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Endophytic Microorganisms of the Tropical Savannah: A Promising Source of Bioactive Molecules

  • Cristina Paiva de Sousa
  • Nadja Fernanda Gonzaga Serrano
  • Paulo Teixeira Lacava
Chapter

Abstract

The Brazilian tropical savannah, known as the “Cerrado”, is comprised of rich and characteristic flora, which makes it one of the 25 most important terrestrial biodiversity hotspots on the planet. This ecosystem is characterized by seasonal weather with annual precipitation that varies between 1200 and 1800 mm and a dry season that occurs during 5–6 months a year. This Brazilian savannah is a typical mosaic biome characterized by plants that can be endemic to this niche and several plant species that have medicinal properties and great pharmaceutical relevance. Although interest has increased in the microbial biodiversity associated with medicinal plants, the diversity, taxonomic composition, and biotechnological potential of endophytic microorganisms associated with these tropical plants from the savannah remain unclear. Plant-associated microorganisms such as endophytes are subjected to constant metabolic and environmental interactions, and these organisms should produce more secondary metabolites. These molecules are characterized by their diverse chemical structures and may be of use due to the wide range of their bioactivity against pathogens. The native plants of the Brazilian savannah are commonly used to treat skin diseases, ulcers, anemia, diabetes, malaria, inflammatory reactions, and hepatic diseases, and this medicinal flora has been used as folk medicine by different people as an alternative to high-priced pharmaceutical drugs. However, only a few of the medicinal Brazilian plants have been studied as a source of bioactive endophytic microbial communities. Several endophytes are important for microbial activities such as antibiotic capability against Gram-positive and Gram-negative bacteria, antifungal, antibiotic resistance, enzyme production, antitumor activity, and anti-Leishimania activity. The exploration of endophytes from new host hosts is important for assessing the potential of these microorganisms in different application areas and for emphasizing the potential of natural compounds that can be used in clinics and the pharmaceutical industry.

Keywords

Actinobacteria Agronomic potential Antimicrobial Bioprospection Biotechnological potential Brazilian tropical savannah Endophytes Bioactive molecules 

References

  1. Adamoli J, Macedo J, Azevedo LG, Madeira Neto J (1985) Caracterização da região dos Cerrados. In: Goedert WJ (ed) Solos dos Cerrados: Tecnologias e Estratégias de Manejo. Embrapa and Nobel Press, São Paulo, pp 33–74Google Scholar
  2. Aghamirian MR, Ghiasian SA (2009) Isolation and characterization of medically important aerobic actinomycetes is soil of Iran (2006–2007). Open Microbiol J 3:53–57CrossRefPubMedPubMedCentralGoogle Scholar
  3. Almeida SP, Proença CEB, Sano SM, Ribeiro JF (1998) Cerrado espécies vegetais úteis. Embrapa, Planaltina, DF, 464pGoogle Scholar
  4. Azevedo JL, Araújo WL (2007) Diversity and applications of endophytic fungi isolated from tropical plants. In: Ganguli BN, Deshmukh SK (eds) Fungi: multifaceted microbes. CRC Press, Boca Raton, pp 189–207Google Scholar
  5. Azevedo JL, Maccheroni W, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65CrossRefGoogle Scholar
  6. Banskota AH, McAlpine JB, Sørensen D, Ibrahim A, Aouidate M, Piraee M, Alarco AM, Farnet CM et al (2006) Genomic analyses lead to novel secondary metabolites. Part 3. ECO-0501, a novel antibacterial of a new class. J Antibiot (Tokyo) 59:533–542CrossRefGoogle Scholar
  7. Batalha MA (2011) O cerrado não é um bioma. Biota Neotrop 11:21–24CrossRefGoogle Scholar
  8. Cao L, Qiu Z, You J, Tan H, Zhou S (2004) Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett Appl Microbiol 39:425–430Google Scholar
  9. Cao J, Jiang Q, Lin J, Li X, Sun C, Chen K (2015) Physicochemical characterization of four cherry species (Prunus spp.) grown in China. Food Chem 173:855–863CrossRefPubMedGoogle Scholar
  10. Carrim AJI, Barbosa EC, Vieira JDG (2006) Enzymatic activity of endophytic bacterial isolates of Jacaranda decurrens Cham. (Carobinha-do-campo). Braz Arch Biol Technol 49:353–359CrossRefGoogle Scholar
  11. Castillo UF, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, Albert H, Robison R (2002) Munumbicins wide spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 148:2675–2685Google Scholar
  12. Castillo UF, Browne L, Strobel G, Hess WM, Ezra S, Pacheco G, Ezra D (2007) Biologically active endophytic streptomycetes from Nothofagus spp. and other plants in Patagonia. Microb Ecol 53:12–19CrossRefPubMedGoogle Scholar
  13. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100:14555–14561Google Scholar
  14. Chater KF, Losick R (1997) Mycelial life style of Streptomyces coelicolor A3(2) and its relatives. In: Shapiro JA, Dworkin M (eds) Bacteria as multicellular organisms. Oxford University Press, New York, pp 149–182Google Scholar
  15. Cho KM et al (2007) Endophytic bacterial communities in ginseng and their antifungal activity against pathogens. Microb Ecol 54:341–351CrossRefPubMedGoogle Scholar
  16. Coombs JT, Franco CMM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608CrossRefPubMedPubMedCentralGoogle Scholar
  17. de Bary A (1866) Morphologie, Phisiologie der pilze, flechten und myxomyceten. Holmeister’s Handbook of Physiological Botany, LeipzigCrossRefGoogle Scholar
  18. Dalponte JC, Lima ES (1999) Disponibilidade de frutos e a dieta de Lycalopex vetulus (carnívora) em um cerrado do Mato Grosso, Brasil. Rev Bras Bot 22:325–332CrossRefGoogle Scholar
  19. Debbab A, Aly AH, Proksch P (2011) Bioactive secondary metabolites from endophytes and associated marine derived fungi. Fungal Divers 49:1–12CrossRefGoogle Scholar
  20. Devi P, Rodrigues C, Naik CG, D'Souza L (2012) Isolation and characterization of antibacterial compound from a mangrove-endophytic fungus Penicillium chrysogenum MTCC 5108. Indian J Microbiol 52:617–623CrossRefPubMedPubMedCentralGoogle Scholar
  21. Elias SRM, Assis RM, Stacciarini-Seraphin E, Rezende MH (2003) Leaf anatomy in young plants of Solanum lycocarpum A. St-Hill. (Solanaceae). Rev Bras Bot 26:3–8Google Scholar
  22. Favoretto, NB (2010) Produção de substâncias bioativas por microrganismos endofiticos isolados do cerrado de São Carlos, SP. MS Thesis, Universidade Federal de São CarlosGoogle Scholar
  23. Firakova S, Sturdikova M, Muckova M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia 62:251–257CrossRefGoogle Scholar
  24. González V, Tello ML (2011) The endophytic mucota associated with Vitis vinífera in central Spain. Fungal Divers 47:29–42CrossRefGoogle Scholar
  25. Guimarães DO, Borges WS, Kawano CY, Ribeiro PH, Goldman GH, Nomizo A, Thiemann OH, Oliva G, Lopes NP, Pupo MT (2008) Biological activities from extracts of endophytic fungi isolated from Viguiera arenaria and Tithonia diversifolia. FEMS Immunol Med Microbiol 52:134–144CrossRefPubMedGoogle Scholar
  26. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  27. Hazalin NA, Ramasamy K, Lim SM, Wahab IA, Cole AL, Abdul Majeed AB (2009) Cytotoxic and antibacterial activities of endophytic fungi isolated from plants at the National Park, Pahang, Malaysia. BMC Complement Altern Med 21:46CrossRefGoogle Scholar
  28. He Z et al (2007) Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic. Appl Environ Microbiol 73:168–178Google Scholar
  29. Hopwood D (2007) An introduction to the actinobacteria. Microbiol Today 1:60–62Google Scholar
  30. Jung HM, Kim SY, Moon HJ, Oh DK, Lee JK (2007) Optimization of culture conditions and scale-up to pilot and plant scales for vancomycin production by Amycolatopsis orientalis. Appl Microbiol Biotechnol 77:789–795Google Scholar
  31. Korn-Wendisch F, Kutzner HJ (1992) The family Streptomycetaceae. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York, pp 921–995Google Scholar
  32. Kunoh H (2002) Endophytic actinomycetes: attractive bio-control agent. J Gen Plant Pathol 68:249–252CrossRefGoogle Scholar
  33. Lacava PT, Azevedo JL (2013) Endophytic bacteria: a biotechnological potential in agrobiology system. In: Maheshwari DK, Sarah M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin/Heidelberg, pp 1–44CrossRefGoogle Scholar
  34. Lacava PT, de Souza CP (2016) Role of endophytic actinomycetes in crop protection: plant growth promotion and biological control. In: Subramaniam G, Arumugam S, Rajendran V (eds) Growth promoting actinobacteria, 1st edn. Springer, Singapore, pp 147–160CrossRefGoogle Scholar
  35. Lins DM, Rodolpho JMA, Romano LH, Zaia MG, Albuquerque S, Anibal FF, Sousa CP (2015) Endophytic Paenibacillus terrae can produce toxic effect in progastigotes forms of Leishmania infantum/chagasi nitric oxide sensitive. Proceeding of the 18th World Congress of the International Society on Toxinology, 103–104, OxfordGoogle Scholar
  36. Mahmoud TS, Marques MR, O Pessoa C et al (2011) In vitro cytotoxic activity of Brazilian Middle West plant extracts. Braz J Pharmacogn 21:456–464CrossRefGoogle Scholar
  37. Mendonça RC, Felfili JM, Walter BMT, Silva Júnior MC, Rezende AV, Filgueiras TS, Nogueira PE (1998) Flora vascular do cerrado. In: Sano SM, Almeida SP (eds) Cerrado: ambiente e flora. Embrapa- CPAC, Planaltina, pp 287–556Google Scholar
  38. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858Google Scholar
  39. Oliveira Junior EN (2002) Alterações pós-colheita da fruta-do-lobo (Solanum lycocarpum St-Hill) durante o amadurecimento. MS Thesis, Universidade Federal de LavrasGoogle Scholar
  40. Oliveira JHHL et al (2007) Isolamento da cefamicina C e de novos metabólitos oriundos de caldos de Streptomyces clavuligerus e de novas linhagens de Streptomyces. 1° Seminário do Projeto Temático (Proc. 05/55079-4). Anais de Resumos Estendidos, São Carlos. p 25Google Scholar
  41. Oliveira MF, da Silva MG, Van Der Sand ST (2010) Anti-phytopathogen potential of endophytic actinobacteria isolated from tomato plants (Lycopersicon esculentum) in southern Brazil, and characterization of Streptomyces sp. R18(6), a potential biocontrol agent. Res Microbiol 161:565–572Google Scholar
  42. Owen NL, Hundley N (2004) Endophytes the chemical synthesizers inside plants. Sci Prog 87:79–99CrossRefPubMedGoogle Scholar
  43. Pavan FR, Sato DN, Higuchi CT, Santos ACB, Vilegas W, Leite CQF (2009) In vitro anti-Mycobacterium tuberculosis activity of some Brazilian “Cerrado” plants. Rev Bras Farmacogn 19:204–206CrossRefGoogle Scholar
  44. Petrini O, Sieber TN, Toti L, Viret O (1992) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1:185–196CrossRefPubMedGoogle Scholar
  45. Piza ACMT, Hokka CO, Sousa CP (2015) Endophytic actinomycetes from Miconia albicans (Sw.) triana (Melastomataceae) and evaluation of its antimicrobial activity. J Sci Res Rep 4:281–291Google Scholar
  46. Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Marostica MR Jr (2014) Fungal growth promoter endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79CrossRefGoogle Scholar
  47. Rangel TFLVB et al (2007) Human development and biodiversity conservation in Brazilian Cerrado. Appl Geogr 27:12–24CrossRefGoogle Scholar
  48. Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian cerrado vegetation and threats to its biodiversity. Ann Bot 80:223–230CrossRefGoogle Scholar
  49. Ratti RP, Serrano NFG, Hokka CO, Sousa CP (2008) Antagonistic properties of some microorganisms isolated from Brazilian tropical savannah plants against Staphylococcus coagulase-positive strain. J Venom Anim Toxins Incl Trop Dis 14:294–302Google Scholar
  50. Rivera-Orduña FN, Suarez-Sanchez RA, Flores-Bustamante ZR, Gracida-Rodriguez JN, Flores-Cotera LB (2011) Diversity of endophytic fungi of Taxus globosa (Mexican yew). Fungal Divers 47:65–74CrossRefGoogle Scholar
  51. Romano LH (2015) Bioprospecção de microrganismos endofíticos isolados de Tabebuia spp. e Hymenaea courbaril e identificação da produção de metabólitos de interesse biotecnológico. MS Thesis, Universidade Federal de São CarlosGoogle Scholar
  52. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280CrossRefPubMedGoogle Scholar
  53. Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216Google Scholar
  54. Schulz B, Boyle C (2006) Microbial root endophytes. In: Sieber TN (ed) What are endophytes? Springer, Berlin, pp 1–13Google Scholar
  55. Schulz B, Boyle CH, Draeger S, Rommert AK, Krohn K (2002) Review: endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  56. Selvin J, Shanmughapriya S, Gandhimathi R, SeghalKiran G, RajeethaRavji T, Natarajaseenivasan K, Hema TA (2009) Optimization and production of novel antimicrobial agents from sponge associated marine actinomycetes Norcadiopsis dassonvillei MAD08. Appl Microbiol Biotechnol 83:435–445CrossRefPubMedGoogle Scholar
  57. Serrano NFG, Mussato SID, Rodrigues LRM, Teixeira JAC, Hokka CO, Sousa CP (2010) Effects of glucose and inoculum concentrations on production of bioactive molecules by Paenibacillus polymyxa RNC-D: a statistical experimental design. J Biotechnol 150:524–524Google Scholar
  58. Serrano NFG, Rodrigues LRM, Hokka CO, Sousa CP, Teixeira JAC, Mussato SID (2012) Optimal glucose and inoculum concentrations for production of bioactive molecules by Paenibacillus polymyxa RNC-D. Chem Pap 66:1111–1117Google Scholar
  59. Sousa CP, Cruz-Hernández A, Baptista-Neto A, Teodoro JC, Cerri M, Ortiz SCA, Araujo MLGC, Badino AC, Hokka CO (2009) Challenges attending upon studies on clavulanic acid production. In: Mendez-Vilas A (ed) Current research topics in applied microbiology and microbial biotechnology. World Scientific Publishing Co., Singapore, pp 739–743CrossRefGoogle Scholar
  60. Strobel GA (2003) Endophytes as sources of bioactive compounds. Microbes Infect 5:535–544CrossRefPubMedGoogle Scholar
  61. Strobel GA et al (1999) Cryptocadin, a potent antimycotic from the endophytic fungus Cryptosporiopsis cf. quercina. Microbiology 17:417–423Google Scholar
  62. Strobel GA, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268CrossRefPubMedGoogle Scholar
  63. Supaphon P, Phongpaichit S, Rukachaisirikul V, Sakayaroj J (2013) Antimicrobial potential of endophytic fungi derived from three seagrass species: Cymodocea serrulata, Halophila ovalis and Thalassia hemprichii. PLoS One 16:e72520CrossRefGoogle Scholar
  64. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19CrossRefGoogle Scholar
  65. Szabó MP, Olegário MM, Santos AL (2007) Tick fauna from two locations in the Brazilian savannah. Exp Appl Acarol 43:73–84Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Cristina Paiva de Sousa
    • 1
  • Nadja Fernanda Gonzaga Serrano
    • 1
  • Paulo Teixeira Lacava
    • 1
  1. 1.Laboratory of Microbiology and Biomolecules - LaMiB, Department of Morphology and PathologyCenter for Biological and Health Sciences, Federal University of São CarlosSão CarlosBrazil

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