Phyto-Beneficial Traits of Rhizosphere Bacteria

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This entry is adapted from the peer-reviewed paper 10.3390/plants11020230

Beneficial interactions between plants and some bacterial species have been long recognized, as they proved to exert various growth-promoting and health-protective activities on economically relevant crops. As well, rhizosphere bacteria direct activity against some phytopathogenic fungal species (such as Aspergillus and Fusarium spp.) have been also observed, resulting highly interesting since these pathogens cause major yield losses in cereal crops and are well-known mycotoxin producers.

antifungal metabolites biocontrol agents plant growth promoting rhizobacteria phytopathogen antagonists siderophores phyto-beneficials

1. Introduction

The rhizosphere is a complex ecosystem in which many relationships are established between bacteria, fungi, and plant root apparatus, and represents the main source of nutrients for plant growth ^[1]. In particular, many soil microbes have established good relationships with plants, supporting their growth and health, for example helping plants to manage both biotic and abiotic stress ^[2]^[3]^[4]. In particular, plant growth promoting rhizobacteria (PGPR) are microorganisms, which form symbiotic interactions with plant roots, promoting plant health and productivity through different mechanisms such as production of plant hormones (auxins, cytokinin, and gibberellins); inhibition of plant senescence; N₂ fixation; phosphate solubilization and mineralization of other nutrients; and siderophores production ^[5]. In addition, being present in the rhizosphere, PGPR may also be endophytic (PGPE) (for example, by colonizing the plant’s tissues), symbiotic (for example, by colonizing the interior of the roots of specific plants by forming nodules), or phyllospheric (i.e., they can be found on the surfaces of plant leaves and stems) ^[6].

The majority of the most known PGPR belong to the genera Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Enterobacter, Klebsiella, Pseudomonas, Rhizobium, and Serratia ^[7]. PGPR beneficial effects on plants include an increase in root growth and shoot biomass, chlorophyll content, nutrient uptake, total protein content, hydraulic activity, abiotic stress tolerance, shoot and root weights, and a delayed senescence. PGPR are, thus, often employed as biofertilizers ^[8].

Besides being determinant for plant health and soil fertility, the interactions between beneficial microbes and plant rhizosphere can also exert direct, positive effects against phytopathies. PGPR can suppress diseases by directly synthesizing pathogen-antagonizing compounds, as well as by triggering plant immune responses ^[9]. Some PGPR have been found to possess several chemotypical traits that make them potential antifungal agents for biocontrol purposes. They can produce siderophores, antimicrobials, lytic enzymes, and various extracellular metabolites which can interfere with, if not completely inhibit, the growth of different, devastating phytopathogenic fungal species with a broad host range ^[10]. For example, Pseudomonas spp. strains isolated from the rhizosphere of alfalfa and clover plants growing on extremely poor pseudogley soil showed interesting antifungal activity against Trichoderma viride, Aspergillus fumigatus, and Aspergillus niger ^[11], while plant-promoting Pseudomonas fluorescens and Bacillus spp. strains from a PGPR collection were found to effectively inhibit three spore-forming genera (Alternaria spp. , Fusarium spp., Bipolaris spp.) ^[12]. Again, Phytophthora capsici, a cucumber pathogen, was successfully suppressed by specific isolates of Pseudomonas stutzeri and B. amyloliquefaciens ^[13]. Recently, a battery of bacteria isolated from the rhizosphere of crops cultivated in different agroecosystems of Pakistan was screened for their biocontrol potential against a range of fungal phytopathogens, showing antagonistic activity against Fusarium oxysporum, F. moniliforme, Rhizoctonia solani, Colletotrichum gloeosporioides, C. falcatum, Aspergillus niger, and A. flavus ^[14]; the antimicrobial effect, which was ascribed to the individuation of antifungal metabolites such as specific antibiotics and cell wall degrading enzymes, was accompanied by the production of a number of compounds recognized as plant growth promoters (hormones and siderophores), suggesting that these PGPR can be exploited for dual-purpose strategies based on the application of a single formulation acting as biopesticide and biofertilizer ^[15]. It is worthy of consideration that specific bacterial siderophores have been demonstrated to possess direct antifungal activity (often affecting spore germination) against phytopathogens such as F. oxysporum, F. udum, A. niger, A. flavus, and Sclerotium rolfsii ^[16] ^[17] ^[18]; pyoverdine and pyocheline in particular, produced by P. aeruginosa and Burkholderia spp., have been attributed the most relevant antifungal activities of these bacterial species.^[19] Interestingly, other molecules produced by some rhizosphere bacteria and also involved in the plant disease resistance show antifungal properties, as it is the case of salicylic acid (SA) and its derivatives. ^[20] ^[21] ^[22] ^[23] ^[24]

2. Evaluation of the Bacterial Strains Phyto-beneficial activities

In this study, a deep characterization of six different bacterial strains isolated from different, harsh environments was performed. As reported in Table 1, the selected strains Pvr_5, Pvr_9, Bioch_2, Bioch_7, NCr-1 and PHA_1 showed some features of PGPR as high in vitro IAA production and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity, as well as the production of siderophores, which was diagnosed by using a qualitative method. ^[25] ^[26] ^[27] ^[28]

Table 1. Characteristics of PGPR bacteria strains isolated from different soil types, rhizosphere, and endosphere samples.

Strains	Homology	Siderophore Production (PSU) ^(a)		IAA Production (mg L⁻¹)	ACC Deaminase Activity ^(b)	Phosphate Solubilization Ability ^(c)	Protease Activity ^(d)	Biofilm Formation (Abs Units)	References
Strains	Homology	SMS	Succinic	IAA Production (mg L⁻¹)	ACC Deaminase Activity ^(b)				References
Pvr_5	Paenarthrobacter ureafaciens (98.16%)	88.64 ± 0.74	91.5 ± 1.05	62.48 ± 6.3	+	-	+	0.037 ± 0.010	[25]
Prv_9	Beijerinckia fluminensis (100%)	91.90 ± 0.11	70.7 ± 2.60	82.08 ± 1.7	+	-	-	1.048 ± 0.141	[25]
Bioch_2	Arthrobacter defluii (98%)	91.29 ± 0.56	85.91 ± 4.70	44.02 ± 2.3	+	-	+	0.1 ± 0.007	[26]
Bioch_7	Arthrobacter nicotinovorans (99%)	92.33 ± 0.70	89.02 ± 1.12	58.65 ± 4.2	+	-	+	0.216 ± 0.032	[26]
NCr-1	Arthrobacter sp. (99%)	93.04 ± 0.08	58.78 ± 2.78	25.6 ± 1.3	+	-	+	0.059 ± 0.003	[27]
PHA_1	Pseudomonas protegens (98%)	90.38 ± 0.09	76.89 ± 4.94	n.d.	n.d.	+	-	0.134 ± 0.007	[28]

^(a) Siderophore production on SMS and succinic media (see Material and Methods for media composition). ^(b) ACC deaminase activity: (-) no bacterial growth on medium containing 1-aminocyclopropane-1-carboxylate as the only N source; (+) bacterial growth on medium containing 1-aminocyclopropane-1-carboxylate as the only N source. ^(c) Phosphate solubilization: (-) absence of solubilization halo; (+) presence of solubilization halo. ^(d) Protease activity. (-) absence of solubilization halo; (+) presence of solubilization halo. Data are average of three independent experiments ± S.D.

UPLC–MS and LC–ESI–MS analyses of culture broths from bacteria resulted in the identification of compounds possibly linked to the plant-promoting and/or fungal-inhibitory activities observed (Table 2).

Table 2. Identified molecules produced by bacteria and their relative functional groups, along with the growth medium and the technique used for the analysis (n.d., not detected).

Isolates	Functional Group	SMS Medium	Succinic Medium
Pvr_5	Carboxylate	Salicylic Acid (UPLC–MS)	n.d.
Pvr_5	Hydroxamate	Desferrioxamine B (UPLC–MS)	n.d.
Pvr_9	Carboxylate	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)
Pvr_9	Catecholate	n.d.	Aminochelin (LC–ESI–MS/MS)
PHA_1	Carboxylate	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)
NCr-1	Carboxylate	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)	Salicylic Acid (UPLC–MS; LC–ESI–MS/MS)
NCr-1	Hydroxamate	n.d.	Asperchrome B (UPLC–MS)
Bioch_2	Carboxylate	Quinolobactin (UPLC–MS)	n.d.
Bioch_7	Carboxylate	Salicylic Acid (UPLC–MS)	n.d.

Among the tested strains, Pvr_9 was considered the most interesting, due to the important effects shown as both plant growth promoter and biocontrol agent against some phytopathogenic fungi. The molecular characterization previously conducted showed a homology with the bacterial species Beijerinckia fluminensis ^[27], belonging to a genus that is still poorly characterized for its putative PGPR properties. On the contrary, strain PHA_1, which shows a significant increase in Arabidopsis secondary root formation and interesting features as a biocontrol agent against phytopathogenic fungi tested, belong to the well-known Pseudomonas genus, which group includes various interesting species that show microbial biocontrol features and PGP traits, and that has proven to be very versatile, with great potential from an agronomic point of view. Many works described P. protegens as an effective antimicrobial agent. Cesa-Luna and collaborators ^[29] evaluated the ability of P. protegens strain EMM-1 against different fungal species, reporting significant activity against Aspergillus spp. and Fusarium spp. P. protegens strain AS15 was shown to be an effective biocontrol agent against A. flavus, whose growth and aflatoxin production were lowered on rice grains after the bacterial co-inoculation ^[30]. The powerful antifungal activity of this species was confirmed by our results; in fact, PHA_1 proved to be highly inhibitory on the fungal growth, especially when the conidia were forced to germinate in the presence of the bacterial cells in co-inoculation assays; in fact, the inhibition reached 100%, independent of the bacterial cell concentration.
Here, the evaluation of the association of PHA_1 with A. thaliana showed a significant increase in the number of secondary roots per cm of primary root, in accordance with what has been recently observed on maize roots inoculated with Pseudomonas PS01 strain ^[31].

Strains Bioch_2, Bioch_7, and NCr-1 belong to the Arthrobacter genus and Pvr_5 to the Paenarthrobacter genus, in which many plant endophytes are grouped. The plant growth promoting traits of the genus Arthrobacter is well documented ^[32] ^[33] ^[34]; all the bacteria tested were siderophore producers and, with the exclusion of Pvr_5, all the strains were more or less able to interfere with the mycelium growth of Fusarium. As previously reported, siderophores can mitigate the toxic effect of fusaric acid produced by the genus Fusarium on Pseudomonas protegens Pf-5 ^[35]. In addition, all the bacterial strains selected showed high siderophore activity. There is increasing interest on siderophore-producing bacteria and siderophore molecules, not only for their possible role in iron bioavailability for plant nutrition, but also to their suppressive activity against fungal phytopathogens. ^[36] ^[37] ^[38] ^[39]
For this purpose, as an objective of this study, the identification of the siderophores produced by bacterial strains could help to better investigate possible molecules involved not only in plant nutrition, but also in bacterial antimicrobial activity against the phytopathogenic fungi tested. Among the molecules with hydroxamate functional group, asperchrome B and desferrioxamine B are well-known siderophores, which are produced by various species of bacteria and fungi. As well, among the molecules with catecholate functional groups, we fond Pvr_9 to produce aminochelin, whose biological properties have been described ^[40]. The carboxylate-containing salicylic acid (SA) was found to be produced by most of the bacterial strains tested: interestingly, in addition to its use - by bacteria- to maintain iron-limiting growth conditions, SA production was reported to also exert an inhibitory potential against several postharvest pathogens. ^[20] ^[21] ^[22] ^[23] ^[24]

3. Conclusions

Amongst the bacterial strains evaluated, Pvr_9 was found to possess the best characteristics for both promoting the plant growth and acting as biocontrol agent against phytopathogens. The results of this study provide important clues about the direct antagonistic effect of these strains on Aspergillus and Fusarium species relevant to crops. Future investigations devoted to deepening and clarifying the mechanism ruling the positive effects on the growth of plants—and in particular of economically important crops—are needed before any possible application in agricultural systems can be proposed. In particular, more research is desirable to elucidate the direct antimicrobial potential of the siderophores identified, which would support the possible use of such bacteria as biocompetitors able to act against phytopathogenic fungal species in different synergistic ways.

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1. Introduction

2. Evaluation of the Bacterial Strains Phyto-beneficial activities

3. Conclusions

References