Actinobacteria

Abstract

Actinobacteria are Gram‐stain‐positive microorganisms with high guanine plus cytosine content in their genome (>50%). They are quite abundant in soil and aquatic sediments where they participate in the decomposition of organic matter. These bacteria are responsible for the distinctive scent of freshly exposed, moist soil. Actinobacteria are morphologically diverse ranging from coccoid, fragmenting hyphal forms to those with a highly differentiated branched mycelium. Many of these bacteria also produce external spores resistant to UV (ultraviolet) light and dehydration. Most actinobacteria are saprophytic microorganisms but several genera are important human, animal and plant pathogens. They are major producers of medically important antibiotics, especially members of the genus Streptomyces, the most abundant group. On the basis of 16S rRNA (ribosomal ribonucleic acid) gene sequences, the phylum actinobacteria contains almost 300 genera but new taxa continue to be discovered.

Key Concepts

  • The phylum actinobacteria is one of the largest groups in the domain Bacteria.
  • Actinobacteria are Gram‐positive bacteria with a high guanine plus cytosine content in their genome.
  • Morphologically, actinobacteria are quite diverse ranging from cocci to complex filaments which form a mycelium and produce specialised reproductive structures called spores.
  • Actinobacteria are chemoorganotrophic and play an important role in the biodegradation and recycling of organic matter.
  • Actinobacteria are mainly aerobes with an oxidative metabolism, but several species are facultative anaerobes or even strict anaerobes.
  • Actinobacteria are widespread in soil but they are also present in marine and freshwater sediments, mangrove ecosystems and inside plant tissues.
  • Most actinobacteria are free‐living microorganisms, but several species are important plant and animal pathogens.
  • Actinobacteria are unsurpassed in their ability to produce many useful compounds with application in medicine, agriculture and industry.
  • Genomic sequence data has revealed that actinobacteria have the potential to produce far more secondary metabolites than previously thought.

Keywords: actinobacteria; classification; Streptomyces; secondary metabolites; phylogeny

Figure 1. Morphological diversity found in the phylum actinobacteria. (a) Nocardia sp.; (b) Streptomyces sp. producing a secondary metabolite (droplets); (c) Micromonospora sp.; (d and e) Streptomyces sp.; (f) Actinomadura sp.; (g) edge of a streptomycete colony producing an antibiotic and (h) Micromonospora sp. (b, e, g) Courtesy of Dr Ramón Santamaria.
Figure 2. Steps involved in the life cycle of a filamentous actinobacterium. Based on information in Kieser et al. (2000).
Figure 3. Classification of the phylum actinobacteria based on Bergey's Manual of Systematic Bacteriology.
close

References

Agarkova IV, Vidaver AK, Postnikova EN, et al. (2006) Genetic characterization and diversity of Rathayibacter toxicus. Phytopathology 96: 1270–1277.

Almeida B, Vaz‐Moreira I, Schumann P, et al. (2013) Patulibacter medicamentivorans sp. nov., isolated from activated sludge of a wastewater treatment plant. International Journal of Systematic and Evolutionary Microbiology 63: 2588–2593.

Anderson RC, Maja W, Rassmussen MA, et al. (2005) Toxicity and metabolism of the conjugates of 3‐nitropropanol and 3‐nitropropionic acid in forages poisonous to livestock. Journal of Agriculture and Food Chemistry 53: 2344–2350.

Barka EA, Vatsa O, Sanchez L, et al. (2015) Taxonomy, physiology and natural products of actinobacteria. Microbiology and Molecular Biology Reviews 80: 1–43.

Bentley SD, Chater KF, Cerdeño‐Tárraga AM, et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141–147.

Bienenstock J, Wiley RE, Neigh GS, et al. (2002) Probiotics in the management and prevention of atopy. Clinical Reviews in Allergy and Immunology 22: 275–285.

Busti E, Monciardini P, Cavaletti L, et al. (2006) Antibiotic‐producing ability by representatives of a newly discovered lineage of actinomycetes. Microbiology 152: 675–683.

Cavaletti L, Mociardini P, Schumann P, et al. (2006) Actinospica robiniae gen nov., sp. nov. and Actinospica acidiphila sp. nov.: proposal for Actinopispaceae fam. nov. and Catenulisporinae subord. nov. in the order Actinomycetales. International Journal of Systematic and Evolutionary Microbiology 56: 1747–1753.

Carro L, Pujic P, Trujillo ME, et al. (2013) Micromonospora is a normal inhabitant of actinorhizal nodules. Journal of Biosciences 38: 685–693.

Cohen ND (2014) Rhodococcus equi foal pneumonia. Veterinary Clinics of North America. Equine Practice 30: 609–622.

Cole ST, Brosch R, Parkhill J, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537–544.

Cole ST, Eiglmeier K, Parkhill J, et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007–1011.

Craig AM, Latham CJ, Blythe LL, et al. (1992) Metabolism of toxic pyrrolizidine alkaloids from tansy ragwort (Senecio jacobaea) in ovine ruminal fluid under anaerobic conditions. Applied and Environmental Microbiology 58: 2730–2736.

Fahal AH (2006) Mycetoma, Clinicopathological Monograph. Khartoum: Khartoum University Press.

Ferreira AC, Nobre MF, Moore E, et al. (1999) Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3: 235–238.

Gao B and Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiology and Molecular Biology Reviews 76: 66–112.

Gartemann KH, Kirchner O, Engemann J, et al. (2003) Clavibacter michiganensis subsp. michiganensis: first steps in the understanding of virulence of a Gram‐positive phytopathogenic bacterium. Journal of Biotechnology 106: 179–191.

Goodfellow M, Kämpfer P, Busse H‐J, et al. (eds) (2012) Bergey's Manual of Systematic Bacteriology, vol. 5, The Actinobacteria, 2nd edn, Part A. New York: Springer.

Ikeda H, Ishikawa J, Hanamoto A, et al. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nature Biotechnology 21: 526–531.

Jensen PR, Gontang E, Mafnas C, et al. (2005) Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environmental Microbiology 7: 1039–1048.

Kieser T, Bibb MJ, Buttner MJ, et al. (2000) Practical Streptomyces Genetics. Crowes, England: John Innes Foundation.

Kim MK, Lee TH, Im WT, et al. (2007) Solirubrobacter soli sp. nov., isolated from soil of a ginseng field. International Journal of Systematic and Evolutionary Microbiology 57: 1453–1455.

Kokare CR, Mahadik KR, Kadam SS, et al. (2004) Isolation, characterization and antimicrobial activity of marine halophilic Actinopolyspora species AH1 from the west coast of India. Current Science 86: 593–597.

Kurahashi M, Fukunaga Y, Sakiyama Y, et al. (2009) Iamia majanohamensis gen. nov., sp. nov., an actinobacterium isolated from sea cucumber Holothuria edulis, and proposal of Iamiaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology 59: 869–873.

Lazzarini A, Cavaletti L, Toppo G, et al. (2001) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 79: 399–405.

Leahy SC, Higgins DG, Fitzgerald GF, et al. (2005) Getting better with bifidobacteria. Journal of Applied Microbiology 98: 1303–1315.

Ludwig W, Euzéby J, Schumann P, et al. (2012) Road map of the phylum Actinobacteria. In: Goodfellow M, Kämpfer P, Busse H‐J, Trujillo ME, Suzuki K‐I, Ludwig W and Whitman WB (eds) Bergey's Manual of Systematic Bacteriology, vol. 5, pp. 1–28, 2nd edn, part A. New York: Springer.

Lykidis A, Mavromatis K, Ivanova N, et al. (2007) Genome sequence and analysis of the soil cellulolytic actinomycete Thermobifida fusca YX. Journal of Bacteriology 189: 2477–2486.

Martínková L, Uhnáková B, Pátek M, et al. (2009) Biodegradation potential of the genus Rhodococcus. Environment International 35: 162–177.

Matsumoto A, Kasai H, Matsuo Y, et al. (2013) Ilumatobacter nonamiense sp. nov. and Ilumatobacter coccineum sp. nov., isolated from seashore sand. International Journal of Systematic and Evolutionary Microbiology 63: 3404–3408.

Meklat A, Bouras N, Zitouni A, et al. (2013) Actinopolyspora mzabensis sp. nov., a halophilic actinomycete isolated from an Algerian Saharan soil. International Journal of Systematic and Evolutionary Microbiology 63: 3787–3792.

Modesto M, Biavati B and Mattarelli P (2006) Occurrence of the family bifidobacteriaceae in human dental caries and plaque. Caries Research 40: 271–276.

Monciardini P, Cavaletti L, Schumann P, et al. (2003) Conexibacter woesei gen. nov., sp. nov., a novel representative of a deep evolutionary line of descent within the class Actinobacteria. International Journal of Systematic and Evolutionary Microbiology 53: 569–576.

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 Research 17: 7–15.

Penn K and Jensen PR (2012) Comparative genomics reveals evidence of marine adaptation in Salinispora species. BMC Genomics 13: 86.

Phillips RW, Wiegel J, Berry CJ, et al. (2002) Kineococcus radiotolerans sp. nov., a radiation‐resistant, Gram‐positive bacterium. International Journal of Systematic and Evolutionary Microbiology 52: 933–938.

Sales CM, Grostern A, Parales JV, et al. (2013) Oxidation of the cycli ethers 1,4‐dioxane and tetrahydrofuran by a monooxygenase in two Pseudonocardia species. Applied and Environmental Microbiology 79: 7702–7708.

van de Sande WWJ (2013) Global burden of human mycetoma: a systematic review and meta‐analysis. PLoS Neglected Tropical Diseases 7: e2550. DOI: 10.1371/journal.pntd.0002550.

Schaal KP and Yassin AF (2012) Genus Actinomyces. In: Goodfellow M, Kämpfer P, Busse H‐J, Trujillo ME, Suzuki K‐I, Ludwig W and Whitman WB (eds) Bergey's Manual of Systematic Bacteriology, vol. 5, pp. 42–109, 2nd edn, part A. New York: Springer.

Senthilkumar S, Kivakumar K and Kannan I (2005) Mercury resistant halophilic actinomycetes from the salt marsh environment of Vellar estuary, southeast coast of India. Journal of Aquatic Biology 20: 141–145.

Singleton DR, Furlong MA, Peacock AD, et al. (2003) Solirubrobacter pauli gen. nov., sp. nov., a mesophilic bacterium within the Rubrobacteridae related to common soil clones. International Journal of Systematic and Evolutionary Microbiology 53: 485–490.

Sorokin DY, van Pelt S, Tourova TP, et al. (2009) Nitriliruptor alkaliphilus gen. nov., sp. nov., a deep‐lineage haloalkaliphilic actinobacterium from soda lakes capable of growth on aliphatic nitriles, and proposal of Nitriliruptoraceae fam. nov. and Nitriliruptorales ord. nov. International Journal of Systematic and Evolutionary Microbiology 59: 248–253.

Sotgiu G, D'Ambrosio L, Centis R, et al. (2015) The multidrug‐resistant tuberculosis threat: old problems and new solutions. Journal of Thoracic Disease 7: 54–60.

Stackebrandt E, Rainey FA and Ward‐Rainey NL (1997) Proposal for a new hierarchic classification system, Actinobacteria classis nov. International Journal of Systematic and Evolutionary Microbiology 47: 479–491.

Trujillo ME, Alonso‐Vega P, Rodríguez R, et al. (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME Journal 4: 1265–1281.

Trujillo ME, Bacigalupe R, Pujic P, et al. (2014) Genome features of the endophytic actinobacterium Micromonospora lupini strain Lupac 08: on the process of adaptation to an endophytic life style? Plos One 9: e108522. DOI: 10.1371/journal.pone.0108522.

Trujillo ME, Goodfellow M, Busarakam K, et al. (2015) Modestobacter lapidis sp. nov. and Modestobacter muralis sp. nov., isolated from a deteriorated sandstone historic building in Salamanca, Spain. Antonie van Leeuwenhoek 108: 311–320.

Udwary DW, Zeigler L, Asolkar RN, et al. (2007) Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proceedings of the National Academy of Sciences USA 104: 10376–10381.

Walker M and Phillips CA (2007) The growth of Propionibacterium cyclohexanicum in fruit juices and its survival following elevated temperature treatments. Food Microbiology 24: 313–318.

Zarrilla KA and Perry JJ (1984) Thermoleophilum album gen. nov. and sp. nov., a bacterium obligate for thermophily and normal‐alkane substrates. Archives of Microbiology 137: 286–290.

Zhi XY, Li WJ and Stackebrandt E (2009) An update of the structure and 16S rRNA gene sequence‐based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. International Journal of Systematic and Evolutionary Microbiology 59: 589–608.

Further Reading

Albuquerque L, Johnson MM, Schumann P, et al. (2014) Description of two new thermophilic species of the genus Rubrobacter, Rubrobacter calidifluminis sp. nov. and Rubrobacter naiadicus sp. nov. and emended description of the genus Rubrobacter and the species Rubrobacter bracarensis. Systematic and Applied Microbiology 37: 235–243.

Goodfellow M, Kämpfer P, Busse H‐J, et al. (eds) (2012) Bergey's Manual of Systematic Bacteriology, vol. 5, The Actinobacteria, 2nd edn, Part B. New York: Springer.

Rosenberg E, DeLong EF, Lory S, Stackebrandt E and Thompson F (eds) (2014) The Prokaryotes, Actinobacteria, 4th edn. Berlin: Springer Verlag.

Sen A, Daubin V, Abrouk D, et al. (2014) Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. International Journal of Systematic and Evolutionary Microbiology 64: 3821–3832.

Staley JT, Gunsalus RP, Lory S and Perry JJ (eds) (2007) Microbial Life, 2nd edn. Sinauer Associates: Sunderland, MA.

Wainwright M (1991) Streptomycin: discovery and resultant controversy. History of Philosophy Life Sciences 13: 97–124.

Woodruff HB (2014) Selman A. Waksman, Winner of the 1952 Nobel Prize for Physiology or Medicine. Applied and Environmental Microbiology 80: 2–8.

Zijlstra EE, van de Sande WWJ, Welsh O, et al. (2016) Mycetoma: a unique neglected tropical disease. Lancet Infectious Diseases 16: 100–112.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Trujillo, Martha E(Apr 2016) Actinobacteria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020366.pub2]