The Potato Yam Phyllosphere Ectosymbiont Paraburkholderia sp. Msb3 Is a Potent Growth Promotor in Tomato

Abstract

The genus Paraburkholderia includes a variety of species with promising features for sustainable biotechnological solutions in agriculture through increasing crop productivity. Here, we present a novel Paraburkholderia isolate, a permanent and predominant member of the Dioscoreae bulbifera (yam family, Dioscoreaceae) phyllosphere, making up to 25% of the microbial community on leaf acumens. The 8.5 Mbp genome of isolate Msb3 encodes an unprecedented combination of features mediating a beneficial plant-associated lifestyle, including biological nitrogen fixation (BNF), plant hormone regulation, detoxification of various xenobiotics, degradation of aromatic compounds and multiple protein secretion systems including both T3SS and T6SS. The isolate exhibits significant growth promotion when applied to agriculturally important plants such as tomato, by increasing the total dry biomass by up to 40%. The open question about the "beneficial" nature of this strain led us to investigate ecological and generic boundaries in Burkholderia sensu lato. In a refined phylogeny including 279 Burkholderia sensu lato isolates strain Msb3 clusters within Clade I Paraburkholderia, which also includes few opportunistic strains that can potentially act as pathogens, as revealed by our ecological meta-data analysis. In fact, we demonstrate that all genera originating from the "plant beneficial and environmental" (PBE) Burkholderia species cluster include opportunists. This indicates that further functional examinations are needed before safe application of these strains in sustainable agricultural settings can be assured.

Modes of Action of Microbial Biocontrol in the Phyllosphere

“…These gene clusters were highly similar to type III secretion systems in other beneficial bacteria, but distinct compared to phytopathogenic P. syringae . Also on the phyllosphere, type III secretion systems have been identified in the genome of a non-pathogenic Paraburkholderia isolate ( Herpell et al, 2020 ). However, more research is needed to determine the presence of type III secretion systems in other beneficial phyllosphere bacteria, to identify effectors associated with pathogens versus biocontrol effectors, and to determine the role of these type III secretion systems in beneficial host–microbe interactions.…”

Paraburkholderia dioscoreae sp. nov., a novel plant associated growth promotor

“…The present study was performed to formally classify strain Msb3 T , which was isolated from the phyllosphere of the 'air potato yam' , Dioscorea bulbifera [6]. Herpell et al [6] demonstrated that this strain is closely related to Paraburkholderia xenovorans and reported several genomic, taxonomic, functional and ecological characteristics of this organism.…”

“…The genus Paraburkholderia contains species formally classified as Burkholderia that were separated from the latter on the basis of phylogenomic evidence [1]. The majority of Paraburkholderia species have been isolated from soil and plant roots or nodules but some have been found in aquatic environments and as opportunistic human pathogens, too [2][3][4][5][6][7]. Bacteria within the genus usually carry large genomes (7)(8)(9)(10) and are metabolically versatile.…”

Dissecting Metabolism of Leaf Nodules in Ardisia crenata and Psychotria punctata

“…The identified bacterial endophytes belong to the order Burkholderiales within the Betaproteobacteria (Yang and Hu, 2018). Certain forms of associations which might present early stages of the development of leaf nodule symbiosis or divergence from early forms of leaf nodule symbiosis, have also been reported (Lemaire et al, 2012;Herpell et al, 2020). Most endophytic bacteria have undergone evolutionary genome reduction as result of this symbiosis to an extend that they are no longer capable of freely living outside their host (Carlier and Eberl, 2012;Carlier et al, 2016).…”

“…Candidatus Caballeronia crenata, the symbiont of A. crenata (Carlier et al, 2016) and a novel bacterial ectosymbiont Paraburkholderia sp. Msb3 from leaf acumens of Dioscorea bulbifera (Herpell et al, 2020). Considering the metabolic capabilities of both, plants and bacteria, there is evidence that leaf nodulated species might be a great resource for novel biologically active natural products.…”