Unlike synthetic metal chelators, microbe-assisted phytoremediation provides plants with natural metal-solubilizing chelators which do not constitute a potential source of environmental pollution. Concurrently with microbial chelators, plant growth promotion can be enhanced through bacterially-produced phytohormones. In this work, the simultaneous production of siderophores and auxins by Streptomyces was studied to gain insight for future application in plant growth and phytoremediation in a metal-contaminated soil. Standard auxin and siderophore detection assays indicated that all of the investigated Streptomyces strains can produce these metabolites simultaneously. However, Al(3+), Cd(2+), Cu(2+), Fe(3+) and Ni(2+), or a combination of Fe(3+) and Cd(2+), and Fe(3+) and Ni(2+) affected auxin production negatively, as revealed by spectrophotometry and gas chromatography-mass spectrometry. This effect was more dramatic in a siderophore-deficient mutant. In contrast, except for Fe, all the metals stimulated siderophore production. Mass spectrometry showed that siderophore and auxin-containing supernatants from a representative Streptomyces species contain three different hydroxamate siderophores, revealing the individual binding responses of these siderophores to Cd(2+) and Ni(2+), and thus, showing their auxin-stimulating effects. We conclude that siderophores promote auxin synthesis in the presence of Al(3+), Cd(2+), Cu(2+) and Ni(2+) by chelating these metals. Chelation makes the metals less able to inhibit the synthesis of auxins, and potentially increases the plant growth-promoting effects of auxins, which in turn enhances the phytoremediation potential of plants.