Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends
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Phosphate (P)-solubilizing microorganisms as a group form an important part of the microorganisms, which benefit plant growth and development. Growth promotion and increased uptake of phosphate are not the only mechanisms by which these microorganisms exert a positive effect on plants. Microbially mediated solubilization of insoluble phosphates through release of organic acids is often combined with production of other metabolites, which take part in biological control against soilborne phytopathogens. In vitro studies show the potential of P-solubilizing microorganisms for the simultaneous synthesis and release of pathogen-suppressing metabolites, mainly siderophores, phytohormones, and lytic enzymes. Further trends in this field are discussed, suggesting a number of biotechnological approaches through physiological and biochemical studies using various microorganisms.
The two main methods for disease control currently available in crop production include repeated applications of chemicals and the use of resistant or tolerant cultivars. However, both approaches have limitations. The overuse of chemicals to combat plant diseases has led to environmental degradation and pollution. Furthermore, such chemicals are lethal to useful soil arthropods and to key microorganisms in the rhizosphere. These products may also enter the food chain, thus presenting potential harm for human beings. On the other hand, the use of cultivars resistant to plant diseases is limited, especially in fruit and vegetable crops (Belanger and Benyagoub 1997). In some cases, genetically engineered crop resistance, although seen as a foremost possibility, is often readily overcome by the target phytopathogen population (Rausher 2001; Stuvier and Custers 2001). Therefore, to continue agricultural growth and to feed the growing human population in a healthy environment, complementary and/or new alternatives to the present dominance of chemical applications need to be developed (Gerhardson 2002). One attractive possibility to suppress soilborne plant pathogens is to use the activity of microorganisms. In the rhizosphere of the plant root system, or in its close vicinity, microorganisms abound. Among them, plant-growth-promoting microorganisms (PGPM) are the best studied (Vessey 2003). It is now firmly established that bacterial and fungal inoculants can directly and indirectly benefit plant growth (Rodriguez and Fraga 1999). The direct promotion of growth is achieved by phytohormone synthesis and biological nitrogen fixation, making nutrients more available and reducing the membrane potential of the roots, etc. The indirect beneficial effect of PGPM is related mainly to their antagonistic properties toward phytopathogens.
The solubilization of insoluble phosphates in the rhizosphere is the most common mode of action involved in PGPM that enhance nutrient availability to plants (Rodriguez and Fraga 1999; Richardson 2001). Some properties of the phosphate (P)-solubilizing microorganisms of interest in the field of biogeochemistry and particularly in the maintenance of soil health and quality were described (Jeffries et al. 2003).
It is now well established that in many cases, a single PGPM species has several modes of action. However, the purpose of this minireview is to provide a critical analysis of the information on the potential for biological control against soilborne phytopathogens, particularly of P-solubilizing microorganisms.
Microbially mediated solubilization of insoluble phosphates
Although phosphate is quite abundant in many soils, frequent applications of phosphate fertilizers is needed to compensate for the rapid process of soluble phosphate complexation by soil constituents (Goldstein 1986) and phosphate runoff from P-loaded soil (Del Campillo et al. 1999). In general, phosphate for agricultural applications is available in two forms: as conventional phosphate fertilizers and rock phosphate. Most phosphate fertilizers are produced by technologies based on the chemical processing of insoluble, inorganic, high-grade rock phosphate ore (RPO). This process is environmentally undesirable, not least because of the release of contaminants into the main product, gas streams, and by-products. A biological approach for extracting phosphate from RPO was proposed as a less expensive and lower-energy technique compared with the conventional processes (Rogers and Wolfram 1993; Goldstein and Rogers 1999). Alternatively, direct application of RPO in soils would minimize pollution and decrease the costs of chemical treatment (Iyamuremye and Dick 1996). This approach is not always effective without previous treatment as, depending on soil and climatic conditions, it could take up to 4 years of annual application before RPO becomes as easily available as superphosphate (Sinclair and Dyson 1988). To improve the agricultural value of RPO, several methods were commonly proposed (Rajan and Watkinson 1993; Chien et al. 1987; Kpomblekou et al. 1991) including microbially based approaches. Microorganisms involved in the solubilization of RPO normally produce organic acids which, through their hydroxyl and carboxyl groups, chelate the cations bound to phosphate, thus releasing soluble phosphate (Kpomblekou and Tabatabai 1994). A large number of studies on phosphate solubilization were carried out employing various microorganisms in fermentation and soil conditions (Kucey et al. 1989; Rodriguez and Fraga 1999; Goldstein 2000; Whitelaw 2000; Vassilev et al. 2001). Immobilized cell technology was demonstrated to offer advantages over the application of freely suspended cells (Vassilev et al. 1996, 1997a–c; Vassileva et al. 1998, 2000). The direct introduction of RPO-solubilizing microorganisms normally confirms the microbial activity demonstrated in fermentation studies. Short-term reduction of the rhizosphere pH due to organic acid production and further complexation of cations result in the release of soluble phosphate, which in turn increases its accessibility to the plant. P-solubilizing microorganisms such as Pseudomonas, Bacillus, Rhizobium, Burkholderia, Enterobacter, Achromobacter, Agrobacterium, Microccocus, Aerobacter, Erwinia, Aspergillus, Penicillium, and some yeasts are common in rhizosphere (Rodriguez and Fraga 1999), although Aspergillus, Penicillium, Bacillus, Pseudomonas, and Enterobacter are the ones often studied (Whitelaw 2000; Vassilev and Vassileva 2003).
The phosphate uptake by plants and subsequent growth promotion in plant–soil systems inoculated with P-solubilizing microorganisms are more pronounced when coinoculated with arbuscular mycorrhizal (AM) fungi, which form beneficial symbioses with the plant roots (Smith and Read 1997). Nutrients taken up by the mycorrhizal fungi lead to improved plant growth and health. AM fungi are also capable of sparingly mobilizing soluble inorganic phosphate by the excretion of H+ after the utilization of the ammonium ion by the hyphae (Yao et al. 2001).
There were a number of studies on plant growth promotion by various microorganisms that can solubilize P-bearing materials in soil. However, some of these reports have mentioned the production of other metabolites beneficial to plants, such as phytohormones, antibiotics, or siderophores (e.g., Kloepper et al. 1989), which are accepted to have biocontrol activity.
Biocontrol properties of P-solubilizing microorganisms
Biochemical mechanisms and metabolites in P-solubilizing microorganisms related to their biocontrol activity
Indole-3-acetic acid (IAA) and siderophores, which are among the most frequently studied metabolites with biocontrol functions, are found to be released by microorganisms that express P-solubilizing activity.
Siderophores are low-molecular-weight, iron-chelating ligands synthesized by microorganisms (Winkelmann 1991). Most bacteria and fungi produce siderophores that differ according to their functional groups. Siderophore production helps a particular microorganism compete effectively against other organisms for available iron. This enhances the growth of the microorganism while limiting iron availability to the competing microorganisms restricts their growth. It is accepted that this mechanism suppresses pathogenic microorganisms (Lemanceau et al. 1985). It was also shown that siderophores are beneficial to plants by solubilizing iron formerly unavailable to the plant (Prabhu et al. 1996).
Similarly, auxins are thought to play a role in host–parasite interactions and particularly the plant-growth regulator IAA is involved in the interaction between a plant pathogen and its host (Hamill 1993). Various authors have proposed mechanisms of biocontrol action of IAA, which resulted in two main hypotheses: (1) a potential involvement of IAA together with glutathione S-transferases in defense-related plant reactions (Hahn and Strittmatter 1994; Droog 1997) and (2) an inhibition of spore germination and mycelium growth of different pathogenic fungi (Brown and Hamilton 1993). Martinez Noel et al. (2001) showed that the IAA supply to excised potato leaves reduced the severity of the disease provoked by Phytophthora infestans.
Increased phenolic metabolism in plant roots was suggested to be part of the mechanism involved in AM-infected plants. AM fungi can cause an accumulation of phytoalexins, flavonoids, and isoflavonoids in the roots of the host plant and thereby, in combination with the lignification of endodermis, and enhance the resistance of mycorrhizal plants to pathogen attacks (Morandi 1996). In addition, poorer pathogen performance may be due to competition between pathogens and AM fungi for plant metabolites or infection sites (Traquair 1995). Although fungal pathogens reduce root colonization by AM fungi, the latter were shown to provide protection through increased hydrolytic enzyme activity, including that directly involved in the regulation of the symbioses (Lambais and Mehdy 1995; Pozo et al. 1998).
P-solubilizing and biocontrol activity in bacteria
P-solubilizing bacteria with biocontrol activity
Metabolite with biocontrol activity
Cattelan et al. 1999
Bano and Musarrat 2004
Dey et al. 2004
Bacillus sp. MR11
Pal et al. 2001
De Freitas et al. 1997
Vassilev et al. 2006b
Cattelan et al. (1999) reported that five of 22 soil bacterial isolates proved positive for solubilization of inorganic phosphates and also inhibited the growth of Sclerotium rolfsii and Sclerotinia sclerotiorum. Fungal-growth inhibition was assessed by measuring the mycelial radial growth in plate assays on media that was either amended or unamended with 0.1 mM FeCl2. Of these five isolates, two significantly affected the soybean growth in a P-deficient soil amended with insoluble phosphate.
A bacterial strain NJ-101 isolated from agricultural soil was characterized and identified as Pseudomonas sp. and further proved to release 74.6 mg/ml soluble phosphate from inorganic phosphate source (Bano and Musarrat 2004). Phosphate solubilization was due to acid production and a pH shift from pH 7.0 to 3.8. In addition, the bacterial culture to produced 11.4 μg/ml IAA after 10 days of cultivation on a mineral-salt medium was supplemented with 0.5% glucose and tryptophan. Significant production of siderophores on chrome azurol S (CAS) agar plates resulted in the formation of 1.2–1.8 mm zones of inhibition when the bacterial culture was grown in the presence of various Fusarium pathogens. As the same culture exhibited efficient carbofuran (a wide spectrum carbamate insecticide), the authors underlined the multifunctional properties of the P-solubilizing Pseudomonas sp., which include potential for concurrent biocontrol, plant-growth promotion, and pesticide bioremediation. In previous reports on pesticide degraders, the same authors revealed the innate capability of simultaneous expression of ancillary traits along with the pesticide potential (Bano and Musarrat 2003a,b). Rhizobium, Pseudomonas, and Proteus species were found to exhibit substantial solubilization of tricalcium phosphate and IAA and siderophore production.
Recently, Dey et al. (2004), investigating nine soil isolates, found that eight produced siderophores while five produced IAA, ammonia, and solubilized inorganic phosphate and inhibited soilborne fungal pathogens such as Sclerotium rolfsii. The performance of these rhizobacterial isolates was repeatedly evaluated for 3 years in pot and field trials. After bacterial inoculation, the content of phosphate in soil, shoot, and kernels significantly rose all in 3 years, in both rainy and postrain seasons. Three Pseudomonas fluorescens isolates demonstrated multiple properties and consistently enhanced growth yield and phosphate uptake of peanut under potted and field conditions, decreasing the incidence of pathogens. Earlier studies by the same research group demonstrated that fluorescent Pseudomonas sp. EM85 and Bacillus sp. MR-11 (2) produced 0.108 and 0.092 mg catechol type of siderophores/mg protein and 3.84 and 3.71 μg IAA/ml, respectively (Pal et al. 2001). Pseudomonas sp. EM85 solubilized tricalcium phosphate (14.13 mg/100 ml) by the production of gluconic, citric, succinic, and α-ketobutyric acid whereas, in the culture broth of Bacillus sp. MR-11 (2), gluconic, citric, tartaric, and α-ketobutyric acids were found and the amount of soluble phosphate reached 25.7 mg/100 ml.
It was speculated that the phytohormone production by P-solubilizing microorganisms may contribute to their stimulatory effect on plant growth (Azcon et al. 1978; Sattar and Gaur 1987). Later studies have identified the exact indole substances that show auxin activity and quantified their amount produced in liquid media with tryptophan by P-solubilizing Pseudomonas, Bacillus, and Acinetobacter under different environmental parameters (Lehinos and Vacek 1994; Lehinos 1994). De Freitas et al. (1997) isolated several P-solubilizing rhizobacteria that also produced IAA-like hormones as determined by in vitro assays. Experiments performed with P-deficient soil showed the plant-growth-stimulating effect of the P-solubilizing bacteria, although in no case was plant growth significantly enhanced in soil amended with rock phosphate.
Recently, we have demonstrated for the first time the capacity of living cells of the biocontrol bacterium Bacillus thuringiensis, entrapped in k-carrageenan, to solubilize insoluble inorganic phosphate and simultaneously produce IAA in a repeated-batch fermentation process (Vassilev et al. 2006b). After five batch-fermentation cycles, an average concentration of 6.9 mg IAA/l was obtained in the presence of 1.5 g rock phosphate/l compared to 4.7 mg IAA/l in the control experiment without rock phosphate. The latter was solubilized with a maximum of soluble phosphate of 115 mg/l after the fourth batch cycle. The addition of tryptophan raised the production of auxin to 20.7 mg/l per batch but bacterial growth and rock phosphate solubilization were lower. Introduced into a soil–plant system, the same bacterial formulation was found to boost plant growth and P-uptake and stimulate the establishment and development of the endomycorrhizal fungus Glomus deserticola coinoculated into the soil–plant system (Vassilev and Vassileva 2004). A similar inoculation scheme containing both B. thuringiensis and AM represents an attractive, less environmentally damaging alternative to chemical methods for phosphate fertilization and pathogen control. On the other hand, encapsulation methods can improve the properties of P-solubilizing/biological control microorganisms, such as easy handling and application, protection of the microbial cells from abiotic and biotic stress factors, and greater efficacy in the soil.
P-solubilizing and biocontrol activity in fungi
P-solubilizing fungi with biocontrol activity
Metabolite with biocontrol activity
Trichoderma harzianum T22
Altomare et al. 1999
Vassilev et al. 2005b
Petruccioli et al. 1999
Arbuscular mycorrhizal fungi
Vassilev et al., unpublished results
Butler et al. 2005
A similar biocontrol effect of P-solubilizing filamentous fungi against Fusarium wilt in tomato (Fusarium oxisporum f. sp. lycopersici; Fol) was shown by Khan and Khan (2001, 2002). Root-dip applications of Bacillus subtilis, P. fluorescens, Aspergillus awamori, Aspergillus niger, and Penicillium digitatum resulted in a significant decline in the rhizosphere population of Fol. Tomato yield was enhanced, being greatest with A. awamori and P. digitatum. Direct soil-plant inoculation with A. niger, A. awamori, and P. digitatum decreased the rhizosphere Fol population by 23–49% while the tomato yield increased by 28–53% in field experiments. The authors propose that organic acids produced by these microorganisms may inhibit fungal infection but other metabolites such as bulbiformin and phenazin could also be involved, particularly in the treatments with B. subtilis and P. fluorescens as reported in earlier studies (Dalla 1986).
More recently, Vassilev et al. (2005a) reported an efficient biotechnological scheme for preparing a material with biocontrol and plant-growth-promoting functions. Sugar beet wastes were mineralized by an acid-producing strain of A. niger with a simultaneous solubilization of rock phosphate under conditions of solid-state fermentation. The product of this process, used as soil amendment, resulted in 347 and 467% higher (vs unamended control) plant biomass in plant–soil experiments contaminated or not with Fol, respectively. Disease severity and number of Fol colony-forming units reached the lowest levels, particularly when plants were mycorrhized with G. deserticola. In vitro studies demonstrated the biocontrol activity of A. niger, which was partly attributed to siderophore production on modified CAS medium.
The potential biocontrol properties of Penicillium variabile P16 deserves mention, this microorganism being reported to solubilize inorganic phosphates when encapsulated in polysaccharide gels (Fenice et al. 2000). Recent work with P. variabile P16 demonstrated increased glucose oxidase (GOD) production in the presence of polysaccharides of plant origin, which were found to serve as activators of defensive systems in this filamentous fungus (Petruccioli et al. 1999). In fact, GOD activity can play a significant role in antibiosis in the soil environment: The hydrogen peroxide enzymatically produced is cytotoxic for microorganisms (Fravel and Roberts 1991).
In studies on the biological control by soil microorganisms that participate in phosphate solubilization and plant-growth promotion, mycorrhizal fungi merit special attention. AM fungi are accepted as an important part of biocontrol microorganisms (Johansson et al. 2004) as they strengthen resistance to certain wilt and root-rot pathogens (Filion et al. 1999; Dar et al. 1997) by enhancing the nutritional status of the host plant and/or releasing unspecified substances. For this reason, AM are currently being studied actively as biological-control microorganisms against soilborne diseases. The importance of such studies is augmented by the fact that under natural conditions, nearly 90% of all plant species are estimated to form this type of symbiotic fungal infection (Smith and Read 1997). Greenhouse and growth-chamber experiments have demonstrated repeatedly that these root symbionts can benefit by host nutrition, primarily by facilitating phosphate uptake in plants. In all relevant literature, the improved phosphate uptake by the mycorrhizal plants is emphasized. The main contribution of AM to the host is to reach and translocate phosphate through their extracortical hyphae, which can penetrate as much as 9 cm into the soil (Sylvia 1998). In addition, a number of studies have demonstrated the ability of AM to solubilize otherwise insoluble phosphate sources (Norlaeny et al. 1996; Yao et al. 2001; Strack et al. 2003). The effects of AM on pathogens are most likely to be indirect and include improved nutrition or altered physiology of the host. Many details are known about the physiological and biochemical changes in plants due to symbiosis (Smith and Gianinazzi-Pearson 1988; Smith et al. 1985). Changes in the balance of phytohormones may determine AM effects on plant growth and health due to their regulatory functions (Dugassa et al. 1996).
Each microorganism able to release organic acids (or at least to provoke lower environmental pH) can be a potential P-solubilizer. On the other hand, organic acids are accepted to have biocontrol properties through their siderophore-like functions. It is well established that some microorganisms release organic acids in response to iron stress. This phenomenon was well documented in Neurospora crassa (Winkelmann 1979) and Bradyrhizobium japonicum (Guerinot et al. 1990). More recently, Machuca et al. (2001) demonstrated that fungi such as Trametes versicolor and Wolfiporia cocos produce hydroxamate derivates and oxalic acid. W. cocos was positive in the CAS assay and it was found to produce siderophores in liquid medium with a simultaneous pH drop to 2.5 due to a high concentration of oxalic acid accumulated in the culture broth. Siderophore production by various fungi was shown on modified CAS agar-plate assays (Milagres et al. 1999). Bearing in mind that some of these fungi solubilize rock phosphate, presumably by releasing metal-chelating metabolites (Vassilev et al. 2006a), we can expect their application as biocontrol microorganisms with simultaneous P-solubilizing activity. In our laboratory, this expectation was confirmed by the suppressive effect of Phanerochaete chrysosporium and Panus tigrinus on Fusarium oxysporum (Vassilev et al., unpublished results). P-solubilizing filamentous fungi are also well-known producers of lytic enzymes. Cell-wall-degrading enzymes, such as β-1,3-glucanases, cellulases, proteases, and chitinases are known to be involved in the activity of some microorganisms against phytopathogenic fungi (Ordentlich et al. 1988; Shapira et al. 1989; Harman et al. 1993; Chernin et al. 1995; Dunn et al. 1997). Particularly, microbial chitinases have attracted attention as potential enzymes to control phytopathogenic fungi and insect pests (Stleger et al. 1986; Roco and Perez 2001). On the other hand, some active microbial producers of chitinase are well-established P-solubilizers (Krishnaraj and Goldstein 2001). The production of lytic enzymes can be stimulated by the presence of organic substances rich in ligno-cellulose used in solid-state fermentations. In this line of studies, melanin-destructive fungi are to be investigated in the near future. Fungal microorganisms, such as A. niger and Ph. chrysosporium, were shown to degrade intact fungal melanin present in phytopathogens (Butler et al. 2005). White-rot fungi, which release manganese peroxidase and filamentous fungi (belonging to Penicillium and Aspergillus), which release GOD, are involved in melanin degradation and their biocontrol activity deserves to be studied. As shown in this review, these fungal microorganisms are strong P-solubilizers.
Investigation into the biocontrol functions of agro-industrial wastes treated microbially in conditions of solid-state fermentation including composting (which, in fact, is part of this technology) will probably be carried out in the near future. Various aspects of disease suppressiveness of microbially treated agro-industrial wastes were well documented but their effect can be guaranteed when the final product is colonized by specific biocontrol microorganisms (Hoitink et al. 2001; Postma et al. 2003). Moreover, the introduction of such specific microorganisms was recommended to boost disease suppressiveness (Segall 1995). Disease suppression is attributed to the general microbial activity of the compost microflora. However, additional inoculation with other beneficial microorganisms including P-solubilizing microbial cultures was performed successfully (Zayed and Abdel-Motaal 2005). Further studies are needed to demonstrate the biocontrol activity of similar organic-matter-based materials inoculated with P-solubilizing microorganisms and their capability of producing hydrolytic enzymes. It was recently reported that soil filamentous fungi (Aspergillus and Penicillium) are capable of producing chitinases in solid-state fermentation conditions using moldy bran (Patidar et al. 2005) or corncob/shrimp shellfish wastes (Rattanakit et al. 2002) as substrates. Therefore, it is only a question of time before we see the testing and production of agro-industrial wastes treated in solid-state conditions and composts of desired quality with both P-solubilizing and biocontrol functions.
Another field of future research concerns the biocontrol function of AM fungi. Research with AM fungi in P-deficient soil–plant systems enriched with rock phosphate will clarify their effect on soilborne pathogens through simultaneous P-solubilizing and biocontrol activity. Studies should be carried out to assess the relationship between the microelement uptake of mycorrhizal plants and the resistance to pathogens in soil amended with rock phosphate. The presence of various metals in the rock phosphate, particularly Cu and Zn, reportedly benefits plant health (Duffy and Defago 1999). On the other hand, Gildon and Tinker (1983) supported the view that AM contribute to the higher accumulation of microelements in mycorrhizal plants. Studies including dual inoculation with AM fungi and other P-solubilizing microorganisms (Vassilev et al. 2005b) can be expected as the combinations of two such partners with complementary mechanisms might increase overall biocontrol and plant-growth-promoting efficacy, thus providing an environmentally safe alternative to chemicals.
It is evident that biological methods demonstrate a number of economic and environmental advantages over chemical-based control applications. On the other hand, the exact biocontrol mechanisms are largely unknown in many microorganisms. As was recently reported, many plant-growth promoters used for inoculation in cropping systems might serve as biocontrol microorganisms (Gerhardson 2002). Therefore, within the complex action modes of diverse plant-benefiting microorganisms, P-solubilizing microorganisms with their multifunctional properties will attract more attention in the field of biological control. We sincerely hope that the suggestions expressed in this review paper will result in new applications of these types of microorganisms.
This work is supported by Project MEC CTM2005-06955 and R&C Programme.
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