siderophore production control; iron piracy; nitrogen fertilizers; common scab; plant pathogen, potato disease
Abstract :
[en] Streptomyces scabiei is the causative agents of common scab on root and tuber crops. Life in the soil imposes intense competition between soil-dwelling microorganisms and we evaluated here the antimicrobial properties of S. scabiei. Under laboratory culture conditions, increasing peptone levels correlated with increased growth inhibitory properties of S. scabiei. Comparative metabolomics showed that production of S. scabiei siderophores (desferrioxamines, pyochelin, scabichelin and turgichelin) increased with the quantity of peptone thereby suggesting that they participate in growth inhibition. Mass spectrometry imaging further confirmed that the zones of secreted siderophores and growth inhibition coincided. Moreover, either the repression of siderophore production or the neutralization of their iron-chelating activity both led to increased microbial growth. Replacement of peptone by natural nitrogen sources regularly used as fertilizers such as ammonium nitrate, ammonium sulfate, sodium nitrate, and urea also triggered siderophore production in S. scabiei. The observed effect is not mediated by alkalinization of the medium as increasing the pH without providing additional nitrogen sources did not induce siderophore production. The nitrogen-induced siderophore production also inhibited the growth of important plant pathogens. Overall, our work suggests that not only the iron availability but also the nitrogen fertilizer sources could significantly impact the competition for iron between crop-colonizing microorganisms.
Treseder KK. Ecological strategies of microbes: thinking outside the triangle. J Ecol 2023;111:1832–43. https://doi.org/10.1111/1365-2745.14115
Chater KF, Biró S, Lee KJ et al. The complex extracellular biology of streptomyces. FEMS Microbiol Rev 2010;34:171–98. https://doi.org/10.1111/j.1574-6976.2009.00206.x
Chater KF, Losick R. Mycelial life style of Streptomyces coelicolor A3(2) and its relatives In: Shapiro JA & Dworkin M (eds.), Bacteria as Multicellular Organisms. New York: Oxford University Press. 1997, 149182.
Treseder KK, Lennon JT. Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev 2015;79:243–62. https://doi.org/10.1128/MMBR.00001-15
Lewin GR, Carlos C, Chevrette MG et al. Evolution and ecology of actinobacteria and their bioenergy applications. Annu Rev Microbiol 2016;70:235–54. https://doi.org/10.1146/ annurev-micro-102215-095748
Klein DA, Paschke MW. Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microb Ecol 2004;47:224–35. https://doi.org/10.1007/s00248-003-1037-4
Raines DJ, Moroz OV, Blagova EV et al. Bacteria in an intense competition for iron: key component of the Campylobacter jejuni iron uptake system scavenges enterobactin hydrolysis product. Proc Natl Acad Sci USA 2016;113:5850–5. https://doi.org/10.1073/pnas. 1520829113
Jarmusch SA, Lagos-Susaeta D, Diab E et al. Iron-meditated fungal starvation by lupine rhizosphere-associated and extremotolerant Streptomyces sp. S29 desferrioxamine production. Mol Omics 2021;17:95–107. https://doi.org/10.1039/D0MO00084A
Gu S, Wei Z, Shao Z et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol 2020;5:1002–10. https://doi.org/10.1038/ s41564-020-0719-8
Bignell DRD, Huguet-Tapia JC, Joshi MV et al. What does it take to be a plant pathogen: genomic insights from streptomyces species. Antonie Van Leeuwenhoek 2010;98:179–94. https://doi.org/10.1007/s10482-010-9429-1
Deflandre B, Stulanovic N, Planckaert S et al. The virulome of Streptomyces scabiei in response to cello-oligosaccharide elicitors. Microb Genom 2022;8:000760.
Liu J, Nothias L-F, Dorrestein PC et al. Genomic and metabolomic analysis of the potato common scab pathogen Streptomyces scabiei. ACS Omega 2021;6:11474–87. https://doi.org/10.1021/acsomega.1c00526
Kerff F, Jourdan S, Francis IM et al. Common scab disease: structural basis of elicitor recognition in pathogenic Streptomyces species. Microbiol Spectr 2023;11:e0197523.
Han W-C, Lee J-Y, Park D-H et al. Isolation and antifungal and antioomycete activity of Streptomyces scabiei strain PK-A41, the causal agent of common scab disease. Plant Pathol J 2004;20:115–26. https://doi.org/10.5423/PPJ.2004.20.2.115
Loria R, Bukhalid R, Creath R et al. Differential production of thaxtomins by pathogenic streptomyces species in vitro. Phytopathology 1995;85:537–41. https://doi.org/10.1094/ Phyto-85-537
Kieser T, Bibb MJ, Buttner MJ et al. Practical Streptomyces Genetics. Colney, Norwich, England: John Innes Foundation, 2000.
Shirling EB, Gottlieb D. Methods for characterization of streptomyces species 1. Int J Syst Evol Microbiol 1966;16:313–40. https://doi.org/10.1099/00207713-16-3-313
Caten C, Jinks J. Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can J Bot 1968;46:329–48. https://cdnsciencepub.com/doi/abs/10.1139/b68-055?journalCode=cjb1 (17 September 2023, date last accessed).
Adam D, Maciejewska M, Naômé A et al. Isolation, characterization, and antibacterial activity of hard-to-culture actinobacteria from cave moonmilk deposits. Antibiotics (Basel) 2018;7:28. https://doi.org/10.3390/antibiotics7020028
Maciejewska M, Adam D, Martinet L et al. A phenotypic and genotypic analysis of the antimicrobial potential of cultivable streptomyces isolated from cave moonmilk deposits. Front Microbiol 2016;7:1455. https://doi.org/10.3389/fmicb.2016.01455
Schwyn B, Neilands JB. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987;160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Shin SH, Lim Y, Lee SE et al. CAS agar diffusion assay for the measurement of siderophores in biological fluids. J Microbiol Methods 2001;44:89–95. https://doi.org/10.1016/S0167-7012(00)00229-3
Craig M, Lambert S, Jourdan S et al. Unsuspected control of siderophore production by N-acetylglucosamine in streptomycetes. Environ Microbiol Rep 2012;4:512–21. https://doi.org/10.1111/j.1758-2229.2012.00354.x
Lambert S, Traxler MF, Craig M et al. Altered desferrioxamine-mediated iron utilization is a common trait of bald mutants of Streptomyces coelicolor. Metallomics 2014;6:1390–9. https://doi.org/10.1039/C4MT00068D
Arora NK, Verma M. Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 2017;7:381. https://doi.org/10.1007/s13205-017-1008-y
Sinclair E, Trivedi DK, Sarkar D et al. Metabolomics of sebum reveals lipid dysregulation in Parkinson’s disease. Nat Commun 2021;12:1592. https://doi.org/10.1038/s41467-021-21669-4
Sun Y, Cheng G, Du L et al. Chuanzhitongluo capsule ameliorates microcirculatory dysfunction in rats: efficacy evaluation and metabolic profiles. Front Pharmacol 2022;13:1011333. https://doi.org/10.3389/fphar.2022.1011333
Burguet P, La Rocca R, Kune C et al. Exploiting differential signal filtering (DSF) and image structure filtering (ISF) methods for untargeted mass spectrometry imaging of bacterial metabolites. J Am Soc Mass Spectrom 2024;35:1743–55. https://doi.org/10.1021/jasms.4c00129
Flores FJ, Martín JF. Iron-regulatory proteins DmdR1 and DmdR2 of streptomyces coelicolor form two different DNA-protein complexes with iron boxes. Biochem J 2004;380:497–503. https://doi.org/10.1042/bj20031945
Tunca S, Barreiro C, Sola-Landa A et al. Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene. FEBS J 2007;274:1110–22. https://doi.org/ 10.1111/j.1742-4658.2007.05662.x
Johnson DB, Kanao T, Hedrich S. Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front Microbiol 2012;3:96. https://doi.org/10.3389/fmicb.2012.00096
Monhemius A. Precipitation diagrams for metal hydroxydes, sulphides, arsenates and phosphates. Trans Inst Min Metall 1977;86:C202–6.
Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Micro 2020;18:152–63. https://doi.org/10.1038/s41579-019-0284-4