
drical as found in mammals. In addition, the collagen amino and carboxy termini
are arranged in a bipolar manner with the center of symmetry existing at the mid-
dle of the long axis of the spindle, rather than monopolar as found in mammals.
This spindle structure can also be obtained using mammalian collagen monomers
to reconstitute synthetic fibrils (Rainey et al. 2002). Clear evidence of proteogly-
cans utilized to aggregate echinoderm fibrils has been found, but these molecules
are all removed in the purification procedure used to obtain the fibrils we measured
(Graham et al. 2004). Thus, sea cucumber fibrils possess the characteristics typi-
cal of vertebrate collagen fibrils; therefore cucumber fibrils offer a suitable model
for the analysis of fibril properties which can be applied to higher ordered struc-
tures based on fibril subunits. Because of the specific structural features of a single
type I collagen fibril isolated from the sea cucumber, Cucumaria frondosa, it was
possible to carry out nanomeasurements with micro-devices as reported by Eppell
et al. (2006). They used the device to obtain the first stress–strain curve of an iso-
lated collagen fibril producing the modulus and some fatigue properties of this soft
nanofibril.
31.4 Echinoderm Collagens 437
31.5 Conclusion
To describe diversity as well as structural and biochemical peculiarities of marine
invertebrates collagens, I would need space for a separate book. Therefore, I perform
only brief analysis of selected examples listed above. Collagens of annelids origin or
those discovered in glass sponges are described in corresponding chapters as well.
Collagens are of interest for materials science, especially from biomechan-
ics point of view. The mechanical response of a biological material to applied
forces reflects deformation mechanisms occurring within a hierarchical architecture
extending over several distinct length scales. Characterizing and in turn predict-
ing the behavior of such a material requires an understanding of the mechanical
properties of the substructures within the hierarchy, the interaction between the sub-
structures, and the relative influence of each substructure on the overall behavior
(Eppell et al. 2006). Progress in development of highly sensitive methods like dif-
ferent nanoindentation techniques allow us today to use even individual collagen
fibrils isolated from marine invertebrates as models for the better understanding of
unique mechanisms of biomechanics.
Due to the ease at which disease spreads in the higher order animals, the biotech-
nological and biomimetical potential for marine invertebrates collagens is beyond
doubt.
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