marine drugs Review Marine Spongin: Naturally Prefabricated 3D Scaffold-Based Biomaterial Teofil Jesionowski 1,*, Małgorzata Norman 1, Sonia Z˙ ółtowska-Aksamitowska 1, Iaroslav Petrenko 2, Yvonne Joseph 3 ID and Hermann Ehrlich 2,* 1 Institute of Chemical Technology and Engineering, Faculty of Chemical Technology, Poznan University of Technology, Berdychowo 4, 60965 Poznan, Poland; [email protected] (M.N.); [email protected] (S.Z.-A.)˙ 2 Institute of Experimental Physics, TU Bergakademie Freiberg, Leipziger str. 23, 09559 Freiberg, Germany; [email protected] 3 Institute of Electronics and Sensor Materials, TU Bergakademie Freiberg, Gustav-Zeuner-Str. 3, 09599 Freiberg, Germany; [email protected] * Correspondence: teofi[email protected] (T.J.); [email protected] (H.E.); Tel.: +48-61-665-3720 (T.J.); +49-3731-39-2867 (H.E.) Received: 30 January 2018; Accepted: 6 March 2018; Published: 9 March 2018 Abstract: The biosynthesis, chemistry, structural features and functionality of spongin as a halogenated scleroprotein of keratosan demosponges are still paradigms. This review has the principal goal of providing thorough and comprehensive coverage of spongin as a naturally prefabricated 3D biomaterial with multifaceted applications. The history of spongin’s discovery and use in the form of commercial sponges, including their marine farming strategies, have been analyzed and are discussed here. Physicochemical and material properties of spongin-based scaffolds are also presented. The review also focuses on prospects and trends in applications of spongin for technology, materials science and biomedicine. Special attention is paid to applications in tissue engineering, adsorption of dyes and extreme biomimetics. Keywords: marine sponge; spongin; aquaculture; hybrid material; dyes 1. Introduction Sponges, belonging to the phylum, Porifera, are the phylogenetically oldest multicellular organisms [1], with an evolution dating back to the Precambrian. Currently (2018), there are 8848 valid species described in the World Porifera Database [2], which occur in marine and freshwater habitats. These aquatic animals are currently described in four classes: Demospongiae, Calcarea, Hexactinellida and Homoscleromorpha, based essentially on morphological data and molecular and genetic analyses. Demospongiae is the largest sponge class, including about 80% of all living sponges (nearly 7000 species worldwide), divided into three subclasses: Verongimorpha, Keratosa and Heteroscleromorpha [3]. The focusses of this review are representatives of demosponges which belong exclusively to the subclass, Keratosa, whose mineral-free skeletons consist of “horny” or “keratose” fibers [4,5]. These fibers are known to consist of the halogenated scleroprotein, spongin. Recently the taxonomic name, Keratosa, has been assigned to the group formed by the Dictyoceratida and Dendroceratida orders in the new phylogenetic tree [6–8]. Dictyoceratida are defined as sponges with well-developed, anastomosing spongin fiber skeletons, which are hierarchically organized into primary, secondary and sometimes tertiary fibers, and make up a significant proportion of the body volume [9]. Since ancient times, these sponges have been recognized as “bath sponges” [10]. A typical example is the Mediterranean bath sponge Spongia officinalis, which is also known as an iconic species with high socioeconomic value [11]. Thus, when we speak about bath sponges, it must be clear that we Mar. Drugs 2018, 16, 88; doi:10.3390/md16030088 www.mdpi.com/journal/marinedrugs Mar. Drugs 20182018,, 1616,, x 88 FOR PEER REVIEW 2 of 23 with high socioeconomic value [11]. Thus, when we speak about bath sponges, it must be clear that are referring to the whole organism (body and skeleton) (Figure1). This is because so-called “marketed we are referring to the whole organism (body and skeleton) (Figure 1). This is because so-called sponges” represent cell- and tissue-free, depigmented and demineralized skeletal constructs (Figure2), “marketedMar. Drugs sponges” 2018, 16, x FOR represent PEER REVIEW cell- and tissue-free, depigmented and demineralized2 ofskeletal 23 which have been defined in the scientific literature as “commercial sponges” [12]. These commercial constructs (Figure 2), which have been defined in the scientific literature as “commercial sponges” sponges represent the main source of the “sponge industry” [13]. [12]. Thesewith high commercial socioeconomic sponges value represent [11]. Thus, the when ma inwe source speak aboutof the bath “sponge sponges, industry” it must be[13]. clear that we are referring to the whole organism (body and skeleton) (Figure 1). This is because so-called “marketed sponges” represent cell- and tissue-free, depigmented and demineralized skeletal constructs (Figure 2), which have been defined in the scientific literature as “commercial sponges” [12]. These commercial sponges represent the main source of the “sponge industry” [13]. Figure 1. Photo of the typical representative of Dictyoceratida demosponges, known also by the Figure 1. Photo of the typical representative of Dictyoceratida demosponges, known also by the common name “bath sponges”. commonFigure name 1. Photo “bath of sponges”. the typical representative of Dictyoceratida demosponges, known also by the common name “bath sponges”. Figure 2. Typical example of a “commercial sponge” after initial bleaching. Figure 2. Typical example of a “commercial sponge” after initial bleaching. Figure 2. Typical example of a “commercial sponge” after initial bleaching. Mar. Drugs 2018, 16, 88 3 of 23 Mar. Drugs 2018, 16, x FOR PEER REVIEW 3 of 23 According to Laubenfels and Storr, “the commercial sponge is the macerated and dried skeleton of one of theAccording sponge animalsto Laubenfels that has and no Storr, proper “the spicules. commercial It must sponge be from is the a macerated species whose and skeletondried skeleton consists of one of the sponge animals that has no proper spicules. It must be from a species whose skeleton of spongin fibers, and furthermore, these fibers must continue to be elastic or ‘spongy’ even after consists of spongin fibers, and furthermore, these fibers must continue to be elastic or ‘spongy’ even having been dried” [12]. Traditionally commercial sponges were isolated from diverse representatives after having been dried” [12]. Traditionally commercial sponges were isolated from diverse of the genera Spongia (S. obliqua, S. officinalis, S. barbara, S. barbara dura, S. anclotea, S. sterea, S. graminea, representatives of the genera Spongia (S. obliqua, S. officinalis, S. barbara, S. barbara dura, S. anclotea, S. S. graminea tampa, S. cheiris, S. lamella, S. zimocca) and Hippospongia (H. gossypina, H. lachne, H. kerion, sterea, S. graminea, S. graminea tampa, S. cheiris, S. lamella, S. zimocca) and Hippospongia (H. gossypina, H. H.lachne, communis H. ).kerion, They H. differ communis in fiber). They morphology, differ in porosityfiber morphology, and size. For porosity example, and specimenssize. For example, of S. sterea ofspecimens up to 75 centimeters of S. sterea of in up size to have 75 centimeters been reported in size [12 have]. been reported [12]. TheThe construct construct of of a a commercial commercial spongesponge consistsconsists of a a network network of of spongin spongin fibers fibers which which can can be befrom from 5 to5 to 100 100 microns microns in in diameter diameter depending depending onon thethe spongesponge species (Figure (Figure 3).3). The The meshes meshes are are almost almost rectangularrectangular in in outline, outline, with with dimensions dimensions varyingvarying fromfrom 100 microns to to a a millimeter. millimeter. Figure 3. Schematic view of the principal structural motive found in bath sponges. The SEM images Figure 3. Schematic view of the principal structural motive found in bath sponges. The SEM images to to the right represent the morphological features of the spongin-based skeletal construct. the right represent the morphological features of the spongin-based skeletal construct. Although the use of commercial sponges began several thousand years ago, studies on their chemistryAlthough with the reference use of commercial to spongin spongesas a biological began material several thousanddate back yearsonly to ago, the studies18th century. on their chemistryUnfortunately, with referencethe pathways to spongin of spongin’s as a biologicalbiosynthesis material in bath datesponges back as only well to asthe the 18thgenomics, century. Unfortunately,proteomics and the protein pathways sequences of spongin’s of this unique biosynthesis biopolymer, in bath are spongesstill unknown. as well To as date, the spongin genomics, proteomics(named also and fibrous protein skeleton, sequences pseudokeratin, of this unique neurokeratin, biopolymer, horny are protein, still unknown. collagen-like To date,protein spongin and (namedscleroprotein) also fibrous has no skeleton, clear chemical pseudokeratin, definition neurokeratin, [14]. In this review, horny protein,we focus collagen-like on the history protein of andcommercial scleroprotein) sponges, has including no clear a chemical brief analysis definition of the [economic14]. In this aspects review, of the we sponge focus industry on the history and ofmarine commercial farming sponges, of bath including sponges as a a brief source analysis for the of renewable the economic biomaterial aspects sp ofongin. the sponge Next, we