Deamination of the ethylene precursor 1‐aminocyclopropane‐1‐carboxylic acid (ACC) is a key plant‐beneficial trait found in plant growth‐promoting rhizobacteria (PGPR) and phytosymbiotic bacteria, but the diversity of the corresponding gene (acdS) is poorly documented. Here, acdS sequences were obtained by screening putative ACC deaminase sequences listed in databases, based on phylogenetic properties and key residues. In addition, acdS was sought in 71 proteobacterial strains by PCR amplification and/or hybridization using colony dot blots. The presence of acdS was confirmed in established AcdS+ bacteria and evidenced noticeably in Azospirillum (previously reported as AcdS−), in 10 species of Burkholderia and six Burkholderia cepacia genomovars (which included PGPR, phytopathogens and opportunistic human pathogens), and in five Agrobacterium genomovars. The occurrence of acdS in true and opportunistic pathogens raises new questions concerning their ecology in plant‐associated habitats. Many (but not all) acdS+ bacteria displayed ACC deaminase activity in vitro, including two Burkholderia clinical isolates. Phylogenetic analysis of partial acdS and deduced AcdS sequences evidenced three main phylogenetic clusters, each gathering pathogens and plant‐beneficial strains of contrasting geographic and habitat origins. The acdS phylogenetic tree was only partly congruent with the rrs tree. Two clusters gathered both Betaprotobacteria and Gammaproteobacteria, suggesting extensive horizontal transfers of acdS, noticeably between plant‐associated Proteobacteria.
The phytostimulatory alphaproteobacterium Azospirillum lipoferum 4B exhibits the plant-beneficial gene acdS, which enables deamination of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). Here, we show that acdS is in the vicinity of acdR, a homolog to leucine-responsive regulator lrp, in A. lipoferum 4B and most other acdS+ Proteobacteria. Unlike in Beta- and Gammaproteobacteria, acdS (and acdR) is preferentially located on symbiotic islands and plasmids in Alphaproteobacteria. In A. lipoferum 4B, acdS was mapped on a 750-kb plasmid that is lost during phenotypic variation, whereas other phytobeneficial genes such as nifH (associative nitrogen fixation) are maintained. In Proteobacteria, the phylogenies of acdR and acdS were largely but not totally congruent, despite physical proximity of the genes, regardless of whether DNA or deduced protein sequences were used. Potential Lrp, cAMP receptor protein (CRP) and fumarate-nitrate reduction regulator (FNR) binding sites were evidenced in the acdS promoter regions of strain 4B and most of 46 other acdS+ Proteobacteria. Indeed, transcriptional and enzymatic analyses done in vitro pointed to the involvement of Lrp- and FNR-like transcriptional up-regulation of ACC deaminase activity in A. lipoferum 4B. This is the first synteny, phylogenetic, and functional analysis of factors modulating acdS expression in Azospirillum plant growth-promoting rhizobacterium.
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