The Biocontrol Agent and Insect Pathogen Photorhabdus luminescens Interacts with Plant Roots

Abstract

Sustainable agriculture techniques are rising to improve pest management and environmental safety: biological control agents are used to enhance disease resistance and abiotic stress tolerance in crops. Here we investigated the capacity of Photorhabdus luminescens secondary variant to react to plant root exudates and its behaviour towards microorganisms in the rhizosphere. P. luminescens is known to live in symbiosis with entomopathogenic nematodes (EPNs) and to be highly pathogenic towards insects. The P. luminescens-EPNs relationship has been widely studied and used as a biological control agent, however, not much attention has been given on a putative lifestyle of P. luminescens in the rhizosphere. We performed transcriptome analysis to show how P. luminescens responds to plant root exudates. The analysis highlighted genes involved in chitin degradation, biofilm regulation, flagella formation and type VI secretion system. Furthermore, we provide evidence that P. luminescens can inhibit growth of phytopathogenic fungi. Finally, we demonstrated a specific interaction of P. luminescens with plant roots. Understanding the role and the function of this bacterium in the rhizosphere might accelerate the progress in biocontrol manipulation and elucidate the peculiar mechanisms adopted by plant growth-promoting rhizobacteria in plant roots interaction. Importance of the study Insect pathogenic Photorhabdus luminescens bacteria are widely used in biocontrol strategies against pests. Very little is known about the life of these bacteria in the rhizosphere. Here we show that P. luminescens can specifically react to and interact with plant roots. Understanding the adaptation of P. luminescens in the rhizosphere is highly important for the biotechnological application of entomopathogenic bacteria and could improve future sustainable pest management in agriculture.

Pseudomonas simiae WCS417: star track of a model beneficial rhizobacterium

“…2c) and the root hairs were extended ( Fig. 2d; Poitout et al 2017;Regaiolo et al 2020;Zamioudis et al 2013). These WCS417-induced features provided the plant with an enhanced capacity to take up water and mineral nutrients, resulting in a 2-3 fold increase in shoot fresh weight in this experimental setup (Wintermans et al 2016;Zamioudis et al 2013).…”

Two novel XRE-like transcriptional regulators control phenotypic heterogeneity in Photorhabdus luminescens cell populations

“…Recently, we demonstrated that P. luminescens 2° cells specifically interact with plant roots, uncovering a different life cycle for the bacteria in soil in absence of the nematode partners [ 9 ]. Transcriptome comparison of 2° cells in presence and absence of plant root exudates highlighted another two XRE-like regulators (PluDJC_03960 and PluDJC_10030), which were highly upregulated in 2° cells upon exposition towards plant root exudates [ 9 ]. This suggested that XRE-like regulators are not only involved in phenotypic switching from 1° to 2°, but also in the adaptation of 2° cells to plants.…”

“…Importantly, while both cell forms are equally pathogenic towards insects, 2° cells are not able to re-associate with the nematodes after depletion of nutrients derived by the insect host [ 7 , 8 ]. Recently, 2° cells have been shown to specifically interact with plant roots and adapt to an alternative life-style when remaining in soil after the nematodes have left the depleted insect cadaver [ 9 ]. Since phenotypic switching from 1° to 2° cells also takes place after prolonged cultivation under laboratory conditions, a response to metabolic or environmental stress has been suggested [ 10 ].…”

Photorhabdus spp.: An Overview of the Beneficial Aspects of Mutualistic Bacteria of Insecticidal Nematodes

“…Hence, various formulations ( Figure 1 ), mainly based on just the bacteria and/or bacterial metabolites, have been recorded [ 2 , 4 , 12 , 51 , 52 , 53 , 54 , 55 , 56 , 57 ]. In this regard, increased pathogenicity islands of the Photorhabdus chromosome, with many genes encoding various insecticidal protein toxins, antibiotics, bacteriocins, and enzymes, were reviewed [ 5 , 58 , 59 ], but more have still been further identified, e.g., [ 55 , 56 , 60 , 61 ]. For instance, the insecticidal categories of protein toxins comprise toxin complexes (TCs), Photorhabdus insect-related (Pir) proteins, makes caterpillars floppy (Mcf) toxins, Photorhabdus virulence cassettes (Pvc), Photorhabdus insecticidal toxin (Pit), Photox, PaxAB, and Galtox [ 9 ].…”