Fitness in soil and rhizosphere of Pseudomonas fluorescens C7R12 compared with a C7R12 mutant affected in pyoverdine synthesis and uptake

Abstract

Fluorescent pseudomonads have evolved an efficient strategy of iron uptake based on the synthesis of the siderophore pyoverdine and its relevant outer membrane receptor. The possible implication of pyoverdine synthesis and uptake on the ecological competence of a model strain (Pseudomonas fluorescens C7R12) in soil habitats was evaluated using a pyoverdine minus mutant (PL1) obtained by random insertion of the transposon Tn5. The Tn5 flanking DNA was amplified by inverse PCR and sequenced. The nucleotide sequence was found to show a high level of identity with pvsB, a pyoverdine synthetase. As expected, the mutant PL1 was significantly more susceptible to iron starvation than the wild-type strain despite its ability to produce another unknown siderophore. As with the wild-type strain, the mutant PL1 was able to incorporate the wild-type pyoverdine and five pyoverdines of foreign origin, but at a significantly lower rate despite the similarity of the outer membrane protein patterns of the two strains. The survival kinetics of the wild-type and of the pyoverdine minus mutant, in bulk and rhizosphere soil, were compared under gnotobiotic and non-gnotobiotic conditions. In gnotobiotic model systems, both strains, when inoculated separately, showed a similar survival in soil and rhizosphere, suggesting that iron was not a limiting factor. In contrast, when inoculated together, the bacterial competition was favorable to the pyoverdine producer C7R12. The efficient fitness of PL1 in the presence of the indigenous microflora, even when coinoculated with C7R12, is assumed to be related to its ability to uptake heterologous pyoverdines. Altogether, these results suggest that pyoverdine-mediated iron uptake is involved in the ecological competence of the strain P. fluorescens C7R12. ß

Role of iron and the TonB system in colonization of corn seeds and roots by Pseudomonas putida KT2440

“…These results are in agreement with previous observations indicating that iron uptake via production of the siderophore pyoverdine by P. fluorescens plays an important role in soil and rhizosphere survival (Mirleau et al ., 2000). As with the exbB/exbD/tonB mutant described here, a P. fluorescens mutant affected in the synthesis of pyoverdine was able to colonize the tomato rhizosphere when inoculated individually, but showed a competitive disadvantage when co‐inoculated with the wild type in sterile soil.…”

“…As with the exbB/exbD/tonB mutant described here, a P. fluorescens mutant affected in the synthesis of pyoverdine was able to colonize the tomato rhizosphere when inoculated individually, but showed a competitive disadvantage when co‐inoculated with the wild type in sterile soil. However, in the presence of indigenous microbiota, this mutant was able to survive, probably thanks to its ability to take up heterologous siderophores (Mirleau et al ., 2000). In our case, as the ExbB/ExbD/TonB complex is required to activate siderophore uptake systems, this capacity would be lost.…”

Diversity of siderophore‐mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines

“…Fluorescent pseudomonads are also able to produce siderophores other than PVDs, but their detection is often possible only in a PVD‐negative background, using the universal chrome azurol siderophore (CAS) detection assay of Schwyn and Neilands (Schwyn and Neilands, 1987; Mirleau et al ., 2000; Mossialos et al ., 2000; Mercado‐Blanco et al ., 2001).…”

Phenazines and their role in biocontrol by Pseudomonas bacteria

“…The mutant mutated in both nitrate reductase and pyoverdine synthesis displayed the lowest competitiveness. The selective advantage given by nitrate reductase was more apparent under conditions of lower aeration (Mirleau et al ., 2000; Mirleau et al ., 2001).…”