Abstract
Several Streptomyces species cause plant diseases, including S. scabies, S. acidiscabies and S. turgidiscabies, which produce common scab of potato and similar diseases of root crops. These species produce thaxtomins, dipeptide phytotoxins that are responsible for disease symptoms. Thaxtomins are produced in vivo on diseased potato tissue and in vitro in oat-based culture media, but the regulation of thaxtomin biosynthesis is not understood. S. acidiscabies was grown in a variety of media to assess the impact of medium components on thaxtomin A (ThxA) production. ThxA biosynthesis was not correlated with bacterial biomass, nor was it stimulated by α-solanine or α-chaconine, the two most prevalent potato glycoalkaloids. ThxA production was stimulated by oat bran broth, even after exhaustive extraction, suggesting that specific carbohydrates may influence ThxA biosynthesis. Oat bran contains high levels of xylans and glucans, and both of these carbohydrates, as well as xylans from wheat and tamarind, stimulated ThxA production, but not to the same extent as oat bran. Starches and simple sugars did not induce ThxA production. The data indicate that complex carbohydrates may act as environmental signals to plant pathogenic Streptomyces, allowing production of thaxtomin and enabling bacteria to colonize its host.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antonopoulos VT, Hernandez MEA, Mavrakos E, Ball AS (2001) The use of extracellular enzymes from Streptomyces albus ATCC 3005 for the bleaching of eucalyptus kraft pulp. Appl Micro Biotech 57:92–97
Babcock MJ, Eckwall EC, Schottel JL (1993) Production and regulation of potato-scab-inducing phytotoxins by Streptomyces scabies. J Gen Microbiol 139:1579–1586
Beauséjour J, Goycer C, Vachon J, Beaulieu C (1999) Production of thaxtomin A by Streptomyces scabies strains in plant extract containing media. Can J Microbiol 45:764–768
Bentley SD et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147
Bernards M (2002) Demystifying suberin. Can J Bot 80:227–240
Bukhalid RA, Takeuchi T, Labeda D, Loria R (2002) Horizontal transfer of the plant virulence gene, nec1, and flanking sequences among genetically distinct Streptomyces strains in the diastatochromogenes cluster. Appl Environ Microbiol 68:738–744
Bunzel M, Ralph J, Lu F, Hatfield R, Steinhart H (2004) Lignins and ferulate-coniferyl alcohol cross-coupling products in cereal grains. J Agric Food Chem 52:6496–6502
Donadio S, Sosio M, Lancini G (2002) Impact of the first Streptomyces genome sequence on the discovery and production of bioactive substances. Appl Micro Biotech 60:377–380
Fernández-Abalos JA, Ruiz-Arribas A, Garda AL, Santamaría RI (1997) Effect of carbon source on the expression of celA 1 , a cellulase-encoding gene from Streptomyces halstedii JM8. FEMS Microbiol Lett 153:97–103
Fry BA, Loria R (2002) Thaxtomin A: evidence for a plant cell wall target. Physiol Mol Plant Pathol 60:1–8
Goto K (1985) The relative importance of precipitation and sugar content in potato peel for the detection of the incidence of common scab (Streptomyces scabies). Soil Sci Plant Nutr 31:419–425
Healy FG, Wach M, Krasnoff SB, Gibson DM, Loria R (2000) The txtAB genes of the plant pathogen Streptomyces acidiscabies encode a peptide synthetase required for phytotoxin thaxtomin A production and pathogenicity. Mol Microbiol 38:794–804
Healy FG, Krasnoff SB, Wach M, Gibson DM, Loria R (2002) Involvement of a cytochrome P450 monooxygenase in thaxtomin A biosynthesis by Streptomyces acidiscabies. J Bacteriol 184:2019–2029
Hiltunen LH, Weckman A, Ylhäinen A, Rita H, Richter E, Valkonen JPT (2005) Responses of potato cultivars to the common scab pathogens, Streptomyces scabies and S. turgidiscabies. Ann App Biol 146:395–403
Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermilitis. Nat Biotechnol 21:526–531
Kadam SS, Dhumal SS, Jambhale ND (1991) Structure, nutritional composition, and quality. In: Salunkhe DK, Kadam SS, Jadhav SJ (eds) Potato: production, processing, and products. CRC, Boca Raton, pp 9–35
Kers JA et al (2004) A bacterial nitric oxide synthase functions to nitrate a peptide phytotoxin. Nature 429:79–82
Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Media, buffers and supplies. In: Kieser T, Bibb MJ, Buttner NJ, Chater KF, Hopwood DA (eds) Practical Streptomyces genetics. The John Innes Foundation, Norwich
King RR, Lawrence CH (1996a) Characterization of new thaxtomin A analogues generated in vitro by Streptomyces scabies. J Agric Food Chem 40:834–837
King RR, Lawrence CH (1996b) Isolation and identification of pigments generated in vitro by Streptomyces acidiscabies. J Agric Food Chem 44:2849–2851
King RR, Lawrence CH, Calhoun LA (1992) Chemistry of phytotoxins associated with Streptomyces scabies, the causal organism of potato common scab. J Agric Food Chem 40:834–837
Koleva L, Stateva L, Vemkov P (1997–1998) Non-wasteful fractionation of fragile yeast cells for the production of nutritional protein and other by-products. Eur Food Res Technol 208:439–443
Lawrence CH, Clark MC, King RR (1990) Induction of common scab symptoms in aseptically cultured potato tubers by the vivotoxin, thaxtomin. Phytopathology 80:606–608
Lisinska G, Leszczynski W (1989) Potato tubers as a raw material for processing and nutrition. In: Potato science and technology. Elsevier, London, pp 11–43
López Fernández CL, Rodríguez J, Soliveri J, Copa-Patiño JL, Pérez-Leblic MI, Arias ME (1995) The effects of culture media on the production of xylan-degrading enzymes by Streptomyces chattanoogensis UAH 23. J Basic Microbiol 35:405–412
Loria R, Bukhalid RA, Creath RA, Leiner RH, Olivier M, Steffans JC (1995) Differential production of thaxtomins by pathogenic Streptomyces species in vitro. Phytopathology 85:537–541
Loria R, Bukhalid RA, Fry BA, King RR (1997) Plant pathogenicity in the genus Streptomyces. Plant Dis 81:836–846
Loria R, Coombs J, Yoshida M, Kers JA, Bukhalid RA (2003) A paucity of bacterial root diseases: Streptomyces succeeds where others fail. Physiol Mol Plant Pathol 62:65–72
Luhaloo M, Mårtensson AC, Andersson R, Äman P (1998) Compositional analysis and viscosity measurements of commercial oat brans. J Sci Food Agric 76:142–148
Madigan MT, Martinko JM, Parker J (2000) Brock biology of microorganisms, 9th edn. Prentice-Hall, Upper Saddle River
Miller DF (1958) Composition of cereal grains and forages. National Academy of Sciences-National Research Council, Washington, DC
Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M. (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. PNAS 98:12215–12220
Otero MA, Vasallo MdC, Verdecia O, Fernández V, Betancourt D (1996) A process for the complete fractionation of baker’s yeast. J Chem Tech Biotechnol 67:67–71
Pasco C, Jouan B, Andrivon D (2005) Resistance of potato genotypes to common and netted scab-causing species of Streptomyces. Plant Pathol 54:383–392
Roubroeks JP, Andersson R, Mastromauro DI, Christensen BE, Äman P (2001) Molecular weight, structure and shape of oat (1–3), (1–4)-beta-d-glucan fractions obtained by enzymatic degradation with (1–4)-beta-d-glucan 4-glucanohydrolase from Trichoderma reesei. Carbohydr Polymers 46:275–285
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Tai GCC, Murphy A, De Jong H (1996) Comparison of efficiency of alternative selection strategies: an example of selection for resistance to common scab in potatoes. Can J Plant Sci 76:849–852
Thompson CJ, Fink D, Nguyen LD (2002) Principles of microbial alchemy: insights from the Streptomyces coelicolor genome sequence. Genome Biol 3:1020.1021–1020.1024
Tuncer M, Ball AS (2003) Co-operative actions and degradation analysis of purified zylan-degrading enzymes from Thermomonospora fusca BD25 of oat-spelt xylan. J Appl Microbiol 94:1030–1035
Zazopoulous E et al (2003) A genomics-guided approach for discovering and expressing cryptic metabolic pathways. Nat Biotechnol 21:187–190
Acknowledgments
We gratefully acknowledge the helpful discussions with Jocelyn Rose, Johann Kers and Evan Johnson. This project was funded by the USDA, ARS Potato Research Program, and a research fellowship to M. Wach through NIH Chemistry of Biological Systems Training Grant at Cornell University. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the US Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that may also be suitable.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wach, M.J., Krasnoff, S.B., Loria, R. et al. Effect of carbohydrates on the production of thaxtomin A by Streptomyces acidiscabies . Arch Microbiol 188, 81–88 (2007). https://doi.org/10.1007/s00203-007-0225-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-007-0225-x