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1. Introduction

Humanity has been using marine biomaterials since ancient times (i.e., molluscan shells, corals, bath sponges skeletons, byssus threads), but reaching an industrial level today has become real thanks to the rapid development of various kinds of processing technologies and maricultures. Often, there is a possibility of the utilization of fish, molluscs, or marine arthropod processing products in order to use them most efficiently and not only for feed production. Due to the absence of possible human pathogens in marine biomaterials, a number of them (i.e., collagen, gelatin, keratin) have become an alternative source of long and well-established biopolymers in medicine and cosmetics. Today, modern scaffolding strategies [1,2,3] for tissue engineering are based on the application of diverse already naturally pre-fabricated 3D skeletal constructs of marine invertebrates origin [4]. Sources of marine biomaterials are still plentiful [5] in spite of partial overfishing, dramatic climate changes, and the increasing pollution of the world’s oceans with industrial waste. An attempt to classify marine biomaterials by their origin is presented by us in Figure 1.

Due to the huge amount of scientific information available in various scientific sources, we considered carrying out its analysis to be expedient, choosing certain topics that include marine polysaccharides of invertebrates and algal origin, marine structural proteins (spongin, collagen, gelatin, keratin, conchiolin) as well as marine biominerals from corals and molluscan shells. For the first time, in order to facilitate the perception of large volumes of information and focus on especially important parameters characterizing a particular biomaterial, we took the liberty of presenting a part of information in the form of so-called “Biomaterial passports” (see Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7, Table 8, Table 9, Table 10, Table 11, Table 12 and Table 13). This form includes scientific name, chemical formula, molecular weight, physicochemical and material properties, extraction methods, market and patent situation of corresponding biological materials discussed in this article. For brevity, some aspects will only be briefly discussed, but interested readers are referred to pertinent references.

This review has the ambitious goal to provide a thorough and comprehensive coverage of marine biomaterials as multifaceted topic. Consequently, we strongly believe that numerous open questions raised in this review will inspire a younger generation of experts in marine biology, biochemistry, bioengineering, biomimetics, bioinspired materials science, biomineralization, marine waste processing, fishery and mariculture to research marine biomaterials as examples of renewable natural sources which stood the test of time through evolutionary development of corresponding organisms. 2. Marine Polysaccharides

Polysaccharides belong to biological materials with carbohydrate backbone-based structures. In this review, we focus attention only on structural aminopolysaccharide chitin and selected polysaccharides of algal origin. Chitosan, an artificially produced derivate of chitin, was not the goal of our analytical research exclusively due to the existence of numerous reviews related to this biopolymer (i.e., [6,7,8,9,10,11]).

2.1. Chitin

The main characteristics of chitin are summarized in Table 1.

2.2. Recent Studies in Crustacean Chitin Applications

Crustaceans (lobster, crab and krill) chitin [48,49] including chitin-based cuticles of more than 300 million tons of Antarctic krill present in the world ocean [50], remains the main industrial source of this structural biopolymer.

Importantly, crustacean shells combined with commercial chitin can be used as biosorbents to remove heavy metals from surface runoff that solves two environmental problems: the use of seafood wastes and water resources management [51]. Moreover, seafood wastes can be employed in agriculture: the use of shrimp chitin as feed additives showed a positive effect on growth and carcass characteristics of broiler chickens [52]. Another application of crustacean shells was shown in a recent research of Las Heras et al. [53] who described the generation of chitin-containing sponge like scaffolds, which were biocompatible with human mesenchymal stromal cells (hMSCs), thus representing a high potential for biomedical technologies, in particular, for tissue engineering. Likewise, novel interesting scaffolds-candidates for tissue engineering were designed from crab shells chitin and silk protein fibroin obtained from silkworm Antheraea pernyi cocoons [41]. Finally, nanomaterials from shrimp chitin (nanocrystals and nanofibers) were reported to have no cytotoxic effect, which was tested with epithelial-like and fibroblast-like cell lines [54]: this research indicates that such components can be safely used in biomedical industry.

2.3. Poriferan Chitin: Progress in the APPLICATion of Poriferan Chitinous Scaffolds

The presence of chitin in marine sponges has been revealed only recently [55,56] that was further confirmed by the detection of chitin in fossilized skeleton of 505 MYR old demosponge Vauxia gracilents [39]. Since then, chitin has been isolated from numerous species of marine [25,43,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69] as well as fresh-water sponges [70].

Over the last decade, 3D chitinous scaffolds of poriferan origin were reported to have a huge potential for biomedical applications due to ability of corresponding sponges to grow under marine farming conditions [71]. Indeed, being biocompatible and supporting cell adhesion, growth, and proliferation, these scaffolds serve as perfect ready-to-use 3D matrices for tissue engineering and regenerative medicine [3,4,43,72,73,74]. For example, hMSCs seeded onto Aplysina aerophoba [61], A. fulva [1], and Ianthella basta [62] chitinous scaffolds displayed good attachment, viability, proliferation, and the capability of differentiation into osteogenic (A. aerophoba, A. fulva), adipogenic (A. aerophoba, I. basta) and chondrogenic (A. aerophoba) lineages, provided that the growth media were supplemented with respective differentiation inducers. Furthermore, chitinous scaffolds from I. labyrinthus were applied for the cultivation of human induced pluripotent stem cell-derived cardiomyocytes (iPSC-CMs): the long-term study (20 days) demonstrated that the cells grown on investigated scaffolds formed contracting cell clusters indicating that I. labyrinthus chitin is a source of suitable matrices to conduct research on the regeneration of myocardial tissue [66]. Additionally, poriferan chitinous scaffolds can serve as templates for co-culture systems mimicking in vivo processes [1,6]. A recent study conducted by our group [75,76] explored the ability of hemocytes from Cornu aspersum snail to grow on chitinous scaffold of A. archeri, which resulted in the generation of a new calcium-layered biomimetic product.

In addition, the study of sponge chitinous scaffolds, i.e., scaffolds of Ianthella species, pointed to their elasticity and capillary effect that allows these unique matrices to assume the shape of the objects they were placed on and swell with liquids (i.e., blood), the properties, which can be used in wound treatment [35,66] (Figure 2). In addition, owing to their capillary effect, sponge chitinous scaffolds can be used as adsorbents of crude oil and synthetic dyes [35] as well as drug delivery systems, which was shown for a sponge scaffold adsorbing antimicrobial drug decamethoxine leading to the inhibition of Staphylococcus aureus pathogene [68]. Another important application of sponge chitinous scaffolds lies in waste water treatment, as was shown for the case of A. aerophoba adsorbing uranium [77].

Intriguingly, sponge chitinous scaffolds serve as a source of inspiration for biomimetic research including the development of diverse composite materials using “extreme biomimetics route” [2,78,79]. Some sponges of Verongiida order were reported to carry unique biocomposites composed of amorphous silica, crystalline aragonite and chitin [74] that can be used as a «natural example» of chitin mineralization. Recently, a great progress in the application of sponge chitinous scaffolds as matrices for metal incorporation has been reported. For example, isolated chitinous skeleton of A. fulva demosponge was shown to undergo electrochemical deposition of copper following “sensibilization” employing silver nitrate solution [80,81]. Other examples include A. aerophoba scaffolds covered by ZrO2 [82] and Fe2O3 [83], the use of A. cauliformis as a template for the growth of GeO2 nanocrystals [84], and nanosilica depositions onto I. basta scaffolds [85]. All such treatments were conducted under hydrothermal conditions up to 185 °C. Such composites could be used for waste water treatment and photocatalytic decomposition of water to convert solar energy into chemical energy [81,86]. These findings are of a very high relevance to the current development in EV industry including the production of sensors, catalysts, electrochemical capacitors, the research focused on the latter also included I. basta chitinous scaffold to produce chitosan/sponge chitin membrane [87]. Finally, poriferan chitin-containing biocomposite materials demonstrated a potential for the adsorption of water pollutants, i.e., A. archeri scaffolds were used as a matrix for the immobilization of Trametes versicolor laccase that proved to efficiently remove tetracycline [69], while metallization of A. aerophoba scaffolds with silver nanoparticles and AgBr proved to be promising for water filtering systems with antibacterial properties [88].

Modern biocomposite-based scaffolding strategies include two key ways: to produce requested 3D constructs from corresponding precursors using technological tools or simply use naturally already pre-fabricated scaffolds if they originate from renewable sources. Such kind of 3D scaffolds remains to be one of the crucial features of skeletons of marine sponges that belong to the Verongiida order inhabiting oceans since the Precambrian [39].

Fabrication of biomimetic materials and scaffolds is usually a micro- or even nanoscale process. However, mostly all practical applications on the industrial level require larger-scale synthesis of nanoscale features. Recent development in micro-CT tomography and 3D printing not only bring us closer to the biomimicry of hierarchical 3D open cell hierarchical structures, but also clearly shows how nature is ahead of our most advanced technologies. Nevertheless, science still can benefit from the remarkable structural advancements of natural chitin-based scaffolds by simply applying them as multi-target templates in biomedicine and various modern technologies. 2.4. Polysaccharides of Algal Origin

Historically, the value of marine macroalgae (seaweeds) was greatly underestimated. Already in ancient Greece, Virgil and Horace, while referring to something completely worthless, used the term “villior alga” [89]. Seaweeds can be divided into green, red and brown algae containing a variety of polysaccharides [90,91], the properties of which were extensively studied during the last decade. Almost all representatives of brown algae are marine, mostly occurring in cold water, especially in the northern latitudes [92], and are rich in polysaccharides such as alginates (Table 2) and fucoidans (Table 3).

As represented below, alginates as biomaterials are widely applied in diverse biomedical fields. Being used as polymeric coating for therapeutic agents, so-called alginate microspheres can be applied for the delivery of different drugs [97,103,104,105,106,107,108,109,110] including tetracycline derivative minocycline [111] and vancomycin [112] antibiotics, lipopolysaccharide subunit antigen as vaccination therapy against Klebsiella pneumoniae [113], paracetamol [114], and anticancer drugs [115]. Additionally, alginates, in the form of hydrogels or composites, in particular, employing bioprinting [116,117,118,119,120,121], are widely employed in tissue engineering, such as tissue engineering of bone [122,123,124,125,126,127,128,129], cartilage [130,131], skin [132,133], muscle [134], and even neural tissue engineering [135] as well as cardiac regeneration [136]. Recently, alginates were reported to be widely researched for wound healing applications [137,138,139,140,141,142,143].

Similar to alginates, fucoidans proved to be valuable in tissue engineering [155,156,157,158,159], drug delivery [160,161,162,163], and wound healing [164,165,166].

Apart from brown seaweeds, read and green algae also produce unique polysaccharides. Brief information on carrageenans, extracted from red algae, is presented in Table 4.

Having viscosity increasing, stabilizing and gelling properties, carrageenans are widely used for controlled drug release, pharmaceuticals, food and other industries [174,179]. In addition, being biodegradable, these polysaccharides can be applied as films for food packaging: in order to increase their mechanical properties, nano-sized fillers such as melanin nanoparticles are employed as reinforcing agents [180]. Finally, carrageenans exhibit anticoagulant [181,182], antithrombotic [183], anti-HIV [151], antiviral [184,185,186], anti-cancer [187], immunomodulatory [177,188,189], and antioxidant [150,177,190] activities.

Green seaweeds, on the other hand, are abundant in ulvans (see Table 5).

Biocompatibility of ulvans, shown in in vitro cell culture assays, enables their use in wound treatment [191,201] and as substrates for cell cultivation [202]. Like other algal polysaccharides with gelling properties, ulvans can be employed for drug delivery [203,204]. Furthermore, ulvans are used for the synthesis of silver nanoparticles, the antimicrobial activity of which are essential for cosmetic and biomedical industries [205]. Iduronic acid, another rare sugar component of ulvans, is reported to have anti-thrombotic activities [206]. Finally, similar to alginates and carrageenans, ulvans are used to produce films as biodegradable material for food packaging, antioxidant, optical, thermal, and mechanical characteristics of which can be modified [207].

Selected marine algae, belonging to the phylum Rhodophyta (red algae), have been recognized as renewable sources of such polysaccharides as agar (agar-agar) (see Table 6), agarose and agaropectin. Numerous methods of agar extraction from such algae species as Gelidium, Acanthopeltis, Ceramium, Gracilaria, and Gloiopeltis have been reported [208].

Nowadays, both agar and agarose represent marine biomaterials with a high potential of their application in biomedicine and tissue engineering [213,214,217]. According to the modern view, “agarose is particularly used as a temporary scaffold for bony cells and growth factors in the field of tissue engineering, as a biocompatible substrate enriched with osteoconductive particles for bone grafting/augmentation procedures, and as a bone spacer in guided tissue regeneration“ [219]. Self-gelling properties and adjustable mechanical stability [220,221] of agarose gels are crucial for their use. For example, non-toxic [222] and biodegradable agarose gels have been effectively used in implantation surgery [219], wound healing, cartilage [223], cardiac, bone and nervous system [224], and regeneration as well as skin tissue engineering [225,226]. These directions are based on tunable features of agarose, which can result in adjustable characteristics similar to native tissues [225]. In addition, applications of this biomaterial for targeted drug delivery have been recently discussed in the review entitled “Agarose-based biomaterials for advanced drug delivery” [227]. Finally, agarose gels can be used in 3D bioprinting [228].

3. Marine Structural Proteins

According to a modern definition, “a structural protein is a protein that possesses a characteristic amino acid sequence or motif that repeats and forms a skeleton or contributes to the mechanical properties of a living organism, cell, or material” [229]. Typical examples of such proteins include actin, tubulin, collagen, elastin, sericin, fibroin, byssus, spongin, conchiolon, resilin, gorgonin, and keratin (see for overview [4,230]). A few selected structural proteins of marine origin are discussed below.

3.1. Spongin

Despite the fact that spongin (Table 7) has been studied by scientists since 1705, its true nature remains unknown and this biological material itself is attributed to one of the last mysteries of water-insoluble structural proteins that arose more than 800 million years ago, at the dawn of multicellular organisms [231,232]. The identification of spongin requires an extraordinary approach and is a challenging task that diverse research groups have failed to solve during 315 years of investigations. The low solubility of natural spongin in acids as well as after enzymatic treatments mentioned earlier [232] is a critical factor limiting its clear identification as collagen, or keratin, or a glycosylated form of one of them.

Spongin represents the biopolymers with high resistance to chemically harsh and thermally extreme conditions and is one of the main players as specialized templates for extreme biomimetics (Figure 3). Nowadays, it is very important to design a bridge between extreme biomimetics and bioinspired materials science where the basic principle is to exploit chemically and thermally stable, renewable biopolymers for the development of the next generation of biologically inspired composite materials never reported, or even suggested before, with sizes and properties which will allow their application in the extremes of modern industry including a large scale level. Recent studies have revealed that especially such renewable structural biopolymers as aminopolysaccharide chitin and proteinaceous spongin can be used as thermostable biopolymeric scaffolds with 3D architecture for the nucleation and growth of a wide range of novel nanoorganized SiO2-, GeO2- Fe2O3-, ZnO-, ZrO2-, TiO2, MnO2, and multiphased TiO2/ZrO2-based composites (see, for an overview, [2,3,79,86]).

In particular, using an extreme biomimetic approach, the spongin scaffold of Hippospongia communis was coated with TiO2 and such new biocomposite could efficiently remove C.I. Basic Blue 9 via adsorption and photocatalysis [237]. Secondly, the application of H. communis scaffold as a template for hydrothermal synthesis of hematite (α-Fe2O3) resulted in the generation of a composite consisting of spongin and hematite, which was shown to enhance the electrochemical properties of the capacitor electrode [241]. Thirdly, the same template was reported to undergo extreme biomimetic treatment yielding a novel MnO2-spongin composite that can be employed for the development of 3D metal oxide layered biocomposites functioning as electrodes [242]. Furthermore, due to their structure composed of 3D fibrous network and to spongin perfect sorption properties, spongin scaffolds serve as excellent matrices for enzyme immobilization. Indeed, H. communis were studied as a template for the immobilization of Candida antarctica lipase B (CALB). Astonishingly, such a biocatalytic system proved to be efficient even after 20 days of storage at 4 °C: immobilized lipase catalyzed the conversion of triglycerides to glycerol and fatty acid methyl esters that is very promising for bio-fuel industry and further research focused on spongin matrix enzyme immobilization [239]. Indeed, a follow-up study using H. communis scaffold showed a successful immobilization of laccase from Trametes versicolor mushroom, which efficiently catalyzed degradation of bisphenols, toxic compounds used in polycarbonates manufacturing [243]. The removal of contaminants, i.e., phenol, chlorophenol, fluorophenol, bisphenol A was also shown in the study that exploited the properties of another biocomposite composed of H. communis spongin and iron phthalocyanine [244]. In addition, H. communis was used to construct 3D carbonized spongin-Cu/Cu2O scaffold that was reported to catalyze the conversion of a toxic compound, 4-nitrophenol to 4-aminophenol [86]. Recently, spongin-based scaffolds isolated from Haliclona sp. marine demosponge have been successfully used for preconcentration and extraction of such substances as fenitrotion [245] and ketamine [245].

3.2. Collagens

The most important features of marine collagens are described in Table 8.

3.2.1. Marine Invertebrates Collagen

Recently, the biocompatibility and cell responses to marine invertebrate collagens have been reported in different studies. For example, employing murine fibroblast cells, biocompatibility of cryogels composed of jellyfish collagen, chitosan, and fucoidan was demonstrated [159]. Poriferan collagenous scaffolds, on the other hand, represent natural 3D scaffolds with a great potential for tissue engineering [263]. In particular, in vitro experiments using primary murine osteoblasts demonstrated a good cell attachment and proliferation when cultured on sponge collagenous scaffolds [269]. A series of experiments revealed a positive effect of sponge collagen hydrolysates on damaged or photoaged skin [270]. In addition, a recent in vivo study using rats demonstrated biocompatibility and the ability to support bone formation of biocomposites generated from collagen, isolated from A. fulva, and biosilicate [271]. Finally, powdered collagenous sponge scaffold loaded with L-cysteine hydrochlorid proved to cause a positive effect on wound healing [272].

Intriguingly, sponge collagen served as a template in several scientific projects aiming at the generation of bioinspired silica layered composite biomaterials [261] that resemble naturally occurring poriferan biocomposites [273,274]. For example, in laboratory conditions, collagen of different origin, i.e., isolated from Chondrosia reniformis marine demosponge, underwent in vitro silicification resembling the growth of siliceous spicules in glass sponges, which is promising for the generation of new collagen-silica hybrid materials on industrial scale [260,275]. Moreover, a specific amino acid motif, Gly-3Hyp-4Hyp, was discovered within the glass rope sponge Hyalonema sieboldi collagen, which presumably is predisposed for silica precipitation [276]. Thus, the modification of collagen amino acid sequence might significantly improve the construction of siliceous spicules layered biocomposites.

3.2.2. Marine Vertebrates Collagen

Both fishery and mariculture of selected fish species represent important sources of collagens (see for overview [254]). Marine fish collagen-based biomaterials (i.e., collagen gels, scaffolds, sponges, films, membranes, and composites) have a wide range of applications including drug delivery, wound healing, wound dressing, tissue engineering, i.e., bone, cartilage, dental, vascular and skin tissues, and therapeutics against skin aging, diabetes, and obesity [256,262,277,278].

The use of marine wastes including by-products of industrial plants, such as fish skin, scales and fins, as a source of fish collagen helps to fight environmental pollution and serves as a strategy to valorize marine resources [254,279]. Intriguingly, it is possible to isolate fish collagen from skin of marine Eel fish [280], codfish [281,282,283], European hake [284], smooth wolf herring [267], blue shark [285,286], small-spotted catshark [253], salmon [266,283], ocellate puffer fish, seaweed pipefish, brownstripe red snapper, brownbanded bamboo shark, carp, largefin longbarbel catfish, Japanese sea-bass, bigeye snapper, surf smelt, brown backed toadfish, Nile perch, skate, blacktip shark [255,256], bones of European hake [284], carp, Japanese sea-bass, skipjack, ayu, yellow sea bream, horse mackerel, Baltic cod [255], swim bladder of Atlantic cod [287], cartilages of brownbanded bamboo shark, blacktip shark, scales of carp, tilapia, spotted golden goatfish, grey mullet, rohu, and catla [255,256].

The application of fish collagen as biomaterial in biomedicine including tissue engineering has been thoroughly studied. Indeed, using cell culture assays, it was shown that 3D printed fish collagen/alginate scaffolds proved to be biocompatible with human MSCs [280]:

  • 3D printed scaffolds consisting of fish collagen/alginate and phlorotannin (as a bioactive component) displayed good biocompatibility and stimulated osteogenic differentiation of osteoblast-like MG63 cells [288];

  • 3D printed fish collagen/alginate hydrogels containing murine fibroblasts were of good biocompatible characteristics [285];

  • fish collagen was reported to be biocompatible with human fibroblasts [282];

  • 3D printed scaffolds composed of fish collagen and calcium phosphates derived from two sharks, blue shark and shortfin mako shark, were biocompatible with osteoblast-like Saos-2 cells [286];

  • composite scaffolds from fish collagen and chitosan promoted osteogenic and chondrogenic differentiation of rat MSCs [266];

  • fish collagen composites cross-linked by genipin under CO2 atmosphere were biocompatible with murine chondrocytes [253].

Fish collagen is also employed in dentistry, usually as membranes and bone graft materials [257,269]. Furthermore, this structural protein is used for controlled drug release including antimicrobial agents such as tetracycline [270]. In another research, a potential of anticancer drug(s) loaded 3D printed patches from fish gelatin for anticancer treatment was demonstrated [271]. Due to its excellent absorption properties and the ability to resorb up to 56 days, fish collagen can be used to control wound blood bleeding [272]. In addition, it has a high potential for cosmetic applications: fish collagen demonstrated a moisturizing effect without irritating skin [263].

3.3. Gelatin

Gelatin (Table 9) can serve as cell carrier to repair tissue defects, i.e., gelatin extracted from marine snail Rapana venosa was reported as a biocompatible template for the growth of human keratinocytes [289]. Hence, this marine biomaterial can be used in tissue engineering, often in combination with other materials such as chitosan and silk fibroin [42]. Indeed, chitosan/gelatin and silk fibroin/gelatin composites were employed in hepatocytes research and can be applied to generate 3D hepatic microenvironments, which would shed more light on hepatic cell functions [290]. Importantly, marine gelatin can be used in the inhibition of angiotensin-converting enzyme in order to lower blood pressure and reduce the risks of myocardial infarction, congestive heart failure, stroke, and arteriosclerosis [291]. Amino acid sequences of peptides inhibiting angiotensin-converting enzyme were detected in the studies on gelatin extracts of Alaska pollack [291] and can be further applied to prevent hypertension.

Moreover, due to its gel-forming properties, marine gelatin is also applied in food industry as a stabilizer, texturizer, thickener and foaming agent in yoghurt, ice-cream, jam, cream cheese, marshmallows, etc. [303,304]. Presumably, due to the lower content of proline and hydroxyproline in comparison to beef- and pork-derived gelatins [294,305], marine gelatins form “weaker gels” [306,307]. Notably, gelatin inhibits peroxidation preventing food from deterioration and functions as an outer protective film against dehydration, oxygen, and light [304]. In addition, isinglass, a high-grade gelatin derived from fish swim bladders that can induce aggregation of yeast and other insoluble particles, can be widely applied as a commercial clarifier in beverages, i.e., wine, beer, cider [303]. Though marine gelatin may trigger allergy, i.e., 0%–8% incidence depending on local food habits and fish consumption is reported [304]. Finally, marine gelatin is widely used in capsule industry. Usually, it is applied for the encapsulation of temperature-sensitive vitamins and other nutrients [308].

3.4. Keratin

Keratin (Table 10) is a fibrous protein of a high importance in the animal kingdom. Keratin presence in horn, hoofs, hair, beaks, shells, toenails, claws, fingernails, and feathers renders it the most abundant structural protein [309]. In such marine mammals as whales, keratin is to be found as the main structural component of baleen (see, for details, [230]). In general, keratin is present in two forms, characteristic for the type of tissue it is present in: α-keratin, found in soft tissues, e.g., wool, hair or skin, and β-keratin dominating in feathers, nails, fish scales, and other hard tissues. Structurally, both keratin types show a filament-type matrix structure. However, α-keratin filaments, denoted as intermediate filaments (IF), are two times greater in diameter (7–10 nm) compared to β-keratin filaments diameter of 3–4 nm. From the mechanical point of view, keratins have high strength and stiffness; the properties typical for the tissues keratin is a component of [310].

Though keratins seem to be constituents of static matrices (i.e., baleen) [310], there are exceptions to this rule such as hagfish. Hagfish (Myxinidae) are deep water inhabiting living fossils the body of which has an eel shape with no scales present. The remarkable feature of hagfishes is their ability to, when provoked or threatened, produce and excrete large amount of slime consisting of keratin IFs. The filaments act as threads binding mucin, a protein capable of forming gels [318]. When shot out of the slime gland followed by the contact with seawater, the slime becomes extremely dilute and is capable of effectively covering or choking the hagfish predator almost instantly. Detailed mechanical analysis of hagfish threads reveals their remarkable mechanical properties, different in dry state when compared to their wet state. In particular, dry hagfish threads show high initial stiffness of 3.6 GPa and a high tensile stress of 530 MPa while wet threads exhibit stiffness of 6 MPa and tensile strength of 180 MPa [317]. The outstanding mechanical properties of dry threads combined with the ease of their synthesis have been the reason for considering hagfish slime as a substrate for engineering fibers acting as a reinforcement for various modern composite materials [319].

Due to its poor solubility and tedious extraction methods, keratin has so far found limited applications; nonetheless, attempts were made to expand its usefulness. Initial studies on potential applications were focused on cells and their behavior on keratin containing films [320] and further extended on the potential of these films to act as active molecule carriers [321] or focused on altering their mechanical and antibacterial properties [322]. Keratin films have also been proposed for ocular surface reconstruction due to their good corneal biocompatibility and transparency [323].

3.5. Conchiolin and Conchixes of Molluscan Origin

To solve the problem of conchiolin insolubility, numerous hydrolysis protocols yielding soluble peptides of better functionality and applicability were developed: hydrolyzed conchiolin protein of pearl shell origin is a common cosmetic ingredient of hair and skin conditioning agents [324] or cleansing solutions [325]. More detailed studies on the properties and possible future applications of molluscan matrix protein extracts have been performed by Latire and co-workers [326]. In the first study, the authors analyzed shell extracts (acid soluble (AS), acid insoluble (AI) and water soluble (WS)) from the marine bivalve Pecten maximus [326]. AS did increase human fibroblast metabolic activity following 24 h of incubation. Likewise, the extracts obtained from mussel Mytilus edulis (AS and WS) and oyster Crassostrea gigas (AS) led to an increase in primary human skin fibroblast metabolic activity and cell proliferation [327]. Such data indicate the potential applications of these matrix proteins or their extracts in medicine, especially in wound healing or the treatment of various skin conditions. Indeed, in vivo study employing rats with dorsal skin wounds [328] demonstrated a progressive wound reduction after the ointment containing powdered shells of Megalobulimus lopesi was applied. This effect was attributed to calcium, which, after being administered to the wound tends to enhance the healing process [329,330], though the authors do not rule out the possibility of so-called conchix proteins to be involved in the facilitation of the healing process. Conchix, a term representing the shell organic matrix, has been recently proposed by Ehrlich and co-workers [331] to underline the importance of this organic piece of mollusc shell architecture. A brief summary on conchiolin properties is provided by Table 11.

The molecular complexity of the conchix hinders its applicability, especially in highly regulated industries, e.g., pharmacy. Dealing with this issue requires an intense focus on the isolation of active matrix components [337].

The optimistic conclusions resulting from the above-mentioned studies are challenged by the vast number of conchix active components which are extremely difficult to get rid of in order to isolate a single substance exhibiting biomedical or cosmetic potential. This fact is reflected in a small variety of products utilizing shell proteins as active components. 4. Marine Biominerals

Biominerals have been recognized as the main players in skeletogenesis of diverse organisms including those inhabiting seas. Being the products of vital activity of cells and specialized tissues, they are formed as the result of the interaction of organic matrices with various mineral phases regulated at the molecular and genetic level. Biosilica, calcium carbonates, and phosphates (mostly in marine vertebrates) represent the dominant mineral phases in a broad diversity of biocomposite-based skeletal constructs. In contrast to Ca-based biominerals discussed below, we paid no attention to highly sophisticated biosilica- based constructs of sponges origin [276,338,339,340,341,342] which represent diverse biomimetic models (Figure 4); however, they are not industrially harvested, or cultivated being mostly protected.

4.1. Corals

Corals (class Anthozoa) are marine invertebrates offering great opportunities for biomedical applications. “Coralline biomaterials” [343] (see also Table 12) have been well recognized in biomaterials science community (see, for an overview, [4,42,166]).

Coral skeletons are often used as the sources for inspiration to create artificial 3D constructs “with a 3D bioprinting platform which mimics morphological features of living coral tissue and the underlying skeleton with micron resolution, including their mechanical properties” [350]. The use of bioceramics of coral origin represents an attractive alternative to metal-based constructs [351] for implantology and tissue engineering [352]. Furthermore, the coral structure can undergo chemical conversions yielding calcium phosphate particles, which could be used in tissue engineering and as drug carriers: the conversion of Tubipora musica coral at 400 °C and 800 °C resulted in plate-like calcium phosphate nanoparticles (mostly Monetite) and spherical shaped calcium phosphate nanoparticles (whitelockite and hydroxyapatite), respectively [353]. Likewise, the scleractinian corals, Porites spp., were converted to hydroxyapatite employing hydrothermal and mechanochemical treatments [353]. Hence, the properties of coral skeletons inspire a whole range of studies focused on coral bone graft substitutes [354] as well on osseointegration with human bones [344,352,353,355,356,357]. Indeed, in vivo study demonstrated efficient bone formation at critical size defects in sheep bone using MSCs-covered scaffolds from Acropora coral [358]. Another research demonstrated that murine preadipocytes cultured on coralline skeletal material obtained from Porites lutea corals differentiated into osteoblasts [359]. In addition, positive effect has been obtained with respect to activity of human osteoblast-like MG-63 cells growing on the scaffolds isolated from the coral Goniopora sp. [360]. Moreover, as recently reported by Gancz and co-workers, “the coral skeleton biomaterial may act as a strong, promotive scaffold for tissue regeneration due to its ability to reduce its rejection by inflammatory reactions such as phagocytosis” [361].

In addition to application of stony corals reported above, octocorals also possess a high biomimetic and biomedical potential [4]. Indeed, their structural architecture, the role of gorgonin-associated mineralization, and the potential of deep-sea bamboo octocoral for tissue engineering were reported [346]. The skeleton structure of black coral species, i.e., Parantipathes larix [27], or Cirrhipathes sp. [25] contains chitin that was also shown to be biocompatible and serves as a template for cell adhesion and differentiation.

Large scale production of coral-based biomaterials is limited due to the protection of coral reefs [362]. However, further investigations to use corals as model 3D porous constructs and source for bioinspiration in materials science are trending well.

4.2. Molluscan Shells

Though molluscan shells (Table 13) have been intensively studied primarily as the indicators of environmental transformations [363,364] and contamination [365,366]; over the years, this has changed with the focus on biomechanics [367,368,369,370], biomimetics, and materials science [26,371,372,373,374,375,376] of these biomineralized constructs.

With about 18 million tons of total annual production, shelled molluscs are one of the most important components of global aquaculture industry [390], being especially important for the regions of Eastern Asia (China, South Korea and Japan), and, to a less extent, North America (the USA) and South America (Chile). Due to the risks associated with freshwater shortage, energy consumption and constantly increasing human population the development of offshore mollusc farms is of an increasing interest. In order to valorize molluscan shell wastes that constitute from 59% up to over 75% of the total organism weight depending on molluscan taxa [391], several solutions were developed.

Being composed mainly from calcium carbonate (it can reach up to 99.9% of the shell mass), shell wastes can be utilized as a mortar component [392]. The authors revealed that crushed oyster shell small particles (0.074–2 mm) were more suitable than the large ones (2–4.75 mm) as sand substitutes. A similar study conducted by [393] demonstrated that mollusc based CaCO3 particles are longer and of prismatic shape in contrast to the round and shorter particles of traditionally used limestone (Figure 5), thus affecting mortar setting time and its mechanical properties.

The use of shell CaCO3 as a source of calcium in livestock feed supplements is another alternative to utilize shell wastes. Such supplements were reported to have a positive impact on animal bones and the strength of eggshells [394]. In addition, different studies indicated that both oyster and clam shells are equally effective regarding eggshell strength and egg production rate [395,396,397,398,399]. Such benefits of shell derived CaCO3, shown in earlier studies, were also confirmed in recent research [400,401].

Furthermore, molluscan shells can be applied for soil neutralization and metal decontamination. Soil neutralization, typically known as liming, is performed in order to reduce acidity, improve oxygen levels, soils fertility and structure, therefore directly affecting agricultural crop yields [402]. Indeed, the use of crushed oyster shells leads to an increase in soil pH, available phosphorus and exchangeable cations, thus, positively affecting the productivity of Chinese cabbage [403]. In addition, marine shell wastes can be applied as soil decontamination agents as was reported for soils containing copper [404], lead, cadmium [405], and arsenic (V) [406].

Another option to utilize molluscan shells lies in wastewater filtration. Several studies pointed to the capabilities of razor clam and oyster shells to accumulate Zn2+, Pb2+, and Cd2+, though with different capacities, favoring calcite rich oyster powder for Pb2+ and aragonite rich razor clam for Cd2+ [407].

Intriguingly, molluscan shells, being among the most important biominerals known to date, challenge man-made ceramics, i.e., they are characterized by a specific internal features hierarchy, structural organization, and organic-mineral phase interactions that are formed in mild conditions unlike ceramics, which require high temperature and/or high pressure [408].

The nacre, of the structural shell elements (Figure 6), has gained special attention. An increasing interest in the nacre, an acellular composite of calcium carbonate acting as an internal shell coating for bivalves, cephalopods and gastropods, stems from its structural similarity to bone and remarkable mechanical properties, i.e., Young’s modulus of 30–40 GPa for the nacre vs. about 20 GPa for human bones, resistance to failure of 185–200 MPa for the nacre vs. about 140 MPa for human bones [409,410]. Hence, nacre material has a great potential to be used as bone grafting material (Figure 7) [411].

Indeed, osseointegrative properties of the nacre and its potential for implantology were shown in numerous studies [411,413,414,416,417,418]. Moreover, molluscan shells can be used in bone biocomposite scaffolds [385,419,420], which are characterized by porosity favouring cell seeding and adhesion (Figure 8).

5. Conclusions Biological materials of marine origin represent a special scientific niche within the global biomaterialogy with a long history of their research and applications in diverse fields of human activity. What was recently referred to as processed marine biological waste is now considered raw material for the production of biomaterials, which differ from their synthetic analogs in biocompatibility and possess excellent biodegradability. In addition, the approach to the study of marine biocomposite structures has shifted to the point of view of modern bionics and biomimetics, when these materials are thought of as models for creating new composites, which are produced according to «drawings drawn by nature» as a result of evolutionary selection. The design of such new hybrid materials is of crucial importance for fundamental science because further progress in their research and application is impossible without understanding the mechanisms of their formation as well as their structural features at the molecular and nano-level. The progress in marine biomaterials research is mainly attributable to its strong interdisciplinary character: the exchange of expertise in marine and structural biology, bioinspired materials chemistry, biomineralogy, biomimetics, biomechanics, and solid state physics is a key action to strengthen the scientific and practical level of this modern research field. We are strongly convinced that the scientific area described herewith will include both a high degree of novelty and challenging tasks in the future. Researchers will discover the key principles of molecular structure of marine biomaterials that will finally let them realize the dream of understanding the chemistry and materials science of diverse unique marine biocomposites spanning from atomistic detail to the macrolevel. This concept will adopt a truly multidisciplinary and multi-scale approach to study not only the structural peculiarities of marine biomaterials, but also the mechanisms of their transformation in hybrid, functionally advanced composites, hierarchically constructed during special treatments and modifications according to human goals. A holistic understanding of the creation of a new generation of bioinspired composites and its impact on large-scale biomimetics with future input in modern technologies can only be achieved by a modern multi-facetted approach, which has not been attempted before. An undoubted factor stimulating progress in marine biomaterials is a sharp move away from synthetic plastic materials due to the serious and global threat of pollution of the world’s oceans by microplastic waste. We readily believe that biomaterials of marine origin will also be actively studied because of their extreme prospects for the so-called marine bioeconomy worldwide.

Figure 1. Overview of the main sources of marine biomaterials used nowadays.

Figure 2. Digital microscopy images: Naturally prefabricated 3D chitinous skeletal constructs of verongiids sponges origin (A) are made of interconnected tube-like fibres with excellent ability to absorb diverse liquids including blood (B). They can be used also as biodegradable 3D scaffold-based bioreactors for cultivation of algal cultures (C,D) for further production of corresponding biologically active compounds under controlled laboratory conditions.

Figure 3. Spongin of the bath sponges origin (A) has been recently recognized as unique marine biomaterial for development of metal oxide-based composites (B, arrow) and the source for creation of mechanically stable 3D turbostratic graphite (C), which can be further functionalized with selected metals (D). For details, see [86].

Figure 4. Digital microscopy images: Despite protection and the lack of industrial harvesting, glass sponges, thanks to the complex architecture of their biosilica-based skeletons (A-C)-Aphrocallistes sp., (D)-Waltheria sp.; (E)-Euplectella sp.) represent a unique source for creating 3D models for potential biomimetic functional materials.

Figure 5. SEM micrographs showing morphology of the particles in (A) mussel and (B) quarry derived limestone. Images adapted with permission from [393].

Figure 6. Abalone (Haliotis sp.) shell and its structure. (A) interior view of the shell and (B) scanning electron microscope micrograph showing the cross section the shell; (C) the microstructure of the nacre. Image reproduced with the permission from [412].

Figure 7. Examples of different forms of nacre used in bone graft studies. (A) nacre powder (denoted with a ★) injected within sheep vertebrae; adapted from [413], with permission; (B) nacre in the form of a cylinder (N) implanted in sheep femoral epiphysis; adapted from [388] with permission; (C) trochlea shaped nacre in sheep femoral trochlea; adapted from [414] with permission; (D) screw shaped nacre implanted in sheep metatarsus; adapted from [415] with permission.

Figure 8. SEM micrographs presenting (A) porous morphology of fabricated scaffold and (B) cells attached to the surface of the scaffold matrix-figures adapted from [385] with permission.

Author Contributions

Conceptualization, H.E.; writing-original draft preparation, Y.K., S.L., I.P., and H.E.; writing-review and editing, H.E. and Y.K.; supervision, H.E. and I.P.; funding acquisition, H.E. All authors have read and agreed to the published version of the manuscript.

Funding

This work was partially supported by DFG Project HE 394/3, SMWK Project no. 02010311 (Germany), by Alexander von Humboldt Polish Honorary Research Scholarship (FNP, Poland) and OPUS19 Program (NCN, Poland). We would like also to thank the Polish National Agency for Academic Exchange for the financial support within the "Polish Returns" programme (PPN/PPO/2018/1/00071/DEC/1). Y.K. is supported by the Russian Science Foundation (Grant No. 18-13-00220).

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of this review, in the writing of the manuscript, or in the decision of this publication.

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Yuliya Khrunyk

1,2,

Slawomir Lach

3,

Iaroslav Petrenko

4 and

Hermann Ehrlich

4,5,*

1Department of Heat Treatment and Physics of Metal, Ural Federal University, 620002 Ekaterinburg, Russia

2Institute of High Temperature Electrochemistry, Ural Branch, Russian Academy of Sciences, 620990 Ekaterinburg, Russia

3Department of Biomedical Chemistry, Faculty of Chemistry, University of Gdansk, 80-308 Gdansk, Poland

4Institute of Electronics and Sensor Materials, Technische Universität Bergakademie Freiberg, 09599 Freiberg, Germany

5Center for Advanced Technology, Adam Mickiewicz University, 61614 Poznan, Poland

*Author to whom correspondence should be addressed.

Word count: 19558

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© 2020. This work is licensed under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.

Abstract

The growing demand for new, sophisticated, multifunctional materials has brought natural structural composites into focus, since they underwent a substantial optimization during long evolutionary selection pressure and adaptation processes. Marine biological materials are the most important sources of both inspiration for biomimetics and of raw materials for practical applications in technology and biomedicine. The use of marine natural products as multifunctional biomaterials is currently undergoing a renaissance in the modern materials science. The diversity of marine biomaterials, their forms and fields of application are highlighted in this review. We will discuss the challenges, solutions, and future directions of modern marine biomaterialogy using a thorough analysis of scientific sources over the past ten years.

Details

Title
Progress in Modern Marine Biomaterials Research
First page
589
Publication year
2020
Publication date
2020
Publisher
MDPI AG
e-ISSN
16603397
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.3390/md18120589
ProQuest document ID
2465300156
Copyright
© 2020. This work is licensed under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.