A Review on the Importance of Mangroves as a Source of Entophyte Microorganisms with Potential Use in the Pharmaceutical Industry. Potentialities in Colombia.

Giorgio Anfuso, Bolivar-Anillo HJ, Hernando SM, Visbal AZ, Serrano MC and Diego AVD

Published on: 2019-11-17

Abstract

Mangrove forests are composed of different species of plants with morphological, physiological and reproductive characteristics that allow them to settle on saline soils. Along tropical and subtropical coastal regions they give rise to a special ecosystem developed in a critical interface between terrestrial, estuarine and nearshore marine environments. Further, they are considered one of the most productive and valuable natural ecosystems on the planet due to their ecological and socioeconomic importance and their function as protectors of coastal ecosystems and human occupations.

Keywords

Mangrove forests; Entophyte microorganisms

Mangrove Forests in Colombia

Mangrove forests are composed of different species of plants with morphological, physiological and reproductive characteristics that allow them to settle on saline soils. Along tropical and subtropical coastal regions they give rise to a special ecosystem developed in a critical interface between terrestrial, estuarine and nearshore marine environments. Further, they are considered one of the most productive and valuable natural ecosystems on the planet due to their ecological and socioeconomic importance and their function as protectors of coastal ecosystems and human occupations [1-3]. Currently, mangrove forests occupy approximately 14 million hectares, of which more than two thirds are located in eighteen countries: indonesia, brazil, australia, mexico, nigeria, malaysia, myanmar, bangladesh, cuba, india, papua new guinea, colombia, guinea bissau, mozambique, madagascar, philippines, thailand and vietnam [3,4]. Of the 14 million hectares, latin america and the caribbean own 26% and 80% of these are located in six countries: brazil, mexico, cuba, colombia, venezuela and honduras [5]. Although the loss of mangrove forests has been reduced in the last two decades, are still recorded rates of loss of up to 3.1% per year in some countries; this process will lead to a loss of their functionality in less than 100 years [3,6]. Colombia is the only south american country with coasts on the pacific ocean and the caribbean sea that sum approximately 3,000 km [7]. Differences in rainfall patterns on both coasts control and determine mangrove cover, with approximately 292,724 ha on the pacific coast and 87,230 ha on the caribbean coast, for a total of approximately 379,954 ha consisting of 8 mangrove species: avicennia germinans, laguncularia racemosa, conocarpus erectus, pelliciera rhizophorae, rhizophora mangle, r. Harrisonii, r. Racemosa and mora oleifera [8]. However, it is estimated that in the last 30 years approximately 40,000 ha of mangrove forest in colombia have been altered mainly by anthropogenic activities (construction of roads, tourist infrastructures, expansion of urban, agricultural and industrial frontiers, deforestation, among others) [9,10]. In addition, climate change scenarios for the colombian coastal zone predict that mangroves will be greatly affected by rising sea level and coastal erosion processes [11]. The alteration and/or disappearance of the mangrove swamp will not only lead to the loss of this strategic ecosystem and associated services, but will also cause a great loss of the microbial biodiversity associated with this ecosystem, which actually in colombia is a little explored area, especially in relation to endophytic microorganisms.

Mangrove Endophytes with Potential Use in the Pharmaceutical Industry

Endophytes are microorganisms found within plant tissues, for at least a part of their life cycle. Such microorganisms never cause disease to their hosting plants, to which they generally offer multiple benefits e.g. favoring the solubilization of phosphates, production of phytohormones, nitrogen fixation, production of secondary metabolites with antimicrobial activity, etc. [12,13]. All plants host one or more species of endophytic microorganisms but only a small number of them have been thoroughly studied [14,15]. The characteristics of the population of these microorganisms depend on conditions such as the species and stage of growth of the plant and the environmental conditions in which the plant develops [16]. In this sense, Colombia is considered the second country in the world with the greatest diversity of plants, with 1,500 exclusive species (17). Despite this immense biodiversity of flora, few plant species in Colombia have been studied from the point of view of their endophytic microbiota and very few investigations have been carried out about their potential use in the pharmaceutical industry. Therefore, Colombia is considered a potential source of these microorganisms and the secondary metabolites associated with them [18]. Endophytes have the capacity of synthesize a wide range of bioactive metabolites with different properties and a single strain has the capacity of produce multiple variants, which means that the search for new endophytes and their metabolites could increase the possibility of finding new natural bioactive products (Figure 1) [16,19,20].

 

Figure 1: Mangrove endophytes as a source of bioactive molecules.

 

Although mangrove endophytic microorganisms have been extensively studied in Southeast Asia, the endophytic microbiota of the extensive mangrove forests of the Americas and the Caribbean remain largely unexplored [21]. Different studies have shown that the endophyte microbiota of mangroves are promising sources of bioactive molecules [21]. In this sense, Wang carried out a very complete review on the natural compounds obtained from endophytes of mangrove fungi where secondary bioactive metabolites are described, among them terpenes, chromones, coumarins, polyketides, alkaloids and peptides with diverse structural features, many of which presented activities such as cytotoxicity against cancer cells, anti-HIV, antibacterial and antioxidants [26]. Demers investigated the capacity of endophytic fungi isolated from different species of mangroves (Rhizophora mangle, Avicennia germinans, Laguncularia racemose) and trees associated to mangroves (Conocarpus erectus and Coccoloba uvifera) in Florida (USA), to demonstrate that extracts obtained from endophyte microorganisms are active against different microorganisms of clinical relevance: Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter cloacae, Mycobacterium tuberculosis, Naegleria fowleri and Leishmania Donovani. Ding Isolated From The Species Bruguiera Gymnorrhiza A Strain Identified As Streptomyces Sp. JMRC:ST027706 With The Capacity Of Producing Bacaryolane A-C, Where Bacaryolane B Showed Activity Against Bacillus Subtilis [22]. Ding Isolated From The Mangrove Species Kandelia Candel A Strain Identified As Streptomyces Sp. HKI0595 Which Was Able To Produce Three Novel Indolosquiterpenes, Xiamycin B, Indosespene, And Sespenine Which Presented Moderate To Strong Antimicrobial Activities Against Several Bacteria Of Clinical Interest, Including Methicillin-Resistant Staphylococcus Aureus And Vancomycin-Resistant Enterococcus Faecalis [23]. Cai Isolated From Acanthus Ilicifolius The Strain Identified As Phomopsis Sp. HNY29-2B Which Was Able To Produce The Molecules Identified As Acropyrone, Ampelanol And Phomopyrone A, The Latter Presenting Antimicrobial Activity against Bacillus subtilis and Pseudomonas aeruginosa [24]. Moron isolated from different mangrove species (Avicennia officinalis, A. rumphiana, Aegiceras corniculatum, Bruguiera gymnorrhiza, Camptostemon philippinense, Excoecaria agallocha, Lumnitzera litorea, Rhizophora apiculata, and R. stylosa, Avicennia marina, Avicennia sp., A. corniculatum and Sonneratia alba) different strains of endophytic fungi identified as: Arthrinium phaeospermum, Colletotrichum siamense, C. tropicale, Fusarium oxysporum, F. chlamydosporum, F. proliferatum, F. solani, Lasiodiplodia theobromae, Nodulisporium sp., Paecilomyces formosus, Penicillium citrinum, and Pestalotiopsis microspora whose extracts showed a different level of activity against clinically important bacteria and fungi such as Escherichia coli, Klebsiella pneumoniae, Serratia marcescens, Staphylococcus aureus and Candida albicans [25]. These investigations highlight as the microorganisms associated with the mangrove forest, especially the endophytes, represent a rich source of molecules with great interest in the pharmaceutical industry. Despite Colombia has a total area of approximately 379,954 ha of mangrove forests (with 8 species) on its two coasts, which present very different environmental conditions suggesting the presence of a wide diversity of endophytes, the mangroves still remain unexplored. It should be noted that the mangroves of Colombia are under strong anthropic pressure which could put at risk the wide associated diversity, making necessary to develop future research aimed not only at the protection and conservation of this ecosystem but also devoted to the investigation of new molecules of pharmaceutical interest through the isolation, identification and study of secondary metabolism of microorganisms associated with mangroves with special attention to endophytes.

 

 

Acknowledgments

This Research Is A Contribution To The Andalusia PAI Research Group RNM-328, The RED PROPLAYAS Network, The University Simon Bolívar (Barranquilla, Colombia) And The Center For Marine And Limn logical Research Of The Caribbean CICMAR (Barranquilla, Colombia).

References

  1. Angarita JL, Roberts CM, Tilley A, Hawkins JP, Cooke RG. Mangroves and people Lessons from a history of use and abuse in four Latin American countries. Ecol Manag. 2016; 368: 151-162.
  2. Jia M, Wang Z, Zhang Y, Mao D, Wang C. Monitoring loss and recovery of mangrove forests during 42 years. The achievements of mangrove conservation in China. Int J Appl Earth Obs Geoinf. 2018; 73: 535-545.
  3. Sanderman J, Hengl T, Fiske G, Solvik K, Adame MF, Benson L, et al. A global map of mangrove forest soil carbon at 30 m spatial resolution. Environ Res Lett. 2018;13:5.
  4. Barbier EB. The protective service of mangrove ecosystems. A review of valuation methods. Mar Pollut Bull Internet. 2016; 676-681.
  5. Lacerda LD de, Borges R, Ferreira AC. Neotropical mangroves. Conservation and sustainable use in a scenario of global climate change. Aquat Conserv Mar Freshw Ecosyst. 2019; 1-18.
  6. Polidoro BA, Carpenter KE, Collins L, Duke NC, Ellison AM, Ellison JC, et al. The loss of species: Mangrove extinction risk and geographic areas of global concern. PLoS One. 2010.
  7. Polania J, Urrego LE, Agudelo CM. Recent advances in understanding Colombian mangroves. Acta Oecologica. 2015; 63: 82-90.
  8. Palacios ML, Cantera JR. Mangrove timber use as an ecosystem service in the Colombian Pacific. Hydrobiologia. 2017; 345-358.
  9. Blanco JF, Estrada EA, Ortiz LF, Urrego LE. Ecosystem wide impacts of deforestation in mangroves. The Uraba Gulf Colombian Caribbean Case Study. ISRN Ecol. 2012; 2012 :1-14.
  10. Sanchez H, Bolívar AHJ, Villate Daza D, Escobar Olaya G, Anfuso G. Influencia de los impactos antropicos sobre la evolucion del bosque de manglar en Puerto Colombia Mar Caribe colombiano . Rev Latinoam Recur Nat. 2019;  1-16.
  11. RodrIguez A, Tinoco A, LeOn JG, Jutinico L, Santos Acevedo, M Acosta A, Gonzalez J, et al. Estado del conocimiento y vacio de informacion. In INVEMAR, editor. Informe del estado de los ambientes y recursos marinos y costeros de Colombia. 2017; 2018:155-169.
  12. Le Cocq K, Gurr SJ, Hirsch PR, Mauchline TH. Exploitation of endophytes for sustainable agricultural intensification. Mol Plant Pathol. 2017; 469-473.
  13. Ludwig Müller J. Plants and endophytes.equal partners in secondary metabolite production. Biotechnol Lett. 2015; 1325-1334.
  14. Aly AH, Debbab A, Kjer J, Proksch P. Fungal endophytes from higher plants. A prolific source of phytochemicals and other bioactive natural products. Fungal Divers. 2010; 41: 1-16.
  15. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN. Bacterial endophytes. Recent developments and applications. FEMS Microbiol Lett. 2008; 278:1-9.
  16. Gouda S, Das G, Sen SK, Shin HS, Patra JK. Endophytes.A treasure house of bioactive compounds of medicinal importance. Front Microbiol. 2016; 7:1-8.
  17. Rangel ch JO. La biodiversidad de Colombia significado y distribucion regional. Rev la Acad Colomb Ciencias Exactas, Fiisica y Nat. 2015; 176-200.
  18. Anillo HB, Sanchez CO, da Silva Lima G, Franco dos Santos G. Endophytic Microorganisms Isolated of Plants Grown in Colombia. A Short Review. J Microb Biochem Technol. 2016; 8: 509-513.
  19. Brien PA. Biological control of plant diseases. Australas Plant Pathol. 2017; 46: 293-304.
  20. Yu H, Zhang L, Li L, Zheng C, Guo L, Li W, et al. Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol Res. 2010; 437-449.
  21. Demers DH, Knestrick MA, Fleeman R, Tawfik R, Azhari A, Souza A, et al. Exploitation of mangrove endophytic fungi for infectious disease drug discovery. Mar Drugs. 2018; 1-11.
  22. Ding L, Goerls H, Dornblut K, Lin W, Maier A, Fiebig HH, et al. Bacaryolanes AC, Rare Bacterial Caryolanes from a Mangrove Endophyte. J Nat Prod. 2015; 2963-2967.
  23. Ding L, Maier A, Fiebig HH, Lin WH, Hertweck C. A family of multicyclic indolosesquiterpenes from a bacterial endophyte. Org Biomol Chem. 2011; 4029-4031.
  24. Cai R, Chen S, Liu Z, Tan C, Huang X, She Z. A new a pyrone from the mangrove endophytic fungus Phomopsis sp. HNY29 2B. Nat Prod Res. 2017; 124-130.
  25. Moron LS, Lim Y. Antimicrobial activities of crude culture extracts from mangrove fungal endophytes collected in Luzon Island, Philippines. Philipp Sci Lett. 2018; 11:28-36.

Wang KW, Wang SW, Wu B, Wei JG. Bioactive Natural Compounds from the Mangrove Endophytic Fungi. Mini Reviews Med Chem. 2014; 370-391.