Siderophores from Marine Bacteria with Special Emphasis on Vibrionaceae

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 Available online at www.ijpab.com

DOI: http://dx.doi.org/10.18782/2320-7051.7492 ISSN: 2320 – 7051 Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) Review Article

Archana V.1, K. Revathi2*, V. P. Limna Mol3, R. Kirubagaran3 1Department of Advanced Zoology and Biotechnology, Madras University, Chennai- 600005 2MAHER University, Chennai, Tamil Nadu – 600078 3Ocean Science and Technology for Islands, National Institute of Ocean Technology (NIOT), Ministry of Earth Sciences, Government of India, Pallikaranai, Chennai- 600100 *Corresponding Author E-mail: [email protected] Received: 11.04.2019 | Revised: 18.05.2019 | Accepted: 25.05.2019

ABSTRACT More than 500 siderophores have been isolated from a huge number of marine bacteria till date. With mankind’s ever-increasing search for novel molecules towards industrial and medical applications, siderophores have gained high importance. These chelating ligands have immense potential in promoting plant growth, drug-delivery, treatment of iron-overload, etc. Many of the potential siderophores have been isolated from bacteria like Pseudomonas, Bacillus, Nocardia, etc. Bacteria belonging to the family Vibrionaceae have recently gained focus owing to their rich potential in secreting siderophores. Many of the vibrionales, viz. Vibrio harveyii, V. anguillarium, V. campbellii. etc. are aquatic pathogens. These bacteria require iron for their growth and virulence, and hence produce a wide variety of siderophores. The genetic basis of siderophore production by Vibrio sp. has also been largely studied. Further detailed genetic analysis of the mode of siderophore production by Vibrionaceae would be highly effective to treat aquaculture diseases caused by these pathogenic organisms.

Key words: Marine bacteria; Siderophore; Vibrionaceae; Bioactivity; Vibrio campbellii.

INTRODUCTION microbial types. Marine bacteria are defined The earth is mainly surrounded by the ocean41. by bacteria living in a marine environment The marine environment harbours huge ranging from pelagic to benthic ecosystems, in biodiversity and is a potential source of marine which salinity plays a vital role9. The essential microorganisms with extensive applications5. contribution of marine microbial communities The fundamental sources for growth and is in global biomass, nitrogen cycling, and survival of plants and animals are abundantly biodiversity50. The prokaryotic microbes lead a available in the marine environment. The sea key role in Fe Cycling to release the energy water contains 1 million microorganisms per and matter and to maintain ecosystem milliliter, which includes several thousands of functioning25,35.

Cite this article: Archana, V., Revathi, K., Limna Mol, V. P., Kirubagaran, R., Siderophores from Marine

Bacteria with Special Emphasis on Vibrionaceae, Int. J. Pure App. Biosci. 7(3): 58-66 (2019). doi: http://dx.doi.org/10.18782/2320-7051.7492

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 Marine microbes are involved in the have also been resolved27. Siderophore peptide fundamental aspects of controlling the backbone is usually made up of several environment based on biogeochemistry44. analogs of nonprotein amino acids, including Marine microbes are free-living which modified and D-amino acids14. Some bacteria supports research which exhibits the produce one type of siderophore while many biogeographic pattern30. Approaches towards produce multiple types of siderophore that the marine microbes were significantly enable microbes to grow in different changed by researchers to isolate the various environments7. potential bioactive products37. The objective of this review is to peruse the Gram-negative bacteria can survive available literature to explain the importance better in the rough oceanic environment of iron for bacterial growth and virulence, because of the cell membrane structure and general contour of the iron Lipopolysaccharides (LPS). The outer assimilation system, role of siderophores in membrane LPS triggers the immune response marine ecosystem with special reference to which leads to infection and even causes siderophores from marine Vibrionaceae. death32,47. Marine bacteria have been found to 1. Siderophore : an overview be a great source of novel bioactive Most of the organisms require iron as an compounds, with more than a thousand essential element in a variety of metabolic and compounds being isolated and screened for the cellular pathways due to its unique chemical potential to produce contemporary medicine22. properties. Iron-containing cofactors such as Metabolic activity of bacterium requires iron iron-sulfur clusters or heme groups are found for its growth and survival. Iron exists in two to be present in over 100 enzymes that act in forms, either as Ferrous Fe II or insoluble processes of primary and secondary ferric Fe III, but in the oceanic environment, it metabolism. Its ability to coordinate and is present in the ferric condition due to the trigger oxygen and to get ideal oxidation neutral to alkaline pH34. Although the chemistry for involvement in electron bacterium requires an easily soluble ferrous transport and metabolic processes makes iron form, survival in the aerobic environment was most suitable for catalyzing broad spectrum of a difficult task. However, in the aerobic a redox reaction29,36. condition under certain biological pH, ferrous Fe (II) is soluble in aqueous solution at is oxidized to ferric iron34. Further, to neutral pH and, if the reductive state is overcome this condition of low iron maintained, is, therefore, sufficiently available availability and to sustain in the aerobic for living cells. In general, omnipresent condition, bacteria developed an interesting divalent metal transporters can be taken mechanism to assimilate the iron from any over8,3,29. In bacteria8 and fungi16, specific Fe given environment by secreting iron-carrying (II)) uptake systems are known. However, Fe or binding molecules, literally coined as (II) is oxidized to Fe (III)) in most microbial siderophores33. habitats either spontaneously by reacting in Siderophore, literally coined as an iron host organisms with molecular oxygen or chelating compound19, are low -molecular enzymatically during assimilation and weight ligands (20-2000 Da) produced to circulation. Knight et al.42 Fe (III) forms ferric hydrolyze and metabolize iron by bacteria, oxide complex in the environment. Fe (III)) fungi and plants36. The iron ligation groups forms complexes of ferric oxide hydrate in the were tentatively classified into three major presence of oxygen and water with neutral to chemical types: Hydroxamate, Catecholate, basic pH. These complexes are very stable, and Hydroxy carboxylates; However, other resulting in a free concentration of Fe (III)27,34. siderophore structures, including oxazoline, Using multiples of membrane-bound iron thiazoline, hydroxypyridinone, α- and β- siderophore receptors, iron-coordinated hydroxy acids and α-keto acid components, siderophore (III) are accumulated by Copyright © May-June, 2019; IJPAB 59

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 microorganisms through facilitative transport. types of siderophores are Catecholate, Iron is predominantly removed from Hyroxymates, carboxylate and mixed ligands. siderophore by a redox-mediated process the 3. Sources of Siderophores affinity of iron (II) siderophore is much lower Most of the microorganisms produce a wide than that of iron (III)38. Some siderophores range of siderophores (iron-chelators) in iron- may be secreted to deprive the competing deficient marine ecosystems. Four significant organisms of iron, which will in turn influence environmental habitats occur naturally: soil the ecology of the environment that the and surface water, marine water, plant tissue secreting colony occupies17,23. The correlation (pathogens) and animal tissue (pathogen). For between siderophore production and virulence bacteria and fungi, the soil is a rich source of is strong for some microorganisms12. The habitat. Generally, gram-positive species are fundamental role of siderophore is involved in those belonging to the Bacillus, Arthobacter, the acquisition of high affinity and receptor- Actinomycetales and Nocardia genera. Almost dependent ferric ion transport. Siderophore all of these microbes produce and secrete production regulation is based on iron ferrioxamines that promote growth not only of concentration in the environment24. the producing organisms but also for other 2. Types of Siderophores microbial population that can avail it. Microbial products, especially secondary Aspergillus and Penicillium, which mainly metabolites can be considered as siderophores produce ferrichromes are soil fungi. This when they possess characteristics such as iron group of siderophore is made up of cyclic chelating property. Iron level plays a vital role hexapeptides and therefore highly resistant to in the biosynthesis of siderophores and has the environmental degradation due to the wide capability to transport across the membrane48. range of hydrolytic enzymes present in the Including secondary metabolites, different and soil49. The pH values of soils containing complex chemical structures within the decaying plant materials are as low as 3-4. siderophore are typical, preventing their Because of the extreme acid stability of these unambiguous and universal classification. molecules, organisms producing hydroxamate Even though siderophore biosynthesis and siderophore have an advantage under such structural characteristics are diverse, a conditions. Freshwater lakes also contain large classification scheme will be arbitrary to some Pseudomonas, Azomonas, Aeromonas and extent. Metrics may include source organisms Alcaligenes species populations6. (bacteria, fungi, plants), backbone character Unlike most freshwater sources, surface (peptide or nonpeptide, cyclic or open-chain), sea-water iron levels are extremely low (1nM or chelating group character15. Given the to 1 μMin the upper 200 m) and much lower considerable structural variation found in than those of V, Co, Ni, Cu and Zn. Almost all siderophores, their common feature is to form of this iron is in the state of iron (III) and high thermodynamic stability six-coordinate complex to organic ligands Rue and Bruland40. complexes with iron (III). Ligating groups The distinct nature of the marine pelagic contain hydroxamate, catecholate, α- atmosphere promotes large diffuse losses and hydroxycarboxylic acids and α-keto carboxylic poses a problem with the efficiency of normal acids of oxygen atoms39. siderophore based iron uptake strategies. Many Additionally, siderophores with various heterotrophic marine bacteria, however, binding groups of Fe (III) ions, such as produce siderophore, although they have salicylic acid, oxazoline, and thiazoline different properties than those produced by nitrogen, and even negative nitrogen as in the terrestrial organisms. Marine siderophores are case of maduraferrin) were isolated1. active on the surface and tend to form Extensive reviews are available on the molecular aggregates. structural variety of siderophores45. Major

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 4. Applications of Siderophores or on normal components of erythrocytes. Only approximately 1% of marine bacteria can These agents have been effective against all be cultured in the laboratory. Siderophore parasite growth. enhances the growth in artificial media of 5. Siderophores from marine Vibrionaceae unculturable microorganisms. The siderophore Vibrionaceae family is widely distributed in based approach has made it possible to the marine environment comprising of several cultivate organisms that are only remotely species which cause diseases to human beings related to microbes previously grown. For and animals2. Subsequently, Vibrios have a many strains from this habitat, the lack of profound ability to produce bioactive growth in the laboratory stems from an secondary metabolites28. Like other pathogenic inability to produce siderophore bacteria, Vibrios also require iron for their autonomously, and the resulting chemical growth31. Although covering a limited dependence on other microbes regulates chemical space, Vibrios produce compounds community establishment in the environment. with attractive biological activities, including Siderophores are involved in the growth of antibacterial, anticancer, and antivirulence plant species to increase the yield by activities. This review highlights some of this enhancing the iron uptake to the plant. In group of bacteria’s most interesting structures. agriculture, soil inoculation with Pseudomonas Many of the compounds found in vibrios have putida, which produces pseudobactin, also been isolated from other bacteria that are increases the growth and yield of different distantly related. This cosmopolitan plants demonstrated the presence of occurrence of metabolites indicates a high hydroxamate siderophore in variety. incidence of transferring horizontal genes, Siderophore type hydroxamate present in soil raising interesting issues. Some of these plays an important role in immobilizing the molecules have an ecological function. This metals in these cases. Siderophore production account highlights the pending potential of activity plays a central role in determining the exploring new bioactive compounds bacterial ability of various microorganisms to improve sources and the challenges associated with the development of plants in soil. Siderophore their research28. acts against harmful phytopathogen and holds Vibrio campbellii is a marine gram- the ability to substitute hazardous pesticides. neagtive curved rod-shaped bacterium closely In the Medical field, Siderophore uses linked to its sister species, Vibrio harveyi In the Trojan strategy to form complexes with aquatic organisms, it is an emerging pathogen. antibiotics and helps in the selective delivery Qurom sensing enables the bacterium to of antibiotics to the antibiotic-resistant communicate with autoinducers, a secreted bacteria. Certain iron overload diseases, for chemical signaling molecule. Some V example, Sickle cell anemia can be treated .campbellii strains are known not to be using siderophores. Deferiprone and luminescent; these strains are believed to be Desferrioxamine combined chelation therapy less virulent than the luminescent strains. of thalassemia major disease has also been Siderophore is synthesized and reported. Reversed siderophore acts as an secreted in their environment where they antimalarial activity. The synthetic chelate ferric iron to overcome hunger. Once ferrichromes antimicrobial activity correlated bound, the siderophore receptor recognizes the with their lipophilicity, and this antimalarial ferric iron- siderophore complexes and are activity was averted when applied as iron (II) transported via ABC transporters over the complexes to the chelators. Synthetic membrane using TonB complexes as energy ferrichrome action sites are located in the transducers. intra-erythrocytic parasite and not in the serum

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051

Fig. 1: The organisation of Vibrionaceae siderophore clusters of biosynthesis and the corresponding siderophore schematic structure.a)Biosynthesis clusters of Vibrionaceae and carboxylate and siderophore.b) Catecholatae Vibrionanaceae and biosynthesis cluster mixed catechol/hydroxamate siderophore c) Vibrionaceae siderophore with known biosynthesis gene cluster representation of schematic 2D structure46.

Vibrionaceae siderophore biosynthesis, biscatecholamide compound, divanchrobactin siderophore receptors and phylogenetic (2), and previously reported siderophores, analyses were used to investigate their vanchrobactin (3) and anguibactin (4). organization, distribution, origin and Vanchrobactin is consist of L-serine, D- evolution. Identified nine different siderophore arginine- and 2, 3-dihydroxybenzoic acid, biosynthesis systems and 13 siderophore while trivanchrobactin is a linear trimer of receptors in Vibrionaceae through literature vanchrobactin joined by two serine ester search. Blast searches identified homologs and linkages. The cyclic trivanchrobactin product mapped the results to a phylogeny of was not detected. In addition to siderophore Vibrionaceae. 81 biosynthetic system in 45 production, extracts of Vibrio sp. DS40M4 species of Vibrionaceae and 16 unclassified were screened for biologically active strains of Vibrionaceae and 409 receptors in molecules; anguibactin was found to be 89 species of Vibrionaceae and 49 unclassified cytotoxic against the P388 Murine leukemia strains of Vibrionaceae have been identified46. cell line (IC50 < 15 μM. Most taxa are associated with at least one type Vibrio campbellii BAA-1116 of siderophore biosynthesis system, some of (formerly Vibrio harveyi) is a model organism which are widely distributed in the family for quorum sensing producing anguibactin and (e.g., aerobactin and vibrioferrin), while others amphi-enterobactin siderophore. This study (e.g., bisucaberin and vibriobactin) are found examined the mechanisms and specificity of in one lineage. siderophore uptake in V. campbellii and V. The Vibrio sp. DS40M4 produced a harveyi, and examined the diversity of V. new triscatechol amide siderophore, campbellii and V. harveyi strains in trivanchrobactin (1), a related new siderophore.

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 Electrospray ionization mass spectrometry and enterobactin.V. campbellii HY01 may absorb bioassay revealed that different V. campbellii Amphi-enterobactin via FapA, indicating that and V. harveyi strains produce a series of Amphi-enterobactin production is a common amphi-enterobactins with different fatty acid phenotype among V. campbellii and V. appendages, including several novel amphi- harveyi, whereas earlier work, reported here enterobactins. in, showed that V. campbellii strains are 6. Genetic basis of siderophore production produced only by an anguibactin. In both by V. campbellii anguibactin and Amphi- enterobactin Vibrio campbellii BAA-1116 Amphi biosynthesis, the 2, 3-dihydroxybenzoic acid enterobactin gene cluster harbors a gene called gene, aebA, located in the Amphi-enterobactin fapA, which is a counterpart that encodes Fe gene cluster, suggest the possibility that (III)-siderophore-specific outer membrane Amphi-enterobactin may is a native receptors. Also carrying this cluster including siderophore of V. campbellii and V. harveyi, fapA is another strain, V. campbellii HY01, a while V. campbellii acquired the anguibactin pathogenic strain to shrimp.HY01-derived system during evolution. indicator strains show that the FapA protein Genomic analysis revealed that V. campbelli located in V. campbellii HY01 outer DS40M4 harbors genes related to the transport membrane fraction is essential for the uptake of iron, virulence and environmental fitness, of both Fe (III)-Amphi-enterobactin and such as proteins encoding anguibactin and enterobactin from E. coli, but not V. vanchrobactin. Secretion system for protein, anguillarum RV22 vanchrobactin while V. types II, III, IV and VI and proteorhodopsin anguillarum may use Fe (III)-Amphi- were also present51.

Fig. 2: Complete genomic studies of Vibrio campbellii51

Archana et al Int. J. Pure App. Biosci. 7 (3): 58-66 (2019) ISSN: 2320 – 7051 CONCLUSION 4. Nagoba, B., Vedpathak, D., Medical Siderophores, the iron-chelating compounds, application of siderophore European are usually produced to hydrolyze and Journal of General Medicine. 8(3): 229- metabolize iron by bacteria, fungi and plants. 235 (2011). The siderophore production has mostly been 5. Beygmoradi, A., Homaei, A., Marine linked to virulence and hence, most of the microbes as a valuable resource for brand marine pathogenic bacteria secrete siderophore new industrial biocatalysts. Biocatal Agric molecules. Among these, Vibrionaceae are the Biotechnol 11: 131–152 (2017). focus of current research owing to their 6. Bossier, P., Hofte, M., & Verstraete, W., relevance in aquaculture activities. Many of Ecological Significance of Siderophores in the Vibrio sp. have been widely explored for Soil. Advances in Microbial Ecology, 385– siderophore production, however, emerging 414 (1988). aquaculture pathogens like V. campbellii are 7. Boukhalfa, H., Crumbliss, A. L., Chemical still largely unexplored. Detailed research on aspects of siderophores mediated iron siderophore production potential of Vibrio sp. transport. Biometals. 15: 325–339 (2002). 8. Cartron, J. E. R., Harness, R., Rogers and would be highly beneficial to the aquaculture Manzano, P., Biodiversity, ecosystem and fraternity. conservation in Northern Mexico PP

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