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Biologically Active Compounds from Bacterial Endophytes

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Endophytes and Secondary Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

Abstract

The phytomicrobiome plays a key role in incrementing the fitness of the host. The interactions between plants and their microbes yield a vast and diverse assortment of secondary metabolites. The myriad of genes within bacterial cells thriving inside plant tissues (i.e., endophytes) contributes to the production and conversion of small molecules into bioactive compounds, and the genome mining can be a powerful tool to extract this knowledge from large amounts of data sets. In this chapter, annotated biosynthetic gene clusters (n = 4614 unique within 60,632 genes) from genomes of endophytes assigned to Actinobacteria (n = 26), Bacteroidetes (n = 6), Firmicutes (n = 15), and Proteobacteria (n = 99) were analyzed and predicted to be involved in the biosynthesis of 4766 types of secondary metabolites classified within 22 families. The vast majority of secondary metabolites was predicted as putative (n = 3684), followed by those involved in the biosynthesis of nonribosomal peptide synthetase (n = 293), polyketide synthases (n = 268), and terpene (n = 120) compounds. This reveals that the community of endophytes conceals a great source of potential proteins with novel enzymatic activities and novel families of secondary metabolites.

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References

  1. Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed Central  PubMed  Google Scholar 

  2. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  3. Abreu-Tarazi MF, Navarrete AA, Andreote FD, Almeida CV, Tsai SM, Almeida M (2010) Endophytic bacteria in long-term in vitro cultivated ‘axenic’ pineapple microplants revealed by PCR–DGGE. World J Microbiol Biotechnol 26:555–560

    Article  Google Scholar 

  4. Dias ACF, Costa FEC, Andreote FD et al (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195

    Article  CAS  Google Scholar 

  5. de Almeida CV, Andreote FD, Yara R, Tanaka FAO, Azevedo JL, de Almeida M (2009) Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J Microbiol Biotechnol 25:1757–1764

    Article  Google Scholar 

  6. Thomas P, Sekhar AC (2014) Live cell imaging reveals extensive intracellular cytoplasmic colonization of banana by normally non-cultivable endophytic bacteria. AoB Plants 6. https://doi.org/10.1093/aobpla/plu002

  7. Maheshwari DK (2012) Bacteria in agrobiology: stress management. Springer, Berlin/Heidelberg

    Google Scholar 

  8. Maheshwari DK (2010) Plant growth and health promoting bacteria. Springer, Berlin/Heidelberg

    Google Scholar 

  9. Chamam A, Sanguin H, Bellvert F et al (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the AzospirillumOryza sativa association. Phytochemistry 87:65–77

    Article  CAS  PubMed  Google Scholar 

  10. Li J, Zhao GZ, Varma A et al (2012) An endophytic Pseudonocardia species induces the production of artemisinin in Artemisia annua. PLoS One 7:e51410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Fernandez O, Theocharis A, Bordiec S et al (2012) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant-Microbe Interact 25:496–504

    Article  CAS  PubMed  Google Scholar 

  12. Sessitsch A, Hardoim P, Döring J et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36

    Article  CAS  PubMed  Google Scholar 

  13. Faoro H, Menegazzo RR, Battistoni F et al (2016) The oil-contaminated soil diazotroph Azoarcus olearius DQS-4T is genetically and phenotypically similar to the model grass endophyte Azoarcus sp. BH72. Environ Microbiol Rep 9:223–238

    Article  Google Scholar 

  14. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    Article  CAS  PubMed  Google Scholar 

  15. Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004

    Article  CAS  Google Scholar 

  16. Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798

    Article  CAS  PubMed  Google Scholar 

  17. Yu TW, Bai L, Clade D et al (2002) The biosynthetic gene cluster of the maytansinoid antitumor agent ansamitocin from Actinosynnema pretiosum. Proc Natl Acad Sci 99:7968–7973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Hadjithomas M, Chen IMA, Chu K et al (2017) IMG-ABC: new features for bacterial secondary metabolism analysis and targeted biosynthetic gene cluster discovery in thousands of microbial genomes. Nucleic Acids Res 45:D560–D565

    Article  CAS  PubMed  Google Scholar 

  19. Varghese NJ, Mukherjee S, Ivanova N et al (2015) Microbial species delineation using whole genome sequences. Nucleic Acids Res 43:6761–6771

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Oksanen J (2008) Multivariate analysis of ecological communities in R: vegan tutorial. http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf. Accessed 01 May 2018

  21. R core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria. http://www.R-project.org/. Accessed 01 May 2018

  22. Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol 4. https://doi.org/10.3389/fmicb.2013.00065

  23. Sandhu SS, Kumar S, Aharwal RP, Nozawa M (2017) Endophytic fungi: eco-friendly future resource for novel bioactive compounds. In: Maheshwari D (ed) Endophytes: biology and biotechnology. Sustainable development and biodiversity. Springer, Cham

    Google Scholar 

  24. Firáková S, Šturdíková M, Múčková M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia (Bratisl) 62:251–257

    Article  Google Scholar 

  25. Qin S, Xing K, Jiang JH, Xu LH, Li WJ (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol 89:457–473

    Article  CAS  PubMed  Google Scholar 

  26. Subramaniam G, Arumugam S, Rajendran V (2016) Plant growth promoting actinobacteria: a new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, Berlin/Heidelberg

    Book  Google Scholar 

  27. Dinesh R, Srinivasan V, Anandaraj STEM, Srambikkal H (2017) Endophytic actinobacteria: diversity, secondary metabolism and mechanisms to unsilence biosynthetic gene clusters. Crit Rev Microbiol 43:546–566

    Article  CAS  PubMed  Google Scholar 

  28. Medema MH, Fischbach MA (2015) Computational approaches to natural product discovery. Nat Chem Biol 11(9):639–648

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Jensen PR (2016) Natural products and the gene cluster revolution. Trends Microbiol 24:968–977

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Tisa LS, Beauchemin N, Gtari M, Sen A, Wall LG (2013) What stories can the Frankia genomes start to tell us? J Biosci 38:719–726

    Article  PubMed  Google Scholar 

  31. Koehorst JJ, van Dam JCJ, van Heck RGA et al (2016) Comparison of 432 Pseudomonas strains through integration of genomic, functional, metabolic and expression data. Sci Rep 6:38699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Kim Y, Koh I, Lim MY, Chung WH, Rho M (2017) Pan-genome analysis of Bacillus for microbiome profiling. Sci Rep 7:10984

    Article  PubMed Central  PubMed  Google Scholar 

  33. Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz M et al (2017) Frankia inefficaxsp. nov., an actinobacterial endophyte inducing ineffective, non nitrogen-fixing, root nodules on its actinorhizal host plants. Antonie Van Leeuwenhoek 110:313–320

    Article  CAS  PubMed  Google Scholar 

  34. Ghodhbane-Gtari F, Beauchemin N, Bruce D et al (2013) Draft genome sequence of Frankia sp. strain CN3, an atypical, noninfective (nod–) ineffective (fix–) isolate from Coriaria nepalensis. Genome Announc 1:e00085–e00013

    Article  PubMed Central  Google Scholar 

  35. Ettinger CL, Shehata HR, Johnston-Monje D, Raizada MN, Eisen JA (2015) Draft genome sequence of Burkholderia gladioli strain UCD-UG_CHAPALOTE (phylum Proteobacteria). Genome Announc 3:e01462–e01414

    PubMed  PubMed Central  Google Scholar 

  36. Kaku H, Nishizawa Y, Ishii-Minami N et al (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci 103:11086–11091

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Lerouge P, Roche P, Faucher C et al (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784

    Article  CAS  PubMed  Google Scholar 

  38. Hocher V, Alloisio N, Auguy F et al (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 156:700–711

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Sathya A, Vijayabharathi R, Gopalakrishnan S (2017) Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:102

    Article  PubMed Central  PubMed  Google Scholar 

  40. Ventura M, Canchaya C, Tauch A et al (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71:495–548

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Doroghazi JR, Albright JC, Goering AW et al (2014) A roadmap for natural product discovery based on large-scale genomics and metabolomics. Nat Chem Biol 10:963–968

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Normand P, Lapierre P, Tisa LS et al (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15

    Article  PubMed Central  PubMed  Google Scholar 

  43. Qin S, Feng WW, Xing K et al (2015) Complete genome sequence of Kibdelosporangium phytohabitans KLBMP 1111T, a plant growth promoting endophytic actinomycete isolated from oil-seed plant Jatropha curcas L. J Biotechnol 216:129–130

    Article  CAS  PubMed  Google Scholar 

  44. Gross H, Loper JE (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

    Article  CAS  PubMed  Google Scholar 

  45. Köksal M, Jin Y, Coates RM, Croteau R, Christianson DW (2011) Taxadiene synthase structure and evolution of modular architecture in terpene biosynthesis. Nature 469:116–120

    Article  PubMed  Google Scholar 

  46. Gürtler H, Pedersen R, Anthoni U et al (1994) Albaflavenone, a sesquiterpene ketone with a zizaene skeleton produced by a streptomycete with a new rope morphology. J Antibiot 47:434–439

    Article  Google Scholar 

  47. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der Donk WA (2010) Discovery of unique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLoS Biol 8:e1000339

    Article  PubMed Central  PubMed  Google Scholar 

  48. Li P, Sher D, Kelly L et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  49. Zakeri B, Wright GD (2008) Chemical biology of tetracycline antibiotics. Biochem Cell Biol 86:124–136

    Article  CAS  PubMed  Google Scholar 

  50. Yang W, Moore IF, Koteva KP, Bareich DC, Hughes DW, Wright GD (2004) TetX is a flavin-dependent monooxygenase conferring resistance to tetracycline antibiotics. J Biol Chem 279:52346–52352

    Article  CAS  PubMed  Google Scholar 

  51. Polkade AV, Mantri SS, Patwekar UJ, Jangid K (2016) Quorum sensing: an under-explored phenomenon in the phylum Actinobacteria. Front Microbiol 7(131):2016

    Google Scholar 

  52. Sansinenea E, Ortiz A (2011) Secondary metabolites of soil Bacillus spp. Biotechnol Lett 33:1523–1538

    Article  CAS  PubMed  Google Scholar 

  53. Romero D, de Vicente A, Rakotoaly RH et al (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant-Microbe Interact 20:430–440

    Article  CAS  PubMed  Google Scholar 

  54. SantAnna BMM, Marbach PPA, Rojas-Herrera M, Souza JTD, Roque MRA, Queiroz ATL (2015) High-quality draft genome sequence of Bacillus amyloliquefaciens strain 629, an endophyte from Theobroma cacao. Genome Announc 3:e01325-15

    Article  PubMed Central  PubMed  Google Scholar 

  55. Piel J (2010) Biosynthesis of polyketides by trans-AT polyketide synthases. Nat Prod Rep 27:996–1047

    Article  CAS  PubMed  Google Scholar 

  56. Riley MA, Wertz JE (2002) Bacteriocin diversity: ecological and evolutionary perspectives. Biochimie 84:357–364

    Article  CAS  PubMed  Google Scholar 

  57. Scholz R, Vater J, Budiharjo A et al (2014) Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol 196:1842–1852

    Article  PubMed Central  PubMed  Google Scholar 

  58. Cao Y, Halane MK, Gassmann W, Stacey G (2017) The role of plant innate immunity in the legume-rhizobium symbiosis. Annu Rev Plant Biol 68:535–561

    Article  CAS  PubMed  Google Scholar 

  59. Fuqua C, Greenberg EP (2002) Signalling: listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695

    Article  CAS  PubMed  Google Scholar 

  60. Daniels R, de Vos DE, Desair J et al (2002) The cin quorum sensing locus of Rhizobium etli cnpaf512 affects growth and symbiotic nitrogen fixation. J Biol Chem 277:462–468

    Article  CAS  PubMed  Google Scholar 

  61. Moulin L, James EK, Klonowska A, Faria SM, Simon MF (2015) Phylogeny, diversity, geographical distribution, and host range of legume-nodulating Betaproteobacteria: what is the role of plant taxonomy? In: de Bruijn FJ (ed) Biological nitrogen fixation. Wiley-Blackwell, Hoboken

    Google Scholar 

  62. Ho YN, Chiang HM, Chao CP et al (2015) In plantabiocontrol of soilborne Fusarium wilt of banana through a plant endophytic bacterium, Burkholderia cenocepacia 869T2. Plant Soil 387:295–306

    Article  CAS  Google Scholar 

  63. Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016) Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J Appl Microbiol 120:756–769

    Article  CAS  PubMed  Google Scholar 

  64. Köberl M, Dita M, Martinuz A, Staver C, Berg G (2017) Members of Gammaproteobacteria as indicator species of healthy banana plants on Fusarium wilt-infested fields in Central America. Sci Rep 7:45318

    Article  PubMed Central  PubMed  Google Scholar 

  65. Jun SR, Wassenaar TM, Nookaew I et al (2015) Comparative genome analysis of Pseudomonas genomes including Populus-associated isolates. Appl Environ Microbiol 82:375. https://doi.org/10.1128/AEM.02612-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Masschelein J, Mattheus W, Gao LJ et al (2013) A PKS/NRPS/FAS hybrid gene cluster from Serratia plymuthica RVH1 encoding the biosynthesis of three broad spectrum, zeamine-related antibiotics. PLoS One 8:e54143

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Parret AHA, Temmerman K, Mot RD (2005) Novel lectin-like bacteriocins of biocontrol strain Pseudomonas fluorescens Pf-5. Appl Environ Microbiol 71:5197–5207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Förster-Fromme K, Höschle B, Mack C, Bott M, Armbruster W, Jendrossek D (2006) Identification of genes and proteins necessary for catabolism of acyclic terpenes and leucine/isovalerate in Pseudomonas aeruginosa. Appl Environ Microbiol 72:4819–4828

    Article  PubMed Central  PubMed  Google Scholar 

  69. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  PubMed  Google Scholar 

  70. Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907

    Article  CAS  PubMed  Google Scholar 

  71. 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 100:14555–14561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Hardoim, P.R. (2018). Biologically Active Compounds from Bacterial Endophytes. In: Jha, S. (eds) Endophytes and Secondary Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-76900-4_1-1

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  • DOI: https://doi.org/10.1007/978-3-319-76900-4_1-1

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  • Print ISBN: 978-3-319-76900-4

  • Online ISBN: 978-3-319-76900-4

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