Screening for Fusarium Antagonistic Bacteria From Contrasting Niches Designated the Endophyte Bacillus halotolerans as Plant Warden Against Fusarium

Abstract

Date palm (Phoenix dactylifera L.) plantations in North Africa are nowadays threatened with the spread of the Bayoud disease caused by Fusarium oxysporum f. sp. albedinis, already responsible for destroying date production in other infected areas, mainly in Morocco. Biological control holds great promise for sustainable and environmental-friendly management of the disease. In this study, the additional benefits to agricultural ecosystems of using plant growth promoting rhizobacteria (PGPR) or endophytes are addressed. First, PGPR or endophytes can offer an interesting bio-fertilization, meaning that it can add another layer to the sustainability of the approach. Additionally, screening of contrasting niches can yield bacterial actors that could represent wardens against whole genera or groups of plant pathogenic agents thriving in semi-arid to arid ecosystems. Using this strategy, we recovered four bacterial isolates, designated BFOA1, BFOA2, BFOA3 and BFOA4, that proved very active against F. oxysporum f. sp. albedinis. BFOA1–BFOA4 proved also active against 16 Fusarium isolates belonging to four species: F. oxysporum (with strains phytopathogenic of Olea europaea and tomato), F. solani (with different strains attacking O. europaea and potato), F. acuminatum (pathogenic on O. europaea) and F. chlamydosporum (phytopathogenic of O. europaea). BFOA1–BFOA4 bacterial isolates exhibited strong activities against another four major phytopathogens: Botrytis cinerea, Alternaria alternata, Phytophthora infestans, and Rhizoctonia bataticola. Isolates BFOA1–BFOA4 had the ability to grow at temperatures up to 35°C, pH range of 5–10, and tolerate high concentrations of NaCl and up to 30% PEG. The isolates also showed relevant direct and indirect PGP features, including growth on nitrogen-free medium, phosphate solubilization and auxin biosynthesis, as well as resistance to metal and xenobiotic stress. Phylogenomic analysis of BFOA1–BFOA4 isolates indicated that they all belong to Bacillus halotolerans, which could therefore considered as a warden against Fusarium infection in plants. Comparative genomics allowed us to functionally describe the open pan genome of B. halotolerans and LC-HRMS and GCMS analyses, enabling the description of diverse secondary metabolites including pulegone, 2-undecanone, and germacrene D, with important antimicrobial and insecticidal properties. In conclusion, B. halotolerans could be used as an efficient bio-fertilizer and bio-control agent in semi-arid and arid ecosystems.

Bacillus halotolerans strain LYSX1-induced systemic resistance against the root-knot nematode Meloidogyne javanica in tomato

“…Previous studies have demonstrated biocontrol activity of Bacillus spp. against plant-parasitic nematodes (Siddiqui and Mahmood 1999;Engelbrecht et al 2018); however, previously recorded biocontrol activity of B. halotolerans was for fusarium wilts and root rots caused by soil-borne fungi, such as Fusarium oxysporum, Phytophthora capsici, and Rhizoctonia solani (Sagredo-Beltrán et al 2018;Slama et al 2019). Thus, this study is the first to demonstrate suppression of plantparasitic nematodes by a strain of B. halotolerans.…”

“…This study demonstrated that LYSX1 elicits concentration-independent antagonistic activity against M. javanica J2s and egg masses, suggesting extracellular nematicidal substances may be present in the culture supernatant. Indeed, Slama et al (2019) reported that plipastatin A1, Inthomycin-A, cyclo (L-Val-L-Phe), and 5-deoxybutirosamine generated by B. halotolerans BFOA1-BFOA4 had antimicrobial properties. Analysis of the LYSX1 supernatant showed that the nematicidal active ingredients were non-protein, heat and cold resistant, and were highly polar (data no shown), so further studies are required to couple with gas chromatography-mass spectrometry (GC-MS), liquid chromatography-mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR) analysis to identify specific nematicidal active substances.…”

“…B. cereus has been shown to be toxic to second-stage juvenile (J2s) of M. javanica, as a result of the ammonia and nitrite production (Oka et al 1993). Rhizobacteriamediated-induced systemic resistance (ISR) in plants may affect nematode activity (Hasky-Günther et al 1998;Reitz et al 2000;Siddiqui and Shaukat 2002;Niknam and Dhawan 2003;Adam et al 2014), and while B. halotolerans has been shown to manage fungal plant diseases (Sagredo-Beltrán et al 2018;Slama et al 2019), its nematicidal effects remain unclear. Hence, the objectives of this study were to (1) isolate and identify Bacillus spp.…”

Durum Wheat Stress Tolerance Induced by Endophyte Pantoea agglomerans with Genes Contributing to Plant Functions and Secondary Metabolite Arsenal

“…Plant growth-promoting rhizobacteria (PGPR) are attracting considerably more attention owing to their remarkable and beneficial effects on plants [14] and their possible replacement of chemical plant protection, which is highly damaging to the environment [15]. They have proven effective in conferring tolerance against abiotic [16,17] and biotic stresses [18,19,20,21]. Plant benefits include direct plant growth promotion (PGP) activities such as phytohormone production, phosphate solubilization, and nitrogen fixation [22], as well as indirect PGP activities such as hydrogen cyanide (HCN), exoenzyme and 1-aminocyclopropane-1-carboxylate (ACC) deaminase production [23].…”

Plant growth promoting and antifungal activity in endophytic Bacillus strains from pearl millet (Pennisetum glaucum)

“…Emerging research evidences clearly pointed out the significance of microbiota dwelling inside the pearl millet host in offering stress tolerance as well as assistance in enhancing the survival and fitness attributes under unfavorable conditions [3,8]. So far, a wide range of bacterial species from Bacillus, Agrobacterium, Burkholderia, Azospirillum, Enterobacter, Rhizobium, Pseudomonas, and Azotobacter genera have been documented as an excellent growth-promoting endophytes in different types of crops [8][9][10][11][12][13][14][15]. Unfortunately, limited reports are available on the plant growth promoting and antifungal activity in endophytic strains of Bacillus species from pearl millet.…”