Secondary metabolites from plant‐associated Pseudomonas are overproduced in biofilm

Abstract

Plant rhizosphere soil houses complex microbial communities in which microorganisms are often involved in intraspecies as well as interspecies and inter-kingdom signalling networks. Some members of these networks can improve plant health thanks to an important diversity of bioactive secondary metabolites. In this competitive environment, the ability to form biofilms may provide major advantages to microorganisms. With the aim of highlighting the impact of bacterial lifestyle on secondary metabolites production, we performed a metabolomic analysis on four fluorescent Pseudomonas strains cultivated in planktonic and biofilm colony conditions. The untargeted metabolomic analysis led to the detection of hundreds of secondary metabolites in culture extracts. Comparison between biofilm and planktonic conditions showed that bacterial lifestyle is a key factor influencing Pseudomonas metabolome. More than 50% of the detected metabolites were differentially produced according to planktonic or biofilm lifestyles, with the four Pseudomonas strains overproducing several secondary metabolites in biofilm conditions. In parallel, metabolomic analysis associated with genomic prediction and a molecular networking approach enabled us to evaluate the impact of bacterial lifestyle on chemically identified secondary metabolites, more precisely involved in microbial interactions and plant-growth promotion. Notably, this work highlights the major effect of biofilm lifestyle on acyl-homoserine lactone and phenazine production in P. chlororaphis strains.

A Cross-Metabolomic Approach Shows that Wheat Interferes with Fluorescent Pseudomonas Physiology through Its Root Metabolites

“…Moreover, apart from these bacterial secondary metabolites known to be involved in plant–bacteria interactions, two newly described families of secondary metabolites were significantly accumulated in F113 in response to root extracts. On one hand, the production of two pyridine-2,6-thiocarboxylic derivatives (PDTC) m/z 198 and m/z 228 [ 28 ] was increased in response to plant extracts; for example, the m/z 198 compound was 930-, 927- and 358-fold overproduced in the presence of Adular, Bordeaux and Soissons extracts, respectively ( Figure 3 ). On the other hand, the production of three atypical compounds described as acyl-dihydro-methyl-pyrrol derivatives [ 28 ], was also strongly influenced by root extracts.…”

“…On one hand, the production of two pyridine-2,6-thiocarboxylic derivatives (PDTC) m/z 198 and m/z 228 [ 28 ] was increased in response to plant extracts; for example, the m/z 198 compound was 930-, 927- and 358-fold overproduced in the presence of Adular, Bordeaux and Soissons extracts, respectively ( Figure 3 ). On the other hand, the production of three atypical compounds described as acyl-dihydro-methyl-pyrrol derivatives [ 28 ], was also strongly influenced by root extracts. The derivative whose synthesis was mostly affected was the m/z 280 compound, with a 46-, 29- and 44-fold overproduction in the presence of Adular, Bordeaux and Soissons extracts, respectively ( Figure 3 ).…”

“…In order to evaluate the impact of plant extracts on the expression of bacterial phytobeneficial properties, we focused our attention on bioactive secondary metabolites produced by the studied strains [ 14 , 28 ]. The secondary metabolism of the five Pseudomonas strains was previously described by us [ 28 ].…”

“…Accordingly, strains P. kilonensis F113, P. protegens CHA0, P. chlororaphis JV395B and P. chlororaphis JV497 belong to the CPC clade, whereas P. koreensis JV222 belongs to the FMJK clade [ 14 ]. They produce a wide range of antimicrobial compounds like 2,4-diacetylphloroglucinol (DAPG), pyoluteorin, phenazine or pyrrolnitrin involved in plant protection, as well as indolic derivatives and signaling compounds involved in plant-growth stimulation and plant-bacteria interaction [ 23 , 24 , 25 , 26 , 27 , 28 ].…”

Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence

“…In a previous study we found that different growth media inflicted variations in the resulting interaction between Bacillus subtilis and Pseudomonas chlororaphis 15 . The two strains come into close contact in lysogeny broth (LB) medium, while in King's B medium, which promotes the production of secondary metabolites by Pseudomonas strains 24 , the two colonies were physically separated by a typical inhibition halo (Suppl. Figure 1a).…”