Genomic and phenotypic insights into Serratia interaction with plants from an ecological perspective

Abstract

We investigated the plant growth-promoting potential of two endophytic strains of Serratia marcescens, namely SmCNPMS2112 and SmUFMG85, which were isolated from the roots of the same maize (Zea mays) plant. The strains were evaluated in vitro for their ability to produce siderophores and indoleacetic acid, form biofilm, solubilize iron phosphate (Fe-P) and Araxá rock phosphate (RP), mineralize phytate, and for their ability to adhere and colonize host roots. Additionally, their plant growth-promoting potential was tested in vivo under greenhouse conditions using millet grown in soil under two fertilization schemes (triple superphosphate, TSP, or commercial rock phosphate, cRP). Both strains improved at least five physiological traits of millet or P content in soil. In order to elucidate the genetic basis of the plant growth-promoting ability of these strains, their genomes were compared. While both genomes exhibited a similar overall functional profile, each strain had unique features. SmCNPMS2112 contained genes related to arsenic and aromatic hydrocarbons degradation, whereas SmUFMG85 harbored genes related to rhamnolipid biosynthesis and chromium bioremediation. Also, we observe a unique repertoire of genes related to plant growth-promotion (PGP) in the SmUFMG85 genome, including oxalate decarboxylase (OxdC), associated with the catabolism of oxalic acid, and aerobactin siderophore (lucD) in the genome of SmCNPMS2112. The alkaline phosphatase was observed on two strains, but acid phosphatase was exclusive to SmUFMG85. Eighteen secondary metabolic gene clusters, such as those involved in the biosynthesis of macrolides and bacillomycin, among others, occur in both strains. Moreover, both genomes contained prophages, suggesting that viral-mediated horizontal gene transfer may be a key mechanism driving genomic variability in the endophytic environment. Indeed, the most genes unique and accessory of SmUFMG85 and SmCNPMS2112 were localized in genomic islands, highlighting genome plasticity and its underlying drivers. To investigate the ecological distribution of plant-interaction traits in the genus Serratia, the genomes of SmUFMG85 and SmCNPMS2112 strains were compared with those of other 19 Serratia strains of different species, which were isolated from different environments. We observe that many features for PGP are present in all genomes, regardless of niche, for instance: formation of flagella, fimbriae and pili, chemotaxis, biosynthesis of siderophores, indole-3-acetic acid (IAA) and volatile organic (VOC) and inorganic (VIC) compounds, such as acetoin and HCN. Also, all the analyzed genomes show an antimicrobial resistance repertoire of genes that confer resistance to several antibiotics belonging to the groups of aminoglycosides and quinolones, for instance. Also, from a niche partitioning perspective, secretion system preference and the ability to produce exopolysaccharides involved in biofilm formation are among the features that vary the most among strains, and most likely influence niche adaptation in Serratia spp., even though only the latter seems to be a feature specifically associated with virulence in the analyzed strains. Our results show that populations of bacteria sharing the same niche can present significant physiological and genomic differences, and reveal the intraspecific metabolic plasticity that underlie plant-bacteria interactions. Also, this study reveals the potential of two Serratia marcescens strains as bioinoculants in agriculture. Considering that Serratia spp. are regarded as low risk biological agents, despite the fact that they can be associated with human disease, we suggest that strain biosafety be evaluated using a combination of genome and phenotypic analyses, as presented herein.

Keywords: Endophytes; Maize; Niche partitioning; Pangenome; Plant-bacteria interaction; Serratia.