Abstract
The influence of iron, aluminium and of the combined application of both metals on microbial biomass and production of siderophores by three fungi (Aspergillus nidulans, Neurospora crassa and Hymenoscyphus ericae) were investigated. All three species showed a strong iron regulation and Al-sensitivity of siderophore biosynthesis although several differences remained species dependent. Inhibitory effects of Fe and Al on siderophore-production were additive and the higher binding capacity of siderophores towards iron could be compensated by a higher Al-availability. Although pH itself is also important for regulation of siderophore biosynthesis, an indirect effect of Al on siderophore production via an Al-induced pH decrease could be outlined. The toxic effects of Al resulting in a reduced biomass production were compensated by high Fe-availability, whereas the addition of DFAM, a bacterial siderophore, enhanced Al-toxicity.
Similar content being viewed by others
References
AM Albrecht-Gary AL Crumbliss (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release A Sigel H Sigel (Eds) Iron Transport and Storage in Microorganisms, Plants, and Animals Marcel Dekker New York 239–327
JEL Arceneaux ME Boutwell BR Byers (1984) ArticleTitleEnhancement of copper toxicity by siderophores in Bacillus megaterium Antimicrob Agents Ch 25 650–652 Occurrence Handle1:CAS:528:DyaL2cXksFWmu70%3D
H Babich G Stotzky (1980) ArticleTitleEnvironmental factors that influence the toxicity of heavy metal and gaseous pollutants to microorganisms Crit Rev Microbiol 8 99–145 Occurrence Handle7000442 Occurrence Handle1:CAS:528:DyaL3MXisFOgug%3D%3D
J Barceló C Poschenrieder (2002) ArticleTitleFast root growth response, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review Environm Experim Bot 48 75–92 Occurrence Handle10.1016/S0098-8472(02)00013-8
H Boukhalfa AL Crumbliss (2002) ArticleTitleChemical aspects of siderophore mediated iron transport BioMetals 15 325–339 Occurrence Handle12405526 Occurrence Handle1:CAS:528:DC%2BD38XntFSgtbo%3D Occurrence Handle10.1023/A:1020218608266
GUL Braga RHR Destéfano CL Messias (1999) ArticleTitleProtease production during growth and autolysis of submerged Metarhizium anisopliae cultures Revista de Microbiologia 30 107–113 Occurrence Handle1:CAS:528:DyaK1MXnvValu7o%3D Occurrence Handle10.1590/S0001-37141999000200004
S Chamnongpol W Dodson MJ Cromie ZL Harris EA Groisman (2002) ArticleTitleFe(III)-mediated cellular toxicity Mol Microbiol 45 711–719 Occurrence Handle12139617 Occurrence Handle1:CAS:528:DC%2BD38Xmt1yrtr0%3D Occurrence Handle10.1046/j.1365-2958.2002.03041.x
WB Davis MJ McCauley BR Byers (1971) ArticleTitleIron requirements and aluminium sensitivity of an hydroxamic acid-requiring strain of Bacillus megaterium J Bacteriol 105 589–594 Occurrence Handle4993339 Occurrence Handle1:CAS:528:DyaE3MXntlWisg%3D%3D
M Eisendle H Oberegger R Buttinger P Illmer H Haas (2004) ArticleTitleBiosynthesis and uptake of siderophores is controlled by the PacC-mediated ambient-pH regulatory system in Aspergillus nidulans Eukaryotic Cell 3 561–563 Occurrence Handle15075286 Occurrence Handle1:CAS:528:DC%2BD2cXjtlKqsL4%3D Occurrence Handle10.1128/EC.3.2.561-563.2004
C Exley (2003) ArticleTitleThe pro-oxidant activity of aluminium Free Radical Bio Med 36 380–387 Occurrence Handle10.1016/j.freeradbiomed.2003.11.017 Occurrence Handle1:CAS:528:DC%2BD2cXnvVKgtQ%3D%3D
A Federspiel R Schuler K Haselwandter (1991) ArticleTitleEffect of pH, L-ornithine and L-proline on the hydroxamate siderophore production by Hymenoscyphus ericae, a typical ericoid mycorrhizal fungus Plant Soil 130 259–261 Occurrence Handle1:CAS:528:DyaK3MXhtl2mtbw%3D Occurrence Handle10.1007/BF00011881
M Gaspar R Grazina A Bodor E Farkas MA Santos (1999) ArticleTitleSiderophore analogues: a new macrocyclic tetraamine tris(hydroxamate) ligand; synthesis and solution chemistry of the iron(III), aluminium(III) and copper(II) complexes J Chem Soc, Dalton Trans 5 799–806 Occurrence Handle10.1039/a809039d
MS Golub JL Domingo (1996) ArticleTitleWhat we know and what we need to know about developmental aluminium toxicity J Toxicol Environm Health 48 585–597 Occurrence Handle1:CAS:528:DyaK28XltlKitrw%3D Occurrence Handle10.1080/009841096161087
H Haas (2003) ArticleTitleMolecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage Appl Microbiol Biotechnol 62 316–330 Occurrence Handle12759789 Occurrence Handle1:CAS:528:DC%2BD3sXmslCmuro%3D Occurrence Handle10.1007/s00253-003-1335-2
K Hantke (1987) ArticleTitleFerrous iron transport mutants in Escherichia coli K12 FEMS Microbiol Lett 44 53–57 Occurrence Handle1:CAS:528:DyaL2sXlslahs7s%3D Occurrence Handle10.1111/j.1574-6968.1987.tb02241.x
K Haselwandter G Winkelmann (1998) Identification and characterization of siderophores of mycorrhizal fungi A Varma (Eds) Mycorrhiza Manual Springer Heidelberg 243–254
X Hu GL Boyer (1996) ArticleTitleSiderophore-mediated aluminium uptake by Bacillus megaterium ATCC 19213 Appl Environm Microbiol 62 4044–4048 Occurrence Handle1:CAS:528:DyaK28Xms1Kiur0%3D
P Illmer C Erlebach (2003) ArticleTitleInfluence of Al on growth, cell size and content of intracellular water of Arthrobacter sp. PI/1–95 Anton Leeuw Int J G 84 239–246 Occurrence Handle1:CAS:528:DC%2BD3sXnslarurY%3D Occurrence Handle10.1023/A:1026024428451
P Illmer U Obertegger F Schinner (2003) ArticleTitleMicrobiological properties in acidic forest soils with special consideration of KCl extractable Al Water Air Soil Poll 148 3–14 Occurrence Handle10.1023/A:1025422229468
NM Johnson CT Driscoll JS Eaton GE Likens WH Mcdowell (1981) ArticleTitle‘Acid rain’, dissolved aluminium and chemical weathering at the Hubbard Brook Experimental Forest, New Hampshire Geochim Cosmochim Acta 45 1421–1437 Occurrence Handle1:CAS:528:DyaL38XnsVansA%3D%3D Occurrence Handle10.1016/0016-7037(81)90276-3
JL Martinez A Delgado-Iribarren F Baquero (1990) ArticleTitleMechanisms of iron acquisition and bacterial virulence FEMS Microb Rev 75 45–56 Occurrence Handle1:CAS:528:DyaK3cXhslGhu7w%3D
J Middaugh R Hamel G Jean–Baptiste R Beriault D Chenier VD Appanna (2005) ArticleTitleAluminium triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase J Biol Chem 280 3159–3165 Occurrence Handle15548528 Occurrence Handle1:CAS:528:DC%2BD2MXovVCrsA%3D%3D Occurrence Handle10.1074/jbc.M411979200
JB Neilands (1993) ArticleTitleSiderophores Arch Biochem Biophys 302 1–3 Occurrence Handle8470885 Occurrence Handle1:CAS:528:DyaK3sXisFWju74%3D Occurrence Handle10.1006/abbi.1993.1172
H Oberegger M Schoeser I Zadra B Abt H Haas (2001) ArticleTitleSREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans Mol Microbiol 41 1077–1089 Occurrence Handle11555288 Occurrence Handle1:CAS:528:DC%2BD3MXntlGhsL8%3D Occurrence Handle10.1046/j.1365-2958.2001.02586.x
RG Pina C Cervantes (1996) ArticleTitleMicrobial Interaction with aluminium BioMetals 9 311–316 Occurrence Handle8696081 Occurrence Handle1:STN:280:DyaK283ovV2iuw%3D%3D Occurrence Handle10.1007/BF00817932
S Ratering S Schnell (2000) ArticleTitleLocalization of iron-reducing activity in paddy soil by profile studies Biochem 48 341–365 Occurrence Handle1:CAS:528:DC%2BD3cXitFygsrk%3D
DJ Read (1996) ArticleTitleThe structure and function of the ericoid mycorrhizal root Annals Bot 77 365–374 Occurrence Handle1:CAS:528:DyaK28XislGgsLk%3D Occurrence Handle10.1006/anbo.1996.0044
NJ Rogers KC Carson AR Glenn MJ Dilworth MN Hughes RK Poole (2001) ArticleTitleAlleviation of aluminium toxicity to Rhizobium leguminosarum bv. viciae by the hydroxamate siderophore vicibactin BioMetals 14 59–66 Occurrence Handle11368276 Occurrence Handle1:CAS:528:DC%2BD3MXjsFCns7g%3D Occurrence Handle10.1023/A:1016691301330
N Roy PK Chakrabartty (2000) ArticleTitleEffect of aluminium on the production of siderophore by Rhizobium sp. (Cicer arietinum) Curr Microbiol 41 5–10 Occurrence Handle10919391 Occurrence Handle1:CAS:528:DC%2BD3cXkvVOrsb4%3D Occurrence Handle10.1007/s002840010082
J Savory C Exley WF Forbes Y Huang JG Joshi T Kruck DRC McLachlan I Wakayama (1996) ArticleTitleCan the controversy of the role of aluminium in Alzheimer’s disease be resolved? What are the suggested approaches to this controversy and methological issues to be considered? J Toxicol Env Health 48 615–635 Occurrence Handle1:CAS:528:DyaK28XltlKitro%3D Occurrence Handle10.1080/009841096161104
B Schwyn JB Neilands (1987) ArticleTitleUniversal chemical assay for the detection and determination of siderophores Anal Biochem 160 47–56 Occurrence Handle2952030 Occurrence Handle1:CAS:528:DyaL2sXhtFKjurs%3D Occurrence Handle10.1016/0003-2697(87)90612-9
M Shenker Y Hadar Y Chen (1996) ArticleTitleStability constants of the fungal siderophore rhizoferrin with various microelements and calcium Soil Sci Soc Am J 60 1140–1144 Occurrence Handle1:CAS:528:DyaK28Xktl2qsb4%3D Occurrence Handle10.2136/sssaj1996.03615995006000040026x
M Sritharan (2000) ArticleTitleIron as a candidate in virulence and pathogenesis in mycobacteria and other microorganisms World J Microb Biot 16 769–780 Occurrence Handle1:CAS:528:DC%2BD3MXjtVynuro%3D Occurrence Handle10.1023/A:1008995313232
S.-C Tam JG McColl (1990) ArticleTitleAluminium- and calcium-binding affinities of some organic ligands in acidic conditions J Environm Qual 19 514–520 Occurrence Handle1:CAS:528:DyaK3cXlsFWgs7s%3D Occurrence Handle10.2134/jeq1990.193514x
PAW vanHees US Lundström R Danielsson L Nyberg (2001) ArticleTitleControlling mechanisms of aluminium in soil solution-an evaluation of 180 podzolic forest soils Chemosphere 45 1091–1101 Occurrence Handle1:CAS:528:DC%2BD3MXntVehtLw%3D Occurrence Handle10.1016/S0045-6535(00)00515-4
G Winkelmann (1991) Specifity of iron transport in bacteria and fungi G Winkelmann (Eds) Handbook of Microbial Iron Chelates CRC Press Boca Raton 65–105
G Winkelmann H Drechsel (1997) Microbial siderophores H Kleinkauf H Döhren Particlevon (Eds) Products of Secondary Metabolism NumberInSeries7 Weinheim VCH Verlagsgesellschaft 199–246
RA Yokel (2002) ArticleTitleAluminium chelation principles and recent advances Coord Chem Rev 228 97–113 Occurrence Handle1:CAS:528:DC%2BD38XksVemu7k%3D Occurrence Handle10.1016/S0010-8545(02)00078-4
P Zatta T Kiss M Suwalsky G Berthon (2002) ArticleTitleAluminium(III) as a promoter of cellular oxidation Coord Chem Rev 228 227–284 Occurrence Handle10.1016/S0010-8545(02)00073-5
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Illmer, P., Buttinger, R. Interactions between iron availability, aluminium toxicity and fungal siderophores. Biometals 19, 367–377 (2006). https://doi.org/10.1007/s10534-005-3496-1
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10534-005-3496-1