See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/263935949 Biotechnological Potential of Sponge-Associated Bacteria Article in Current Pharmaceutical Biotechnology · July 2014 DOI: 10.2174/1389201015666140711115033 · Source: PubMed CITATIONS READS 30 1,188 4 authors: Juliana Santos Gandelman Marcia Giambiagi-deMarval Federal University of Rio de Janeiro Federal University of Rio de Janeiro 6 PUBLICATIONS 85 CITATIONS 77 PUBLICATIONS 1,276 CITATIONS SEE PROFILE SEE PROFILE Walter M R Oelemann Marinella S Laport Federal University of Rio de Janeiro Federal University of Rio de Janeiro 46 PUBLICATIONS 1,201 CITATIONS 85 PUBLICATIONS 717 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Bioprospection of antibiotic and heavy metal resistance genes in two genera isolated from marine invertebrate organisms View project Evaluation of anti-biofilm activity of marine sponges associated bacteria against Staphylococcus spp. View project All content following this page was uploaded by Marinella S Laport on 11 August 2014. The user has requested enhancement of the downloaded file. Send Orders for Reprints to reprints@benthamscience.net Current Pharmaceutical Biotechnology, 2014, 15, 143-155 143 Biotechnological Potential of Sponge-Associated Bacteria Juliana F. Santos-Gandelman, Marcia Giambiagi-deMarval, Walter M.R. Oelemann and Marinella S. Laport* Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho, 373, Cidade Universitária, 21941-590, Rio de Janeiro, Brazil Abstract: As sessile and filter-feeding metazoans, marine sponges represent an ecologically important and highly diverse component of marine benthic communities throughout the world. It has been suggested that marine sponges are hosts to many microorganisms which can constitute up to 40-60% of its biomass. Recently, sponges have attracted a high interest from scientific community because two important factors. First there is the fact that sponges have a wide range of associated bacteria; and, second, they are a rich source of bioactive substances. Since 1950, a number of bioactive substances with various pharmacological functions have been isolated from marine sponges. However, many of these substances were subsequently shown to be actually synthesized by sponge-associated bacteria. Bacteria associated with marine sponges constitute an interesting source of novel bioactive compounds with biotechnological potential such as antimicrobial substances, enzymes and surfactants. In addition, these bacteria may be biofilm forming and can act as bioindicators in bioremediation processes of environmental pollution caused by oil and heavy metals. This review focuses on the biotechnological applications of these microorganisms. Keywords: Bioactive substances, bioindicators, biofilm, bioremediation, biosurfactant, sponge-associated bacteria. INTRODUCTION As the simplest and most primitive metazoans, marine sponges are important components of benthic communities due to their biomass and potential influences on pelagic processes [1-4]. Marine sponges belong to the phylum Porifera which consists of four classes, Hexactinellida, Calcarea, Demospongiae, and Homoscleromorpha, the latter of which was more recently established [5]. The architecture of sponges differs from that of any other taxon. Sponges are the simplest form of multi-cellular animals. They do not possess typical tissues found in other multicellular animal species and their cells retain some degree of totipotency and independence [6]. The basic body plan comprises of several different cell layers (Fig. 1). The outer surface, or pinacoderm, is formed by epithelial cells known as pinacocytes. Through pores (ostia) on the sponge surface, these cells also extend along the interior canals which permeate the sponge. Inside the sponge, specialized flagellated cells (choanocytes) form a series of chambers where feeding takes place. In these choanocyte chambers, collectively called the choanoderm, the movement of the choanocytes’ flagella pumps in water through the ostia and along the often elaborated aquiferous systems within the sponge. Choanocytes also filter food particles (including bacteria and microalgae) from the water, and these are transferred to the mesohyl, an extensive layer *Address correspondence to this author at the Instituto de Microbiologia Paulo de Góes - Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho, 373, Cidade Universitária, 21941-590, Rio de Janeiro, Brazil; Tel: +5521-3938-8344; Fax: +5521-3938-8028; E-mail: marinella@micro.ufrj.br 18-/14 $58.00+.00 of connective tissue (Fig. 1). In the mesohyl, food particles are digested via phagocytosis by another group of sponge cells, the archaeocytes (or amebocytes). These totipotent cells are capable of differentiating into any of the other sponge cell types. Mesohyls present in many sponges represent dense communities of microorganisms [6, 7]. The presence of these microorganisms near the amebocytes suggests that the sponge cells either recognize different types of microorganisms or that the latter have developed mechanisms to prevent being engulfed. Once filtered in the choanocyte chambers, the water is expelled through an opening at the top, the osculum [8]. In its natural habitat, the spatial distribution of Porifera is strongly influenced by water quality, especially with respect to its content of particles (organic and mineral), pollutants, and dissolved organic matter. Therefore, marine sponges are good indicators of water quality and have been used in environmental monitoring and bioremediation processes [9-11]. Sessile organisms such as sponges and other marine invertebrates, including corals and sea squirts, greatly rely on the production of chemical compounds as defense against natural predators, competitors, and invading organisms such as bacteria, viruses, and eukaryotes. Therefore, marine sponges have been attracting a particular interest in research, and a wide variety of natural products with different pharmacological properties was identified and characterized [12]. Pharmaceutical interest in sponges began in 1950 with the discovery of the nucleosides spongothymidine and spongouridine, which were isolated from the marine sponge Cryptotethya crypta [13, 14]. These nucleosides formed the basis for the synthesis of ara-C, the first anticancer agent © 2014 Bentham Science Publishers 144 Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 Santos-Gandelman et al. Pinacoderm Choanocyte Spicule Mesohyl Pinacocyte Bacteria Choanocyte chamber Amebocyte Secondary metabolites Porocyte Sclerocyte Water flow Fig. (1). Simplified schematic representation of a sponge. (Left) Cross-section of a sponge showing the mesohyl, pinacoderm and interconnected choanocyte chambers. Water enters the sponge through multiple small pores and exits through a large excurrent pore (arrows). (Right) A close up of an area surrounding a choanocyte chamber. Flagellated choanocyte cells that capture food particles, which are then phagocytosed by the mobile amebocytes, line the choanocyte chamber. Many members of the sponge symbiotic microbial community exist extracellularly in the mesohyl, alongside food particles and potential pathogens. There, microorganisms and sponge cells likely interact for the purposes of nutrient uptake, metabolite exchange and cell signaling and recognition. derived of marine organisms, and ara-A, an antiviral compound [15]. Interestingly, in some cases compounds isolated from sponges appear to be synthesized by their associated microorganisms [7]. Sponges interact with associated microorganisms in several ways. For the sponge, microorganisms may represent either pathogens, or parasites, or symbionts, or simply a different source of nutrients [16]. Microorganisms may comprise 40 to 60% of the biomass of the sponge, with densities exceeding 109 of cells per gram of sponge tissue [17-19]. The ecologic and evolutionary importance of spongemicrobe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in some cases, the compounds are synthesized by sponge-associated microorganisms [7, 20-21]. In this review we survey the discovery of products derived from spongeassociated bacteria with potent in vivo or in vitro activities. Our objective is to highlight various biotechnological applications of these microorganisms (see also Fig. 2). pharmaceutical importance of these substances is attributed to their antimicrobial, anti-inflammatory, antitumor and anticancer properties. Among the large number of bioactive substances that have been isolated from marine sponges, some bioactive substances have already undergone pre-clinical and clinical screening as anticancer and anti-inflammatory agents. Of the various chemical classes of this substances, polyketides, alkaloids, fatty acids, peptides and terpenes are the most abundant ones [26]. The identification of structurally similar bioactive substances from phylogenetically unrelated sponges suggests that these bioactive substances are produced by sponge-associated bacteria, rather than the sponge itself [7, 21]. This is further confirmed in case of compounds particularly known to be produced exclusively by bacteria, such as polyketides and non-ribosomal peptides. Therefore, several studies have been conducted to investigate bioactive substance produced by bacteria that are commonly associated with marine sponges [26-32]. Production of Antimicrobial Substances In this review, we do not intend to comprehensively review sponge-derived natural products; such reviews belong in the field of chemistry rather than microbiology per se, and many reviews dedicated to this topic already exist [12, 20, 33-43]. Therefore, we focus our attention on some relevant examples of antimicrobial (antibacterial, antiviral, antifungal, antiprotozoal) substances produced by spongeassociated bacteria. Marine microbial bioactive substances have interesting biomedical potential, pharmaceutical relevance and diverse biotechnological applications [22-25]. The biomedical and In the marine environment, competition for nutrients and space is a powerful driving force that leads to the evolution of effective strategies for marine microorganisms to colonize BIOTECHNOLOGICAL POTENTIAL OF SPONGEASSOCIATED BACTERIA Biotechnological Potential of Sponge-Associated Bacteria Production of 145 Biological indicators Production of enzymes antimicrobial substances a. Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 b. c. Organic matter urease Nitrogen cycle ammonia contaminant Biotechnological potential of sponge-associated bacteria e. d. oil biofilm waste water oil clean water biofilm oreanic matter Production of biosurfactants Biofilm generation Fig. (2). Examples of the biotechnological potential of sponge-associated bacteria. (a) Production of antimicrobial substances: A number of substances with various pharmacological functions have been described; (b) Production of enzymes: sponge-associated bacteria produce hydrolytic enzymes as for example, urease. Hydrolysis of urea by endosymbionts represents a predominant ecological characteristic of sponges-associated bacteria. Urease converts urea into ammonia that in turn participates in the nitrogen cycle; (c) Biological indicators: the cultivable bacteria are ideal bioindicators, especially for monitoring marine pollution caused by heavy metals. In addition, they can be used in bioremediation processes; (d) Production of biosurfactants: studies have indicated a function directed towards the bioremediation of environments contaminated by oil and/or heavy metals; (e) Biofilm generation: Biofilms have been applied in wastewater remediation processes. and grow. Consequently, antimicrobials and other secondary metabolites produced by microorganisms aim at antagonizing the growth of other microorganisms by affecting their survival and reproduction [44]. The synthesis of these compounds depends on complex regulatory systems and is generally induced during the stationary phase of microbial growth [45]. The major groups of microorganisms recognized as possible contributors of pharmacologically relevant secondary metabolites of sponges include Actinobacteria, α, β, γ, δ Proteobacteria and Firmicutes. Many of the compounds produced by bacteria are not yet characterized. The phylum Actinobacteria dominates in the production of therapeutic compound, and is followed by Proteobacteria. The bioactive potential of Firmicutes and Cyanobacteria is yet to be explored [26]. According to the previous studies, a number of sponge-associated bacterial genera have been shown to produce antimicrobial substances [26, 27, 30, 41, 46-53, 73], including Actinomyces, Aeromonas, Bacillus, Corynebacterium, Flavobacter, Micrococcus, Pseudoalteromonas, Pseudomonas, Streptomyces and Vibrio. Table 1 [53-73] summarizes some examples of antimicrobial substances produced by sponge-associated bacteria. Several of these substances possess a great potential for drug development, but so far none resulted in a commercial medication. The most promising antimicrobial substances appear to be 2-undecyl-4-quinolone, cyclic dipeptides (also known as diketopiperazines, DKPs), lipopeptides (surfactins, iturins and fengycins), manzamine A, organohalogens (2,4,4’trichloro-2’-hydroxydiphenylether), phenazine, pyrone I, rifamycins and thiopeptides. Some of the substances produced by bacteria have been shown to be multifunctional. Among these, manzamine A produced by an actinomycete shows antibacterial, anti-malarial, anti-HIV, anti-tumor, insecticidal and anti-inflammatory activities [43] and appears to hold great promise for the future. Production of Enzymes Apart from some exceptions, sponge-associated microbial communities appear to be relatively stable over time and space [19]. Moreover, these associations are very specific for the production of particular bioactive compounds. However, the mechanism acting in compound production between host and microbial associate is not well understood [26]. It became, clear that gene transfer frequencies are high among sponge-associated bacteria communities. Gene transfer increases the genomic flexibility within these populations and thereby facilitate their continuous adaptation to changing environmental conditions [74]. Therefore, enzymes produced by these bacteria present high potential for application in various industrial processes [75]. Table 2 summarizes some examples of enzymes produced by sponge-associated bacteria that possess potential biotechnological application. 146 Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 Table 1. Santos-Gandelman et al. Antimicrobial substances produced by sponge-associated bacteria. Antimicrobial substances Activity Bacteria producing Sponge Reference 2,4,4’-trichloro-2’-hydroxy-diphenylether (triclosan) and Acyl-1-(acyl-6’-mannobiosyl)3-glycerol (lutoside) Antibacterial Micrococcus luteus R-1588-10 Xestospongia sp. [53] 2-nonyl-4-hydroxyquinoline n-oxide Antibacterial Pseudomonas sp. 1537-E7 Homophymia sp. [54] 2-undecyl-4-quinolone Antimalarial anti-HIV Pseudomonas sp. 1537-E7 Homophymia sp. [54] 3,6-diisopropylpiperazin-2,5-dione Antimicrobial Pseudomonas sp. NJ6-3-1 Hymeniacidon perlevis [55] Acetic acid,-butylester ethanol, 2-(octyloxy)oxalic acid, Allylnonyl ester, 2-Isopropyl-5methyl-1-heptanol, Butylatedhydroxytoluene, Cyclohexanecarboxylic acid, Hexyl ester, Diethyl- phthalate, Pentadecanal- 1-tridecanol and 9-Octadecenal Antimicrobial Nocardiopsis dassonvillei Dendrilla nigra [56] Andrimid Antibacterial Vibrio sp. M22-1 Hyatella sp. [57] Chitinase Antigungal Streptomyces sp. DA11 Craniella australiensis [58] Cyclo-(glycyl-L-seryl-L-prolyl-L-glutamyl) Antibacterial Ruegeria sp. Suberites domuncula [59] Cyclo-(L-proline-L-methionine) Antibacterial Pseudomonas aeruginosa Isodictya setifera [60] Cyclo-(l-pro-l-phe) Antimicrobial Alcaligenes faecalis A72 Stelletta tenuis [61] Diketopiperazine Antibacterial Micrococcus spp. Tedania ignis [62] Iturin Antifungal Bacillus subtilis A202 Aplysina aerophoba [49] Majusculamide c Antifungal Lyngbya majuscula Ptilocaulis trachys [63] Manzamine A Antimalarial Micromonospora sp. Acanthostrongylophora sp. [64] N-Hexadecanoic- acid Nematicide Nocardiopsis dassonvillei Dendrilla nigra [56] MAD08 MAD08 Pumilacidin containing β-Hydroxy fatty-acid Antifungal Bacillus pumilus A586 Aplysina aerophoba [49] Pyrone-I Antibacterial antifungal Pseudomonas sp. F92S91 Unidentified [65] Rifamycin B and Rifamycin SV Antibacterial Salinospora sp. Suberea clavata [66] Streptophenazines G and K Antibacterial Streptomyces sp. HB202 Halichondria panicea [67] Subtilomycin Antibacterial Bacillus subtilis MMA7 Haliclona simulans [68] Surfactin Antifungal Bacillus subtilis A190 Aplysina aerophoba [49] Surfactin, Iturin and Fengycin Antibacterial antifungal Bacillus subtilis A184 Aplysina aerophoba [49] Tetrabromo-diphenyl ethers Antibacterial Vibrio sp. Dysidea sp. [69] Tetromycin B Antiprotozoal Streptomyces axinellae Pol001 Axinella polypoides [70] Thiopeptide (YM-266183 and YM-266184) Antibacterial Bacillus cereus QN03323 Halichondria japonica [71] Trisindoline Antibacterial Vibrio sp. Hyrtios altum [72] Valinomycin Antiprotozoal Streptomyces sp Unidentified [30] Urauchimycin Antibacterial Streptomyces sp. Ni-80 Unidentified [73] Biotechnological Potential of Sponge-Associated Bacteria Table 2. Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 147 Enzymes produced by sponge-associated bacteria with potential biotechnological application. Enzymes Bacteria producing Sponge Reference Acetylcholinesterase Arthrobacter ilicis Spirastrella sp. [80] Agarase Cytophaga sp. Halichondria panicea [79] Alkaline cellulase Marinobacter MSI032 Dendrilla nigra [84] Alkalophilic amylase Halobacter MMD047 Unidentified [83] Anticholinesterases Bacillus subtilis M18SP4P Fasciospongia cavernosa [86] Chitinase Streptomyces sp. DA11 Craniella australiensis [58] Dehalogenase Desulfovibrio Aplysina aerophoba [89] Phospholipase A2 (PLA2 Streptomyces dendra sp. nov. MSI051 Dendrilla nigra [56] Psychrophilic alkaline lipase Pseudomonas sp. Unidentified [81] SGNH hydrolase Unknown Hyrtios erecta [85] Thermo-stable amylase Nocardiopsis dassonveille MAD04 Unidentified [82] Thermo-tolerant alkaline protease Roseobacter MMD040 Unidentified [82] Urethanase Micrococcus sp. Spirastrella sp. [87] Phospholipase A2 (PLA2) is an ubiquitous defense enzyme that was first described in snake and bee venoms and later shown to be widely distributed among both, plant and animal kingdoms [76]. Previous studies have demonstrated different levels of PLA2 in a number of marine invertebrates including Cnidaria [77], Porifera [78] and Echinodermata [56]. In addition to secondary metabolites, sponge-associated microorganisms also can produce PLA2. However, there is only one report on the production of PLA2 by the bacterium Streptomyces dendra sp. nov. MSI051 which in turn is associated with the sponge Dendrilla nigra. Both, the sponge and its bacterial symbiont, contain high levels (about 1,032 U/L) of PLA2. It has been speculated that PLA2 may play a functional role in the protection of the sponge against fouling [56]. Because marine sponges are in constant contact with large amounts of water and organic matter, one hypothesis suggests that some sponge-associated microorganisms produce hydrolytic enzymes to convert this organic matter into nutrients for the sponge. Some evidence from studies on enzyme production by different microorganisms isolated from marine sponges support this hypothesis. Bacteria of the genus Cytophaga associated with the sponge Halichondria panicea were shown to hydrolyze agar [79]. Other bacteria isolated from six marine sponges (Spirastrella sp., Phyllospongia sp., Ircinia sp., Aaptos sp., Azorica sp. and Axinella sp.) were found to produce amylase, protease, and carboxymethylcellulase [80]. In addition, other studies have demonstrated that the cultivable endosymbionts associated with the sponges Fasciospongia cavernosa and Dendrilla nigra produce valuable enzymes for the production of nutrients, including amylase, cellulase, lipase and protease [8183]. Cellulases are important biocatalysts with many industrial applications, for instance in textile and paper industry, in laundry detergents, as well as in the grains processing, like coffee and beans. Apart from cellulases, esterases and lipases are also important biocatalysts used in organic synthesis. They have been used in a broad range of industrial applications because their stability, their high activity in organic solvents, and their enantio-⁄stereoselectivity. Proteases represent one of the largest groups of industrial enzymes and possess a variety of applications ranging from use in detergents, in leather preparation and in food processing [75]. Enzyme production under in vitro conditions has been observed in numerous studies, such as the synthesis of alkalophilic amylase by Halobacter MMD047 [83], psychrophilic alkaline lipase by Pseudomonas sp. [81], thermotolerant alkaline protease by Roseobacter MMD040, alkaline cellulase by Marinobacter MSI032 [84], and thermo-stable amylase by Nocardiopsis dassonveille MAD04. These enzymes can be obtained from cultured bacteria and possess potential application in the production of drugs, foods, beverages, detergents, textiles, and in the processing and treatment of contaminated water [82]. Using a metagenomic library constructed from bacteria associated with a marine sponge Hyrtios erecta, a novel esterase was identified that belongs to the SGNH hydrolase superfamily of esterases. This esterase shows thermal stability and salt tolerance necessary for its use as an industrial enzyme [85]. Enzymes produced by sponge-associated bacteria may also have clinical relevance, for example in the degradation of the neurotransmitter acetylcholine in the brain, where acetylcholinesterase (AChE) inhibitors or anticholinesterases decrease the activity of enzyme acetylcholinesterase [86]. These inhibitors play an important pharmacological role in neurodegenerative diseases like Alzheimer and Parkinson. Recently, a potent AChE inhibitor was identified [86] that is 148 Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 produced by Bacillus subtilis strain M18SP4P, isolated from the marine sponge Fasciospongia cavernosa. The bacterium Arthrobacter ilicis isolated from the sponge Spirastrella sp. produces the enzyme acetylcholinesterase. This enzyme was shown to be heat tolerant and its activity is not affected by the relatively high concentration of the major cations found in seawater, such as Na+, Ca2+, and Mg2+. The bacterium Micrococcus sp. is associated with the sponge Spirastrella sp. and is capable of producing urethanase that could potentially be used to remove the chemical carcinogen urethane from alcoholic beverages [87]. Selvin and colleagues [88] reported that about 65% of the microorganisms isolated from marine sponges released the enzyme urease at an early stage of growth. They assumed that the sponges were exposed in an area contaminated with urea which is toxic to microorganisms. Thus, effective hydrolysis of urea by endosymbionts represents a predominant ecological characteristic of sponges-associated bacteria. Urease converts urea into ammonia that in turn participates in the nitrogen cycle. Moreover, ammonia generated by hydrolysis can be used by the sponge in protein synthesis. These findings suggest that these bacteria play multiple roles in nutrition, physiology and ecology of the marine sponge and its environment [88]. Bioremediation Bioremediation is the process of using microorganisms in situ or ex situ to clean up contaminated environments. The metabolic ability of the microorganisms to mineralize or transform organic contaminants into less harmful substances can be integrated into natural biogeochemical cycles. Bioremediation is an attempt to accelerate naturally occurring degradation by optimizing the limiting conditions. Bioremediation is nondestructive, treatment- and cost-effective and therefore represents a logistically favorable clean-up technology [90]. Some common microorganisms which are able to perform bioremediation in the marine environment are Pseudomonas, Flavobacterium, Arthrobacter, Azotobacter, Rhodococcus, and Bacillus [91]. To better illustrate the biotechnological application of sponge-associated bacteria in the bioremediation process, this section is subdivided into three topics: biological indicators, production of biosurfactants and biofilm generation. Santos-Gandelman et al. arise within a standard time pattern [97]. This sub-lethal exposure can affect physiological functions and behavior of organisms [98]. Thus, the effects of heavy metal pollution in the environment could be detected directly in spongeassociated bacteria instead of in situ monitoring of changes in the sponge host organisms [96]. Free-living marine bacteria are constantly exposed to environmental contaminants and could preferentially be used as a model for monitoring of contamination in marine ecosystems. However, the population structure of these microorganisms changes drastically as a consequence of excessive exposure to contaminants and to external disturbances, such as the movement of migratory animals [94, 99]. On the other hand, the cultivation of sponge-associated bacteria would allow to estimate these effects since sponges have a high filtration capability with retention of about 80% of the particles, including free-living bacteria [100]. According to a study by Selvin and colleagues [96] and De and colleagues [101], marine pollution caused by heavy metals can be monitored by culture of bacteria associated with sponges. In addition to their use as bioindicators, sponge-associated bacteria can also be used as actors in bioremediation processes. Significant reduction of cadmium in culture supernatants of marine bacteria suggests microbial absorption of this metal [102], and an absorption rate of about 110 mg of lead per gram of dry weight has been reported for Pseudomonas aeruginosa [103]. Heavy metals have remarkable influences on mammalian cells and have the ability to modulate the function of multicellular networks, such as the immune system. Certain metals, such as zinc, manganese, and copper are necessary for normal physiological processes, whereas others, including lead, cadmium, chromium and mercury are environmental pollutants and may adversely affect human health. Among the several heavy metals related with health risks, mercury is notable for its wide distribution in the environment and the wide spectrum of effects that it can induce [104]. The organic form of mercury, methylmercury (MeHg), acts as a potent neurotoxin [105]. MeHg accumulates in various levels throughout the aquatic food chain and humans are exposed primarily through consumption of contaminated fish. Numerous toxicological studies examined the bacterial sensitivity and resistance to metals [93-95]. Generally, the introduction of heavy metals in the environment can produce substantial changes in microbial communities and their activities, and bioavailability and bioaccumulation of these metals in aquatic ecosystems have tremendous importance worldwide [96]. Several studies have been conducted with the aim of reducing the impact of contamination by heavy metals in various environments. Regarding the removal of heavy metals, bioremediation processes are more attractive when compared to physicochemical methods because the overall cost of bioremediation is generally significantly lower than physicochemical methods and it is highly efficient [106]. The mechanisms of resistance to heavy metals that evolved in microorganisms include: precipitation of metals as phosphates, carbonates and/or sulfates; volatilization of metals by methylation or ethylation; physical exclusion of electronegative components in membranes and in extracellular polymeric compounds; and energy-dependent efflux systems and intracellular sequestration by low molecular weight cysteinerich proteins [107]. The harmful effects of the accumulation of sub-lethal amounts of heavy metals are not obvious because they do not Certain environmental strains of bacteria have developed resistance mechanisms that are highly specific for mercury. Biological Indicators Marine sponges filter a large volume of water and accumulate heavy metals and other contaminants from the surrounding environment. Therefore, bacteria associated with sponges have been used over a long period as indicators of contamination in marine ecosystems [92]. Biotechnological Potential of Sponge-Associated Bacteria The mechanism of bacterial resistance to mercury involves two enzymes that operate sequentially: an organomercurial lyase (MerB) that cleaves the carbon-mercury bonds of organomercury compounds, and a mercuric reductase (MerA) that reduces Hg2+ to Hg0 (volatile) [108]. Under anaerobic conditions, some bacteria are not affected by mercury, since it is directly used for production of mercury sulfide (HgS) which is apparently non-toxic [109]. Mobile genetic elements such as plasmids and transposons may carry multiple genes encoding proteins involved in metal resistance. Thus, exposure to these agents can select microorganisms resistant to a variety of heavy metals. These microorganisms are useful in bioremediation in contaminated environments, like a genetically engineered strain of Escherichia coli which expresses metallothionein and an Hg2+ transport system. Metallothioneins are cysteine-rich proteins that have high affinity to metals [110], and bioaccumulation of toxic metals using genetically engineered microorganisms have been reported in a number of studies [111-114]. Another example is the extremophile bacterium Deinococcus radiodurans that has been employed to treat mixed radioactive wastes and to volatilize mercury [115]. All mercury -resistant strains isolated from either terrestrial or fresh water environments harbor genes with homology to merTn21 [116] or to merTn501 [117]. However, in mercury -resistant marine strains, the observed frequency was lower [118-119]. In the study conducted by De and colleagues [101], only 9 of the 11 mercury-resistant marine strains were positive of merA, suggesting the presence of other genes involved in mercury resistance. In Alcaligenes eutrophus CH34, Liesegang and colleagues [120] identified various genes involved in metal resistance, including three genes for mercury resistance, one for chromium resistance and two for resistance to bivalent cations. Furthermore, the gene cluster czr in P. aeruginosa was reported to contribute to the resistance to cadmium and zinc [121]. Microorganisms resistant to multiple heavy metals are of great importance because they can be used in bioremediation of environments contaminated with various metals, as previously reported [101]. Production of Biosurfactants Biosurfactants are a structurally diverse group of tensioactive substances produced by microorganisms. All biosurfactants are amphiphilic, with a polar (hydrophilic) portion and a nonpolar (hydrophobic) portion. The hydrophilic group is composed of mono-, oligo- or polysaccharides, peptides or proteins, while the hydrophobic portion usually contains saturated or unsaturated fatty acids or aliphatic alcohols [122]. Due to their amphiphilic structure, biosurfactants increase the surface area of hydrophobic water-insoluble substances, leading to an increase in the bioavailability of such substances in water. Furthermore, they change the properties of the bacterial cell surface. The surface activity of biosurfactants makes them excellent emulsifying agents, dispersants, and defoamers [123]. Compared with their chemically synthesized equivalents, biosurfactants have many advantages because they are biodegradable, less toxic, and show higher selectivity and increased foaming capacity. Further- Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 149 more, biosurfactants can be active under extreme temperature, pH and salinity conditions and may also be produced from industrial waste and sub-products [124-125]. Several studies have demonstrated the biosurfactant potential of sponge-associated bacteria. Most of these studies indicated a possible application in the bioremediation of environments contaminated by oil and/or heavy metals [126131]. The potential of biosurfactants for decontamination of soil containing heavy metals was confirmed by Juwarkar and colleagues [132]. The authors showed that a dirhamnolipid biosurfactant produced by Pseudomonas aeruginosa strain BS2 was able to selectively remove heavy metals from contaminated soil in the following order of efficiency: chrome/ cadmium ≥ copper/lead ≥ nickel [132]. The role of biosurfactants produced by marine bacteria in the remediation of polyaromatic hydrocarbons has also been previously reported [125]. Das and colleagues [133] further investigated the possibility of using biosurfactants produced by marine bacteria in the removal of heavy metals from solutions. Their study revealed that the biosurfactants tested were able to bind metal ions, and that the removal percentage of cadmium and lead was variable depending on the different concentrations of metals and biosurfactants. The ability of marine biosurfactants to sequester toxic heavy metals and to form an insoluble precipitate may be useful in the treatment of wastewater containing such metals [133]. In 2010, Gnanamani and colleagues [128] found that the marine strain Bacillus sp. MTCC 5514 reduced the concentration of hexavalent chromium and developed tolerance to trivalent chromium through the synthesis of biosurfactants by the extracellular enzyme chromium-reductase. The hypothesis is that trivalent chromium generated by the reduction of hexavalent chromium would be entrapped in micelles formed by the biosurfactants synthesized by the cell. Thus, the micelles would prevent microbial cells from being exposed to trivalent chromium, and microbial growth and tolerance to chromium were observed even at increased concentrations of chromium. In this context, our group observed that six out of 21 mercury-resistant isolates from marine sponges produced biosurfactants. However, no merA gene was detected in these strains, suggesting that tolerance to mercury may involve sequestration [134]. Recently, Santos-Gandelman and colleagues [135] described the potential mercury bioremediation by Bacillus cereus strain Pj1 isolated from the marine sponge Polymastia janeirensis.B. cereus Pj1 was found to be resistant to 100 µM HgCl2 and to 10 µM methylmercury. Pj1 was also highly resistant to other heavy metal salts, including CdCl2 and Pb(NO3)2, either alone or in combination. The mer operon is located on the bacterial chromosome, and the volatilization test indicated that the B. cereus Pj1 was able to reduce Hg2+ to Hg0. This strain demonstrated a potential for biosurfactant production and presented a higher emulsification activity than synthetic surfactants. Biosurfactants of the lipopeptide type are also produced by sponge-associated bacteria. The production of lipopeptide biosurfactant from sponge-associated actinomycetes Nocardiopsis alba MSA10 has been characterized [136]. Recently, 150 Current Pharmaceutical Biotechnology, 2014, Vol. 15, No. 2 Lawrance and colleagues [137] investigated the production of a lipopeptide surfactant from the sponge-associated Bacillus licheniformis NIOT-AMKV06, isolated from the Andaman and Nicobar Islands. The purified surfactant showed excellent emulsification activity with crude oil, kerosene and diesel. The lipopeptide surfactant was highly stable over a pH range of 5.0-10.0 and a temperature range of 20-70°C in the presence of high NaCl concentrations. Besides, the surfactant biosynthesis gene cluster (sfp, sfpO and srfA) from B. licheniformis NIOT-AMKV06 was heterologously expressed in Escherichia coli and the production was increased threefold when compared to the original strain. These results confirmed the potential of the surfactant for use in bioremediation of hydrocarbons in a marine environment and for enhanced oil recovery. Biofilm Generation The high density of microbial communities associated with marine sponges prompted several groups to investigate their ability to form biofilm in the sponge host [27, 134, 138139]. Biofilm, by definition, is composed of bacterial communities surrounded by an extracellular polymeric matrix and attached to surfaces [140]. The polymeric matrix can present different structures and functions depending on the bacterial community and/or environmental conditions involved. The biofilm matrix can physically prevent the penetration of antimicrobial agents, especially those that are hydrophilic and positively charged. In some cases, biofilms are capable of sequestering cations, metals and toxins. Additionally, biofilms can act to protect against ultraviolet radiation, changes in pH, osmotic shock and desiccation [141]. Polysaccharides are a major component of the polymeric matrix, but proteins, lipids and nucleic acids may also be present in the biofilm. In a study by Whitchurch and colleagues [142], DNA was observed in biofilms formed by P. aeruginosa. Allesen-Holm and colleagues [143] described evidence that the DNA was liberated by lysis of a portion of the bacterial population and its presence depended on quorum sensing. The construction of a marine biofilm requires a series of steps that are regulated during the maturation of the structure [144]. Initially, free bacteria in seawater interact with organic and inorganic particles on a surface to promote an initial adhesion. After primary adhesion, bacteria accumulate in the biofilm through growth, resulting in bacterial colonies that can synthesize an extracellular matrix, which in turn can act as a substrate for the adhesion of more microorganisms, the so called secondary colonizers. These secondary colonizers can adhere either directly to the primary film, or they may promote the co-aggregation with other microorganisms and then adhere to the primary film [145]. Biological processes for treating toxic effluents are better than chemical and physical methods in terms of their efficiency and economy and researchers became aware of the potential of biofilm communities for bioremediation processes [144, 146]. Many reports have shown the enhanced bioremediation capability of biofilm forming isolates [147, 148]. Biofilm-mediated bioremediation has showed high efficiency and safety, since the cells in a biofilm have a higher possibility of adaptation and survival (especially Santos-Gandelman et al. under stress) because they are protected within the matrix [149]. In early 1980, Akinson [150] described the use of biofilms for the treatment of water and sewage. However, only in recent decades researchers in the field of bioremediation became interested in biofilm reactors [146]. Chemotaxis and biosurfactant production are physiological properties of the microorganisms in a biofilm that elevate the degradation levels of hydrophobic compounds [151-152]. Microorganisms that form biofilm and secrete polymers on the surface of hydrocarbons are very suitable for the degradation of recalcitrant or slowly degrading compounds, due to their high biomass and the ability to immobilize compounds by bioaccumulation (enhanced accumulation of microorganisms under influence), biosorption (sequestration by interactions with biological matter) and biomineralization (formation of inorganic materials with complex form by interactions with microbial metabolic products) [153]. Most of the recent work published has focused on the adsorption of heavy metals to bacteria or tobiofilm formed by a single bacterial strain intentionally grown in the laboratory [154-162]. In order to exemplify this statement, two mercury-resistant strains, Bacillus thuringiensis PW-05 [163] and Pseudomonas putida SP1 [164] isolated from marine environments were shown to posses an interesting potential for bioremediation of mercury. These bacteria formed biofilm in the presence of high concentrations of HgCl2 [163, 164]. In relation to sponge-associated bacteria, SantosGandelman and colleagues [134] observed that 71 of 100 strains were able to produce biofilm. Among these bacteria, which belonged mainly to Proteobacteria and Firmicutes, 21 strains were resistant to HgCl2, (unpublished data). In addition, the biofilm-forming bacterium Bacillus cereus Pj1 isolated from the sponge is a strain that can potentially be applied in the bioremediation of HgCl2 and MeHg contamination in aquatic environments [135]. These studies suggest that marine sponge-associated bacteria able to produce biofilm may represent an important tool for remediation of contaminated sites either through reduction or sequestration Biofilm has high adsorption capacities and low production cost. The utilization of biofilm as an adsorbent of polluting ions is one of the promising technologies for treatment of contaminated water. Marine bacteria provide a useful source for bioremediation, and there are many advantages of using them under extreme conditions. When a bacterium is capable of forming biofilms, it increases its bioremediation capability due to the presence of many extracellular polymeric substances like neutral polysaccharides, amyloids, extracellular enzymes and biosurfactants [163]. CONCLUDING REMARKS The mesohyl of marine sponges provides a favorable environment for interactions of a large number of taxonomically diverse bacteria [144]. Several review articles have emphasized the need for understanding symbiotic functions in marine sponges [7, 88, 165-166]. The biotechnological potential of these microorganisms (Fig. 2) remains little investigated and discussed. As shown in this mini-review, the Biotechnological Potential of Sponge-Associated Bacteria high diversity of marine bacteria is underexplored. These microorganisms constantly metabolize sponge products and synthetize numerous specific enzymes and secondary metabolites. From their immense diversity and their constant activity stems their great potential as source of novel and original metabolites and enzymes. In addition, it is likely that disruption of the microbial symbiosis as a result from climate change and/or environmental stress will have a significant impact on the growth of marine sponges and their protection against contamination, predation, and diseases. In an era of rapid environmental change and degradation of marine ecosystems, sponge microbiology investigating the interaction of marine sponges and associated microorganisms is fundamental for unraveling the maximum potential of microorganism for human use. Advances have been made in the field of marine microbial biotechnology but a more extensive and focused approach is needed to investigate what else the marine microbes have to offer. It is important to seriously consider the exploitation of marine microbial life and its associated secondary metabolites. Such studies can be aided by genomic analyses, applying metabolomic approaches and employing combined biomedical and biotechnological efforts, which would lead to discovery of new compounds with a variable degree of bioactivity [41]. The novel antimicrobial substances isolated and characterized from sponge-associated bacteria seem to be very useful and promising for biomedical research in the design of very specific and potent new pharmaceuticals for a wide variety of diseases [21]. The enzymes produced by these microorganisms have the potential capacity to be uniquely suited for many industrial processes [75]. Furthermore, the treatment of environmental pollution by employing microorganisms is a promising technology, either by using bacteria associated with sponges as indicators of contamination or for forming biofilms, or for biosurfactants produced by them in marine ecosystems. Certain bioactive metabolites may also be beneficial in ensuring environmental hygiene, as such antifouling compounds [167]. Unfortunately, there are few studies on these compounds isolated from sponge-associated bacteria [168-169]. Although new compounds are being added day by day, our knowledge of marine microbial bioactive metabolites is very small considering what exists in the deep ocean [41]. Clearly, coordination among microbiologists, natural product chemists, and bioengineers will contribute significantly to investigate the biotechnological potential of spongeassociated bacteria to the pharmaceutical and enzyme industries, and for bioremediation of contaminated aquatic environments. 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