Marine Actinomycetes Antifouling Agents: History
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Contributor:
Radwa N. Morgan
,
Amer Al Ali
,
Mohammad Y. Alshahrani
,
Khaled M. Aboshanab

Marine actinomycetes produce a multitude of active metabolites, some of which acquire antifouling properties. These antifouling compounds have chemical structures that fall under the terpenoids, polyketides, furanones, and alkaloids chemical groups. These compounds demonstrate eminent antimicrobial vigor associated with antiquorum sensing and antibiofilm potentialities against both Gram-positive and -negative bacteria. They have also constrained larval settlements and the acetylcholinesterase enzyme, suggesting a strong anti-macrofouling activity. Despite their promising in vitro and in vivo biological activities, scaled-up production of natural antifouling agents retrieved from marine actinomycetes remains inapplicable and challenging. This might be attributed to their relatively low yield, the unreliability of in vitro tests, and the need for optimization before scaled-up manufacturing. 

  • marine actinomycetes
  • biofouling
  • antibacterial
  • antifouling

1. Introduction

Biological fouling, often known as biofouling, is an engineering problem that plagues numerous industries. It is the buildup of undesired biological material, corrosions, and suspended particles on surfaces. Fouling varies greatly between medicinal, marine, and industrial applications with significantly high financial burdens [1]. Marine biofouling is also a pertaining issue that has been associated with diminished drill ship efficiencies, high fuel consumption rates among commercial tanks and vessels that consequently level up greenhouse gas emissions, and reared environmental pollution [2][3]. Additionally, ship and vessel biofouling can transfer non-native macro/microorganisms from one region to another, which may disrupt the local marine biodiversity and alter the ecological balance [3][4]. It has been a usual practice to coat the submerged surfaces of artificial structures (hulls, ships, pipelines) with antifouling paints that incorporate biocidal substances and to release them at a controlled rate to prevent unwelcome biofouling [5].
The three main categories of antifouling paints currently in use are self-polishing systems, ablative paints, and soluble matrix paints, generally known as conventional paints [6]. Tributyltin (TBT) released from self-polishing copolymer (SPC) has been used instead of copper coats, and it successfully eliminated settling fouling organisms [7]. However, TBT is not selective; it affects off-target creatures and disturbs the ecosystem balance (disappearance of shellfish, invertebrate species; dog whelk, Nucella lapillus). For its toxic effects, TBT is prohibited in many regions [8]. Few other antifouling biocides are now in use; these include irgarol 1051 (a triazine herbicide), zinc pyrithione (an anti-dandruff fungicide), and Sea-Nine 211 (an isothiazolone). These are mostly employed with copper as co-biocides, particularly to boost the effectiveness against algae [9]. However, toxicities are reported from these antibiofouling coats [10], which necessitate the presence of environmentally benign and eco-friendly natural antifouling agents. Researchers gathered different antifouling compounds from different natural sources (e.g., microorganisms, sponges, plants, algae, etc.) that were more selective against fouling species and had lower toxicity [11][12].
Marine aquatic invertebrates, like sponges and corals, as well as vertebrates like pufferfish, are associated with marine actinomycetes [13]. Interestingly, not only can marine actinomycetes be isolated from marine sediments, but they can coexist with other species and live in both planktonic and biofilm habitats [14]. Most of the novel biologically active compounds (antibacterial, anticancer, antifouling, etc.) were discovered by studying marine actinomycetes, which have recently garnered a lot of interest. Different genera of actinomycetes, including Streptomyces, Actinomyces, Arthrobacter, Corynebacterium, and Micromonospora, can generate a variety of chemicals with a spacious spectrum of activities spanning various biological aspects [15]. Due to their ability to adapt to a variety of severe environmental factors (variable pH, temperature, salinity), marine actinomycetes secrete these biologically active substances in response to the surrounding stress inflicted upon them [15]. Marine actinomycetes are also rich sources of natural antifouling/antibacterial agents with EC50 values < 25 μg/mL [16]. According to the US Navy program, a safe, eco-friendly antifouling agent must record an EC50 < 25 μg/mL. The LC50 value is the 50% fatal concentration for the tested organism, whereas the EC50 value is the median effective concentration at which the chemical exerts its biological impact in 50% of the tested planktonic organisms. Therefore, for a potential non-toxic and environmentally safe antifouling agent, the LC50/EC50 ratio must be >15, emphasizing the need for relatively low EC50 values during experimentation [17]. These antifouling agents belong to the chemical classes of terpenoids, phenolics, steroids, polyketides, furanone, alkaloids, peptides, and lactones [18].

2. Fouling

Fouling is a term used to describe the deposition of undesirable organic or inorganic materials on external surfaces. There are two major types of fouling: non-biological and biological fouling (biofouling). Non-biological (also known as inorganic fouling) includes the accumulation of corrosions, oils, salt crystals, and ice on submerged surfaces. Biofouling is the undesirable deposition of organic elements secreted by micro- or macro-organisms (biofilm, EPS, etc.) over submerged surfaces [19][20][21]. As the habitual conditions and causative microorganisms vary, medical, maritime, and industrial fouling forms are very different from one another. While maritime and industrial biofouling are combinations of biofilm and macro- and inorganic fouling, medical biofouling is primarily made up of biofilm buildup [22].
Medical fouling may damage indwelling prosthetics, such as fasteners, prosthetic valves, bone plates, dental and orthopedic implants, pacemakers, long-drug-delivery devices, or short-term temporary medical devices, such as catheters, biosensors, ophthalmic lenses, drug-delivery devices, ventilation tubes [23]. Enterococcus faecalis, Staphylococcus epidermidis, Staphylococcus aureus, Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Proteus mirabilis, and Streptococcus viridans are among the organisms that cause infectious biofilm deposition and medical fouling of catheters, tracheal tubes, and ventilators [24][25].
On the other hand, maritime fouling, which affects ships, sonar devices, pipelines, pillars, offshore infrastructures, oil installations and platforms, undersea cables, etc., is the most prevalent type of environmental fouling [22].
After a few seconds from the initial exposure of the submerged surface and the aquatic habitat affluent in nutrients and microorganisms, the multistage process of marine biofouling takes place (Figure 1) [26]. Bacteria initially attach themselves to solid surfaces, colonize, and start secreting extracellular polymeric substances (EPSs). Electrostatic and Van der Walls interactions play a substantial role in the early phases of fouling when bacteria cling to the exposed surfaces.
Microorganisms 11 02444 g001
Figure 1. Stages and different forms of fouling.
In industrial fouling, the shear forces might reduce the likelihood of biofilm deposition on industrial membranes. Although the active sludge produced by membrane filtrations may have strong shear pressures that may nevertheless have higher bacterial populations than in a marine environment, promoting the development of slimy biofilms and the initiation of membrane fouling [27]. 

3. Synthetic Antifouling Strategies and Toxicities Associated with Conventional Antifouling Coatings

Various tactics are used to combat maritime, medical, and industrial fouling. The numerous surface factors that significantly affect biofouling include the surface’s wettability, texture, contours, and colors. Hydrophilic surfaces have high wettability and low surface energy, while hydrophobic surfaces have low wettability and high surface energy. Unexpectedly, surfaces with low adhesion and high hydrophobicity enhance contaminant clearance and self-cleaning. Surfaces with super hydrophilic textures can also show less protein adsorption and bioadhesive characteristics [22].
Sufficient antifouling coatings are also applied to affected surfaces while considering the stability of the hydration layer in the case of superhydrophilic layers, the rate of coating degradation, and the rate of antifouling agent release from the coating layer [3]. These coatings may have synthetic or natural origins. Antifouling coating materials have a variety of modes of action; some reduce macrofouling by inducing algal cellular Ca2+ efflux, which stops development and induces cellular arrest [28]. 
TBT and its derivatives have been used in antifouling coats for commercial ships and hulls for the past decades. It belongs to the class of organic compounds named the trisubstituted organotin compounds (OTCs) and has been used as an antifouling agent along with the other organotin derivatives (monobutyltin (MBT), monophenyltin (MPT), and azocyclotin (ACT) [29][30]. TBT and organotin derivatives are very toxic to several aquatic species [31]. TBT acetate has been lethal to Crassostrea gigas oyster larvae at (50 ngL−1) with a no-observed-effect level conc. (i.e., NOEL) of 20 ngL−1, which denotes the minor difference between both concentrations and the toxicity of TBT [31].
When compared to samples taken in 1986, the content of TBT in oysters (Crassostrea gigas) and mussels (Mytilus edulis) in 1989 was reduced by 25 to 33% after the UK passed legislation to regulate and control the sale of TBT. In the years that followed, oysters with regular shells grew normally with acceptable meat quality [32]. Additionally, organotin chemicals may disrupt the normal interaction between sex hormones and their receptors and impair steroid receptor signaling according to molecular docking studies [29][30].
Antifouling paints have also incorporated both irgarol 1051 and diuron for their algicidal activities. It has been demonstrated that irgarol 1051 and diuron at concentrations above 0.5 μg/L reduce the seagrass Zostera marina’s photosynthetic abilities, which is associated with a prominent reduction in their growth [33]. Depending on the quality of the water and environmental parameters, like temperature, salinity, light, current, etc., the effects of copper-based antifouling chemicals are only transient, lasting between 5 and 12 months [9]. They are best suited for seawater and extremely harmful to freshwater and riverine algae and mollusks. On the other hand, zinc pyrithione found in several antifouling coatings has been found to be exceedingly toxic to aquatic plants and animals despite the fact that it is assumed to be environmentally safe due to its propensity to photo-degrade into less toxic chemicals [9][34].
Since then, numerous studies have been dedicated to finding the optimal antifouling coatings that are biocidal to fouling creatures yet capable of maintaining normal ecological balance (safe and non-toxic to aquatic creatures). An ideal antifouling agent must develop sufficient antifouling activity while imposing the least amount of hazardous effect on the maritime organisms that inhabit the surrounding environments of submerged surfaces. Different types of recently developed antifouling coatings that are utilized to prevent medical fouling [35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50] and maritime/environmental fouling [51][52][53][54][55][56][57][58][59][60][61][62][63] are listed in Table S2.

4. Natural Antifouling Agents (AFs) as an Alternative to Synthetic Antifouling Coatings

Natural AFs are alternatives to synthetic antifouling coatings that are environmentally benign with acceptable compatibilities. Effective fouling prevention without long-lasting negative environmental effects is the key characteristic of an excellent natural antifouling agent [64]. One of the primary sources of production for such chemicals is marine microorganisms. AFs function as inhibitors of metabolic signaling pathways, neurotransmitter disruptors, or anti-bioadhesives that eventually block larval settlement (anti-macrofoulers). While neurotransmitter disrupters cause invertebrate larvae to resist settling, anti-bioadhesive AFs work by altering the proteinaceous surface to remove the surface-level inductive hints [17]. When a natural AF’s fatal dose (LC50) to minimal concentration inhibiting settling (EC50) ratio (LC50/EC50) is more than 15, it is deemed non-toxic [17][64].
The terpenoids (terpenes) extracted from the red alga Laurencia rigida prevent the larvae of Amphibalanus amphitrite (also known as Balnus Amphitrite) and Bugula neretina from forming settlements [65][66]. L. rigida extracts are rich in terpenoids, elatol, and deschloroelatol; anti-settlement activity against the barnacle larvae was tested using cyprids of Amphibalanus amphitrite (also known as B. amphitirite) against three synthetic antifouling agents, irgarol 1051, Sea-Nine 211, and nopcocide N-96. Both terpenoids inhibited the attachment of B. amphitirite cypris larvae at a conc. of 10 ng cm−2 with etalol inhibiting 100% of larval settlement and deschloroelatol exerting 90% inhibition. The control synthetic antifouling agents were, however, less effective than elatol and deschloroelatol. Irgarol 1051 was the least active compound at 10 ng cm−2. It is interesting to highlight the eminent lethality of both elatol and deschloroelatol to B. amphitrite nauplii (early larval stages), incurring 100% mortality at 100 ng cm−2 and almost 90% and 50–60% mortality at 10 and 1 ng cm−2, respectively. 
Halogenated terpene derivatives are also useful natural AFs in the prevention of larval adhesion. Sargassum tenerrimum phlorotannins hinder the metamorphosis of Hydroides elegans [67]. S. tenerrimum extract is opulent with phlorotanins, phloroglucinol, and tannic acid. The compounds elucidate variable anti-adhesive potentialities against Hydroides elegans larva settlement. Phlorotanins attain high safety profiles since the reported LC50 score was 27 times higher than their EC50 score, which were 13.984 ppm and 0.526 ppm, respectively. This gives an LC50/EC50 score of 26 for S. tenerrimum phlorotanins. Phloroglucinol reports an EC50 score of 5.231 ppm and an LC50 score of 206.823 ppm (LC50/EC50 ratio of 38).
At non-toxic doses, the gorgonian Junceella juncea diterpene extract exhibits potent antifouling activity against A. amphitrite larval colonization [68]. The J. juncea extract rich with briarane diterpene, including juncin ZII, attained moderate insecticidal and antifeedant activity against Spodoptera litura second-instar larvae when compared to synthetic material, azadirachtin. When tested against Balanus amphitrite settlement, juncin ZII exerted significant anti-settlement effects with an EC50 score of 0.004 μg/mL [68]. The brown seaweed Canistrocarpus cervicornis’ dolastane, seco-dolastane diterpene, and isolinearol affluent extract hinder Perna perna mussel settlement [69].
The Streptomyces tumemacerans albofungin is a potent antifouling agent with an equivalent efficacy to butenolide against Amphibalanus amphitrite larvae and an EC50 score of 1.6 μg/mL. It also acquires acceptable safety profiles with an LC50/EC50 ratio > 100 even when used at high concentrations (up to 40 μg/mL) [70]. The anti-adhesive characteristics of the previously mentioned natural antifouling agents may be assigned to the inhibition of the phenoloxidase and tyrosinase enzymes that regulate the crosslinking and creation of the adhesive plaques needed to anchor the mussels’ byssal and substrata. This was observed when arctic marine sponge Stryphnus fortis bromotyrosine-rich extract blocked blue mussel phenoloxidase and hindered their settlement [71]. 
The first known antifouling benzenoid, 3-chloro-2,5-dihydroxybenzyl alcohol, retrieved from Ampelomyces sp. UST040128, is known for its anti-larval settlement effect against both Balanus amphitrite cyprids and Hydroides elegans larvae. Its EC50 score for B. amphitrite ranged from 3.19 μg/mL to 3.81 μg/mL, and the LC50 score was 266.8 μg/mL. Upon testing on Hydroides elegans, the observed effect was dose-dependent, and the EC50 score was 0.67 μg/mL to 0.78 μg/mL, and the LC50 value was 2.64 μg/mL [72].
Amibromdole isolated from Sarcophyton sp. fungus is a halogenated benzenoid with powerful antifouling activity against Balnus amphitrite. Similarly, pestalachlorides E and F secreted by the fungal strain Pestalotiopsis ZJ-2009-7-6 elucidates strong antifouling activity against B. amphitrite larval settlement [16]. Both compounds have EC50 scores ranging from 1.65 to 0.55 μg mL−1 against the barnacle Balanus amphitrite’s larval settlement with an LC50/EC50 score > 15, suggesting their safety and efficacy [73].
Dihydroquinolin-2-one-containing alkaloids isolated from Scopulariopsis sp. fungal extracts are known for their eminent anti-macrofouling vigor against Balanus amphitrite larval colonization with acceptable safety and therapeutic profiles [74]. The dihydroquinolin-2-ones have average EC50 scores of ~25–50 μg/mL and LC50 scores of ~3.79–7.85 μM when tested against the brine shrimp A. salina [74]. They are also known for their bactericidal effects against the fouling bacterial species S. aureus, B. cereus, V. parahaemolyticus, N. brasiliensis, and P. putida, with MIC scores of 0.78, 1.56, 6.25, 0.78, and 1.56 μM, respectively [74].
The N-methyltetrahydroellipticine and furoquinoline alkaloids, kokusaginine and flindersiamine, purified from Atlantic yellow guatambu’ Aspidosperma australe and white guatambu’ Balfourodendron riedelianum trees elucidate eminent anti-macrofouling potential against the Mytilus edulis platensis mussel [75]. A. australe bark extract was opulent with pyridocarbazole olivacine, indole alkaloids uleine, and N-methyltetrahydroellipticine, where N-methyltetrahydroellipticine yielded the best anti-adhesive macrofouling activity with an EC50 value of 1.56 nmol cm−2 against Mytilus edulis platensis mussels. Second to N-methyltetrahydroellipticine in its anti-macrofouling vigor is the kokusaginine retrieved from B. riedelianum bark extract that scored an EC50 value of 3.86 nmol cm−2. The others, flindersiamine, olivacine, and uleine, recorded EC50 scores of 5.56, 7.59, and 9.95 nmol cm−2, respectively.

5. Marine Actinomycetes as Sources of Natural Antifouling Agents

Actinomycetes, in particular, marine actinomyctes, are highly important industrial sources of secondary metabolites that include a wide range of antimicrobial, antibacterial, and antifouling agents. They belong to the Gram-positive bacterial order Actinomycetales and display a wide range of distinctive features, such as habitat, ideal pH, thermophilicity, and moisture tolerance. They interact with a wide range of aquatic animals, including invertebrates, like sponges, corals, and echinoderms, as well as vertebrates, like pufferfish corals, and a variety of invertebrates [76][77]. The evolution of secondary metabolic pathways may be influenced by these interactions, which may promote particular chemical ecologies. Although most strains have been identified from sediments, marine actinomycetes can coexist with other species and live in both planktonic and biofilm habitats [13].

5.1. Antifouling Agents from the Streptomycetaceae Family

Several bioactive compounds that are helpful in various aspects (agriculture, biotechnology, etc.) are generated within microbes belonging to the Streptomycetaceae family. Streptomyces is the most investigated genus among Streptomycetacea members, and several of its species have been found to have insecticidal, larvicidal, pesticidal, acaricidal, antifouling, and nematocidal action [15]. Streptomyces sp. is non-motile, filamentous, Gram-positive bacteria with aerial hyphae that generate long spore chains (>50) [78]. Numerous antifouling substances are secreted by Streptomyces sp.; these include terpenes, alkaloids, and quorum-sensing inhibitors.

5.2. Antifouling Agents from Micromonosporaceae, Nocardiaceae, and Pseudonocardiaceae Families

The actinomycetes Micromonosporaceae family includes the Micromonospora genus that develops highly branched substrate hyphae but infrequently shows sparse aerial hyphae [79]. The aerobic actinomycetes make up the Nocardiaceae family, which is distinguished by filamentous growth and genuine branching. Nocardia sp. is a catalase- and urease-positive organism that can grow on a variety of media, including basic blood agar, a Löwenstein–Jensen medium, and Sabouraud dextrose agar [80]. Finally, the solitary member of the suborder Pseudonocardineae is the family of bacteria known as Pseudonocardiaceae, and they include several genera, Actinocrispum, Haloactinomyces, and Allosaccharopolyspora [81]. These families have recently garnered a lot of attention as a prospective source of new, physiologically significant chemicals.

6. Obstacles Facing Commercial Use of Natural Antifouling Agents

A significant barrier to converting marine natural chemicals into commercial goods has always been the question of supply. As previously discussed, the extracts from marine actinomycetes represent promising antibacterial and antifouling agents; however, the yield is relatively low, and the retrieved volumes are usually not suitable for commercial usage. Thus, chemical synthesis studies should be expanded to facilitate the production of natural AF agents on larger scales. For instance, laboratory-produced monoterpene–furan geraniol hybrid molecules effectively suppressed cypris larvae of the barnacle Balanus Amphitrite more than the natural parent did [82].
The late-stage divergent method is used to formulate hybrid compounds of geraniol and butenolide. The butenolide moiety was built by ring-closing metathesis, and the eight synthetic hybrid compounds were biologically assessed. The synthetic hybrids attain anti-macrofouling activities against Balanus Amphitrite cyprid larva with EC50 values of 0.30–1.31 μg mL−1. This outcome paved the way for the successful hybridization of the geraniol and butenolide structural motifs that are associated with high anti-macrofouling activities [83].
Further, nine antifouling hybrid compounds were formulated and biologically tested by combining a dihydrostilbene scaffold with the oxime moiety prevalent among the structures of marine antifoulants. The generated hybrids exert aligicidal activity that prohibited microalgae settlement and proliferation with the best-performing hybrid recording an MIC score of 0.01 μg/mL [84].
The C24–C40 section of aculeximycin is stereo-selectively synthesized through epoxy-opening rearrangement events and Kobayashi aldol reactions. First, the C25–C32 segment was formulated by a Kobayashi aldol reaction followed by epoxidation and Jung rearrangement of epoxide 9. The other segment C33–C40 was formulated by a Kobayashi aldol reaction only. For the final step, both segments were fused by an adol reaction that converts ethyl ester to ethyl ketone followed by subsequent dehydration [85]. Justicidin B can be also laboratory hybridized through Suzuki–Miyaura cross-coupling of a triflated naphthalene lactone intermediate and various potassium organotrifluoroborates [86].
The second barrier before the development of AF compounds is the need for rigorous, reliable, and broad-spectrum bioassay systems in research labs, which is yet unfulfilled. Several marine organisms were used during the assessment of the anti-micro/microfouling agent activities for the compounds of interest (larva, algae, bacteria, fungi, etc.). A common feature observed among these assays was the variability of the test outcomes due to the different experimenting techniques that affect the overall reliabilities of the performed tests. It is a prerequisite to develop anti-microfouling and anti-macrofouling bioassay systems that include as many target species as feasible. A robust anti-macrofouling bioassay system should include sessile hard foulers that are regularly found in fouling communities, such as barnacles and tube-building worms, as well as soft foulers, such as the bryozoan B. neritina or seaweed, such as Ulva. Collaboration among research labs should be encouraged to overcome geographic constraints [87].

7. Conclusions

Considering that the largest untapped source of natural goods is still marine microorganisms, a wide variety of novel actinomycetes strains were recovered from different marine environments over the past years. The Micromonosporaceae, Nocardioidaceae, Pseudonocardiaceae, and Streptomycetaceae actinomycetes families were home to the organisms that were most frequently isolated from the marine sediments. The collected marine organisms were profitably and effectively utilized to extract brand-new compounds that belonged to a variety of antifouling agent classes. These compounds have shown positive anti-microfouling and anti-macrofouling properties that will enable their application as marine and medicinal antifouling agents for future applications. To provide a complete and detailed description of these novel antifouling agents, research on the molecular mechanisms of action of these antifouling compounds needs to be conducted. Different optimization techniques should be implemented to improve the yield of natural antifouling agents with actinomycetes. The introduction of genetic modification techniques will revolutionize the industry of natural antifouling agents.

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms11102444

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