Abstract
Microbial natural products, in particular, the ones produced by the members of the order Actinomycetales, will continue to represent an important route to the discovery of novel classes of bioactive compounds. As a result, the search for and discovery of lesser-known and/or novel actinomycetes is of significant interest to the industry due to a growing need for the development of new and potent therapeutic agents, mainly against drug resistant bacteria. Current advancements in genomics and metagenomics are adding strength to the target-directed search for detection and isolation of bioactive actinomycetes. New discoveries, however, will only stem from a sound understanding and interpretation of knowledge derived from conventional studies conducted since the discovery of streptomycin, on the ecology, taxonomy, physiology and metabolism of actinomycetes, and from a combination of this knowledge with currently available and continuously advancing molecular tools. Such a powerful information platform will then inevitably reveal the whereabouts, taxonomical and chemical identities of previously undetected bioactive actinomycetes including novel species of streptomycetes as potential producers of novel drug candidates.
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References
Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594
Asolkar R, Kirkland TN, Jensen PR, Fenical W (2010) Arenimycin, an antibiotic effective against rifampin- and methicillin-resistant Staphylococcus aureus from the marine actinomycete Salinispora arenicola. J Antibiot (Tokyo) 63(1):37–39
Baltz RH (2005) Antibiotic discovery from actinomycetes: will a renaissance follow the decline and fall? SIM News 55(5):186–196
Baltz RH (2006a) Marcel Faber Roundtable: is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration. J Ind Microbiol Biotech 33:507–513
Baltz RH (2006b) Combinatorial biosynthesis of novel antibiotics and other secondary metabolites in actinomycetes. SIM News 56:148–160
Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8:557–563
Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58(1):1–26
Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. Chem Bio Chem 3:619–627
Bull AT (ed) (2004) Microbial diversity and bioprospecting. ASM Press, Washington
Bull AT (2007) Alice in Actinoland, and looking glass tales. SIM News 57(6):225–234
Bull AT (2010) Actinobacteria of the extremobiosphere. In: Horikoshi K, Antranikian G, Bull AT, Robb F, Stelter K (eds) Extremophiles handbook. Springer-Verlag GmbH, Berlin
Bull AT, Stach JEM (2007) Marine actinobacteria: new opportunities for natural product search and discovery. Trends Microbiol 15(11):491–499
Bull AT, Ward AC, Goodfellow M (2000) Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Biol R 64:573–606
Butler MS (2004) The role of natural product chemistry in drug discovery. J Nat Prod 67:2141–2153
Butler MS, Buss AD (2006) Natural products—the future scaffolds for novel antibiotics? Biochem Pharmacol 71:919–929
Capon RJ (2010) Marine natural products chemistry: past, present, and future. Aust J Chem 63:851–854
Challis GL (2008) Genome mining for novel natural product discovery. J Med Chem 51:2618–2628
Challis GL, Ravel J (2000) Coelichelin, a new peptide siderophore encoded by the Streptomyces coelicolor genome: structure prediction from the sequence of its non-ribosomal peptide synthetase. FEMS Microbiol Lett 187(2):111–114
Chater KF (2006) Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Phil Trans R Soc B 361:761–768
Chopra I, Hesse L, O’Neill AJ (2002) Exploiting current understanding of antibiotic action for discovery of new drugs. J Appl Microbiol Symp Suppl 92:4S–15S
Davies J (2006) Are antibiotics naturally antibiotics? J Ind Microbiol Biotechnol 33:496–499
DeLong EF (2005) Microbial community genomics in the ocean. Nat Rev Microbiol 3:459–469
Donadio S (2010) Antibiotic discovery in the twenty-first century: current trends and future perspectives. J Antibiot 63:423–430
Dunlap WC, Jaspars M, Hranueli D, Battershill CN, Peric-Concha N, Zucko J, Wright SH, Long PF (2006) New methods for medicinal chemistry—universal gene cloning and expression systems for production of marine bioactive metabolites. Curr Med Chem 13:697–710
Ellen EE, Banfield JF (2005) Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3:489–498
Ferrari BC, Winsley T, Gillings M, Binnerup S (2008) Cultivating previously uncultured soil bacteria using a soil substrate membrane system. Nat Protoc 3:1261–1269
Fiedler H-P, Bruntner C, Riedlinger J, Bull AT, Knutsen G, Goodfellow M, Jones AL, Maldonado L, Pathom-aree W, Beil W, Schneider K, Keller S, Süssmuth RD (2008) Proximicin A, B and C, novel aminofuran antibiotic and anticancer compounds isolated from marine strains of the actinomycete Verrucosispora. J Antibiot 61:158–163
Firn RD, Jones CG (2000) The evolution of secondary metabolism—a unifying model. Mol Microbiol 37(5):989–994
Fujimori DG, Hrvatin S, Neumann CS, Strieker M, Mohamed A, Marahiel MA, Christopher T, Walsh CT (2007) Cloning and characterization of the biosynthetic gene cluster for Kutznerides. Proc Natl Acad Sci 104(42):16498–16503
Gavrish E, Bollmann A, Epstein S, Lewis K (2008) A trap for in situ cultivation of filamentous actinobacteria. J Microbiol Methods 72(3):257–262
Genilloud O, González I, Salazar O, Martín J, Tormo JR, Vicente F (2011) Current approaches to exploit actinomycetes as a source of novel natural products. J Ind Microbiol Biotechnol 38:375–389
Glöckner FO, Joint I (2010) Marine microbial genomics in Europe: current status and perspectives. Microb Biotechnol 3:523–530
Goodfellow M (2010) Selective isolation of Actinobacteria. In: Section 1: Bull AT, Davies JE (section eds) Isolation and screening of secondary metabolites and enzymes. Manual of industrial microbiology and biotechnology (Baltz RH, Davies J, Demain AL, eds), Washington: ASM Press, pp.13-27
Goodfellow M, Fiedler H-P (2010) A guide to successful bioprospecting: informed by actinobacterial systematics. Antonie Van Leeuwenhoek 98:119–142
Goodfellow M, Williams E (1986) New strategies for the selective isolation of industrially important bacteria. Biotechnol Genet Eng Rev 4:213–262
Handelsman J. (2004) Soils—the metagenomics approach. In: Bull AT (ed) Microbial diversity and bioprospecting, ASM Press, pp.109-119
Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:245–249
Hayakawa M (2008) Studies on the isolation and distribution of rare actinomycetes in soil. Actinomycetologica 22:12–19
Heidelberg KB, Gilbert JA, Joint I (2010) Marine genomics: at the interface of marine microbial ecology and biodiscovery. Microb Biotech 3(5):531–543
Hopwood DA (2006) Soil to genomics: the Streptomyces chromosome. Annu Rev Genet 40:1–23
Hornung A, Bertazzo M, Dziarnowski A, Schneider K, Welzel K, Wohlert S-E, Holzenkaempfer M, Nicholson GJ, Bechthold A, Suessmuth RD, Vente A, Pelzer SA (2007) Genomic screening approach to the structure-guided identification of drug candidates from natural sources. Chem Bio Chem 8:757–766
Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Ōmura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotech 21:526–531
Janso JE, Carter GT (2010) Biosynthetic potential of phylogenetically unique endophytic actinomycetes from tropical plants. Appl Environ Microbiol 76(13):4377–4386
Jensen PR (2010) Linking species concepts to natural product discovery in the post-genomic era. J Ind Microbiol Biotechnol 37:219–224
Jensen PR, Lauro FM (2008) An assessment of actinobacterial diversity in the marine environment. Antonie Van Leeuwenhoek 94:51–62
Jensen PR, Mafnas C (2006) Biogeography of the marine actinomycete Salinispora. Environ Microbiol 8:1881–1888
Jensen PR, Gontang E, Mafnas C, Mincer TJ, Fenical W (2005a) Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 7:1039–1048
Jensen PR, Mincer TJ, Williams PG, Fenical W (2005b) Marine actinomycete diversity and natural product discovery. Antonie Van Leeuwenhoek 87:43–48
Jensen PR, Williams PG, Oh CD, Zeigker L, Fenical W (2007) Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl Environ Microbiol 73:1146–1152
Joint I, Mühling M, Querellou J (2010) Culturing marine bacteria—an essential prerequisite for biodiscovery. Marine Biotechnology (In: Giuliano L, Barbier M, Briand F (eds) Special Issue: Marine Omics), 3(5):564-575
Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127–1129
Kellenberger E, Hofmann A, Quinn RJ (2011) Similar interactions of natural products with biosynthetic enzymes and therapeutic targets could explain why nature produces such a large proportion of existing drugs. Nat Prod Rep 28:1483–1492
Kennedy J, Marchesi JR, Dobson ADW (2007) Metagenomic approaches to exploit the biotechnological potential of the microbial consortia of marine sponges. Appl Microbiol Biotechnol 75:11–20
Kim TK, Hewavitharana AK, Shaw PN, Fuerst JA (2006) Discovery of a new source of rifamycin antibiotics in marine sponge actinobacteria by phylogenetic prediction. Appl Environ Microbiol 72:2118–2125
Konstantinidis K, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264
Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509
Kurtböke DI (ed) (2003) Selective isolation of rare actinomycetes. Queensland Complete Printing Services, Nambour, Queensland, Australia
Kurtböke DI (2009) Use of phage-battery to isolate industrially important rare actinomycetes. In: Adams HT (ed) Contemporary trends in bacteriophage research. NOVA Science, New York, pp 79–117
Kurtböke DI (2010a) Biodiscovery from microbial resources: Actinomycetes leading the way. Microbiol Aust 31(2):53–57
Kurtböke DI (2010b) Bacteriophages as tools in drug discovery programs. Microbiol Aust 31(2):67–70
Kurtböke DI (2011) Exploitation of phage battery in the search for bioactive actinomycetes. Appl Microbiol Biotechnol (2011) 89:931-937
Kurtböke DI, French JRJ (2007) Use of phage battery to investigate the actinofloral layers of termite-gut microflora. J Appl Microbiol 103(3):722–734
Lang G, Mayhudin NA, Maya I, Mitova MI, Sun L, Sun L, van der Sar S, Blunt JW, Cole AJL, Ellis G, Laatsch H, Munro MHG (2008) Evolving trends in the dereplication of natural product extracts: new methodology for rapid, small-scale investigation of natural product extracts. J Nat Prod 71:1595–1599
Martin R, Sterner O, Alvarez MA, deClercq E, Bailey JE, Minas W (2001) Collinone, a new recombinant angular polyketide antibiotic made by an engineered Streptomyces strain. J Antibiot (Tokyo) 54(3):239–249
McLeod MP, Warren H, Hsiao WW, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanih M, Hara H, Petrescu A, Morin RD, Yang G, Scott JM, Schein JE, Shin H, Smalius D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus RHA 1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci 103:15582–15587
Metsä-Ketelä M, Halo L, Munukka E, Hakala J, Mäntsälä P, Ylihonko K (2002) Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various Streptomyces species. Appl Environ Microbiol 68(9):4472–4479
Mills SD (2003) The role of genomics in antimicrobial discovery. J Antimicrob Chemoth 51:749–752
Nett M, Ikeda H, Moore B (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26(11):1362–1384
Olano C, Méndez C, Salas JA (2011) Molecular insights on the biosynthesis of antitumour compounds by actinomycetes. Microb Biotech 4(2):144–164
Oliynyk M, Samborskyy M, Lester JB, Mironenko T, Scott N, Dickens S, Haydock SF, Leadley PJ (2007) Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL 23338. Nat Biotechnol 25:447–453
Ōmura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shibai T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci 98:12215–12220
Palmu K, Ishida K, Mantsala P, Hertweck C, Metsa-Ketela M (2007) Artificial reconstruction of two cryptic angucycline antibiotic biosynthetic pathways. Chem Bio Chem 8:1577–1584
Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discover 6:29–40
Penn K, Jenkins C, Nett M, Udwary DW, Gontang EA, McGlinchey RP, Foster B, Lapidus A, Podell S, Allen EE (2009) Genomic islands link secondary metabolism to functional adaptation in marine actinomycetes. ISMEJ 3:1193–1203
Qin S, Xing K, Jiang J-H, Xu L-H, Li W-J (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol 89:457–473
Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: Genomic analysis of microbial communities. Annu Rev Genet 38:525–552
Sánchez C, Butovich IA, Braña AF, Rohr J, Méndez C, Salas JA (2002) The biosynthetic gene cluster for the antitumor rebeccamycin: characterization and generation of indolocarbazole derivatives. Chem Biol 9:519–531
Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6:229–232
Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492
Stach JEM, Bull AT (2005) Estimating and comparing the diversity of marine actinobacteria. Antonie Van Leeuwenhoek 87:3–9
Stach JE, Maldonado LA, Ward AC, Goodfellow M, Bull AT (2003) New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5:828–841
Stackebrandt E (2011) Molecular taxonomic parameters. Microbiol Aust 32(2):59–61
Tiwari K, Gupta RK (2011) Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 2011:1–25
Turner WB (1973) Secondary metabolism with special reference to Actinomycetales. Soc Appl Microbiol Symp Ser 2:209–217
Udwary DW, Ziegler L, Asolbar HN, Singan V, Lapidus A, Fenical W, Jensen PR, Moore BS (2007) Genome sequencing reveals complete secondary metabolome in the marine actinomycete Salinispora tropica. Proc Natl Acad Sci USA 104:10376–10381
Udwary DW, Gontang EA, Jones AC, Jones CS, Schultz AW, Winter JM, Yang JY, Beauchemin N, Capson TL, Clark BR, Esquenazi E, Eustáquio AS, Freel K, Gerwick L, Gerwick WH, Gonzalez D, Liu WT, Malloy KL, Maloney KN, Nett M, Nunnery JK, Penn K, Prieto-Davo A, Simmons TL, Weitz S, Wilson MC, Tisa LS, Dorrestein PC, Moore BS (2011) Significant natural product biosynthetic potential of actinorhizal symbionts of the genus Frankia, as revealed by comparative genomic and proteomic analyses. Appl Environ Microbiol 77(11):3617–3625
Vaishnav P, Demain AL (2010) Unexpected applications of secondary metabolites. Biotechnol Adv 29:223–229
Van Lanen SG, Shen B (2006) Microbial genomics for the improvement of natural product discovery. Curr Opin Microbiol 9:252–260
Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309:1–7
Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71(3):495–548
Vickers JC, Williams ST, Ross GW (1984) A taxonomic approach to selective isolation of streptomycetes from soil. In: Ortiz-Ortiz L, Bojalil LF, Yakoleff V (eds) Biological, biochemical and biomedical of actinomycetes. Academic Press, London, pp 553–561
Ward A, Bora N (2006) Diversity and biogeography of marine actinobacteria. Curr Opin Microbiol 9:279–286
Ward A, Goodfellow M (2004) Taxonomy as a roadmap for search and biodiscovery. Microbiol Aust 25:13–15
Watve MG, Tickoo R, Jog MM, Behole BD (2001) How many antibiotics are produced by the genus Streptomyces? Arch Microbiol 176:386–390
Wellington EMH, Berry A, Krsek M (2003) Resolving functional diversity in relation to microbial community structure in soil: exploiting genomics and stable isotope probing. Curr Opin Microbiol 6:295–301
Wilkinson B, Micklefield J (2007) Mining and engineering natural-product biosynthetic pathways. Nat Chem Biol 3(7):379–386
Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983a) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813
Williams ST, Goodfellow M, Wellington EMH, Vickers JC, Alderson G, Sneath PHA, Sackin MJ, Mortimer AM (1983b) A probability matrix for the identification of streptomycetes. J Gen Microbiol 129:1815–1830
Williams ST, Vickers JC, Goodfellow M (1984) New microbes from old habitats? In: Kelly DP, Carr NG (eds) The microbe 1984, II: prokaryotes and eukaryotes. Cambridge University Press, Cambridge, pp 219–256
Wink J (2011) How can actinomycete taxonomy and natural product research work together? The Sanofi–Aventis approach. Microbiol Aust 32(2):81–85
Xu J (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools, and recent advances. Mol Ecol 15:1713–1731
Zak JC, Willing MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26(9):1101–1108
Zhou J, Kang S, Schadt CW, Garten CT Jr (2008) Spatial scaling of functional gene diversity across various microbial taxa. PNAS 105(22):7768–7773
Acknowledgements
The author would like to thank Dr. Ken Wasmund for the construction of phylogenetic tree for the isolate USC-633.
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Kurtböke, D.İ. Biodiscovery from rare actinomycetes: an eco-taxonomical perspective. Appl Microbiol Biotechnol 93, 1843–1852 (2012). https://doi.org/10.1007/s00253-012-3898-2
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DOI: https://doi.org/10.1007/s00253-012-3898-2