Bioactive Pigments from Marine Bacteria: Applications and Physiological Roles
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Hindawi Publishing Corporation Evidence-Based Complementary and Alternative Medicine Volume 2011, Article ID 670349, 17 pages doi:10.1155/2011/670349 Review Article Bioactive Pigments from Marine Bacteria: Applications and Physiological Roles Azamjon B. Soliev, Kakushi Hosokawa, and Keiichi Enomoto Department of Environmental Systems Engineering, Kochi University of Technology, 185 Miyanokuchi, Tosayamada, Kami, Kochi 782-8502, Japan Correspondence should be addressed to Keiichi Enomoto, [email protected] Received 15 January 2011; Accepted 28 June 2011 Copyright © 2011 Azamjon B. Soliev et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Research into natural products from the marine environment, including microorganisms, has rapidly increased over the past two decades. Despite the enormous difficulty in isolating and harvesting marine bacteria, microbial metabolites are increasingly attractive to science because of their broad-ranging pharmacological activities, especially those with unique color pigments. This current review paper gives an overview of the pigmented natural compounds isolated from bacteria of marine origin, based on accumulated data in the literature. We review the biological activities of marine compounds, including recent advances in the study of pharmacological effects and other commercial applications, in addition to the biosynthesis and physiological roles of associated pigments. Chemical structures of the bioactive compounds discussed are also presented. 1. Introduction a wide variety of diverse biological systems. The Earth’s surface consists of 70% water, which is inhabited by 80% of 1.1. Marine Bacteria and Its Role in Life Sciences. A wide vari- all life forms [1], and consequently aquatic organisms have ety of diseases and medical problems represent a challenging a greater diversity than their terrestrial counterparts. As re- threat to humans, who since ancient times have searched for search into the marine environment is still in its early phases, natural compounds from plants, animals, and other sources many mysteries associated with aquatic fauna and flora have to treat them. Although the process of finding effective treat- ffi yet to be discovered. Therefore, the marine environment ments against fatal diseases is di cult, extensive searches for has recently become an attractive research subject for many natural bioactive compounds have previously yielded some investigations, because of its rich biodiversity. Despite being successful results. The isolation and identification of specific comprised of a diverse ecosystem, the search for marine met- natural compounds led to the development of folk medicine, abolites is difficult because of the inaccessibility and noncul- and humans learned to separate the isolates into medicinal turability of the majority of organisms [2]. Nevertheless, the drugs, which could be used to treat different diseases, and existing technologies like deep seawater pumping facilities, poisonous substances, which could be used for nonmedicinal scuba diving, and other available equipments, have facilitated purposes (i.e., during tribal wars, hunting, etc.). Statistically, at least 50% of the existing drugs that are used to treat human investigation of the sea environment. As a result, scientific illnesses are derived from natural products, most of which research has increasingly focused on marine biochemistry, are obtained from terrestrial organisms [1]. However, due microbiology, and biotechnology. to continuous and exhaustive research, land-based natural Microorganisms and their isolates represent a major bioactive compounds have become increasingly difficult to source of undiscovered scientific potential. It should be noted find. Instead, water-based natural compounds have become that the number of microbial organisms isolated from the a more promising source, not only from a pharmacological vast ocean territories continues to increase each year. Con- view, but also for industrial and commercial applications. sequently, natural products isolated from microorganisms Theoretically, life is considered to have originated in the inhabiting environments other than soil are an attractive sea and, as a result of evolutionary changes, developed into research tool, not only for biochemists and microbiologists, 2 Evidence-Based Complementary and Alternative Medicine but also for pharmacologists and clinicians. Laatsch [3] 2.1. Prodiginines. Red-pigmented prodigiosin compounds described the isolation and description of nearly 250 marine were first isolated from the ubiquitous bacterium Serratia bacterial metabolites versus 150 isolated from terrestrial marcescens and identified as secondary metabolites. The bacteria between 2000 and 2005. Research into marine mi- common aromatic chemical structure of these pigmented croorganisms and their metabolites has therefore become a compounds was first named prodiginine by Gerber [6] major task in the search for novel pharmaceuticals. (Figure 1). Prodigiosin was the first prodiginine for which Although many compounds show promising biological the chemical structure was determined [7]. The name activities, it is difficult to point out any particular bioactive “prodigiosin” has been attributed to the isolation of prodi- agent that has readily been commercialized as a medicine. giosin from Bacillus prodigiosus bacterium (later renamed Currently, 13 natural products isolated from marine micro- Serratia marcescens)[8], which was historically famed for organisms are being tested in different phases of clinical the mysterious “bleeding bread” report [9, 10]. Prodiginines trials, and a large number of others are in preclinical investi- share a common pyrrolyldipyrromethene core structure gations [4], thus highlighting the potential of marine natural and have a wide variety of biological properties, including compounds. antibacterial, antifungal, antimalarial, antibiotic, immuno- Despite thousands of marine bioactive compounds hav- suppressive, and anticancer activities [9, 11]. Such properties ing been isolated and identified, in this paper, we will focus potentially make them one of the most powerful research on the pharmacologically active pigmented compounds pro- tools in the past decade. duced by marine microorganisms exhibiting in vitro or in There are many research reports and reviews regarding vivo biological activities. Although pigmented compounds prodiginines and their biological activity investigations. In produced by terrestrial bacteria are beyond the scope of this addition to the Serratia, several species of marine bacteria review, specific examples will still be mentioned for com- of the genera Streptomyces [8], Actinomadura [8], Pseu- parative purposes, to outline common biological activities or domonas [12], Pseudoalteromonas [13–18], and others [19] because identical pigments were isolated from both types of have also been reported to produce prodigiosin and related microorganisms. compounds. In particular, Alteromonas denitrificans, which was isolated from the fjord systems off the west coast of 1.2. Marine Microorganisms and Their Bioactive Isolates. Norway [16] and later reclassified as Pseudoalteromonas deni- Marine and terrestrial microfloras differ from each other due trificans [20], has been reported to produce cycloprodigiosin. to the influence of their respective environmental conditions. This compound has immunosuppressive, antimalarial, and Microorganisms living in the sea must be able to survive apoptosis-inducing activities [18, 21, 22]. Pseudoalteromonas and grow in the water environment with low nutrition, high rubra, found in the Mediterranean coastal waters [13], salinity, and high pressure. That is why most bacteria isolated also produces cycloprodigiosin, in addition to prodigiosins from seawater are Gram-negative rods, as it is postulated that [14, 15]. α-Proteobacteria isolated from a marine tunicate their outer membrane structure is evolutionarily adapted to collected in Zamboanga, Philippines, was reported to pro- aquatic environmental factors. Marine microorganisms can duce heptyl prodigiosin. In vitro antimalarial activity against be divided on the basis of habitat into psychrophiles (living Plasmodium falciparum 3D7 (IC50 = 0.068 mM and SI = 20) at low temperatures), halophiles (living at high salinity), was about 20 times the in vitro cytotoxic activity against and barophiles (living under high pressure). Although these L5178Y mouse lymphocytes [23]. In vivo experiments using characteristics highlight the differences between marine and Plasmodium berghei-infected mice, at concentrations of terrestrial microorganisms, it remains difficult to separate 5 mg/kg and 20 mg/kg, significantly increased their survival, bacterial genera on the basis of habitat due to the ubiquitous while also causing sclerotic lesions at the site of injection. presence of similar species in both environments. As such, Other bacteria reported to produce red pigments include most bioactive compounds have been isolated from bacteria Hahella [24], Vibrio [25], Zooshikella [26], and Pseudoal- in both environments. teromonas [17], isolated from the coasts of Korea, Tai- Marine bacteria, however, are attractive to researchers wan, and Japan. Kim et al. [27] identified red-pigmented because they can potentially produce compounds with prodiginines from Hahella chejuensis. Nakashima et al. also