Antibiotic Compounds Present in Suppressive Soils against Fungal and Oomycetes Plant Pathogens: A Mini-Review
María Belén Colavolpe*
Instituto Nacional de Investigação Agrária e Veterinária, I. P. Oeiras, Portugal
Received Date: 17/11/2020; Published Date: 25/11/2020
*Corresponding author: María Belén Colavolpe, Instituto Nacional de Investigação Agrária e Veterinária, I. P. Oeiras, Portugal
Cite this article: María Belén Colavolpe, Antibiotic Compounds Present in Suppressive Soils against Fungal and Oomycetes Plant Pathogens: A Mini-Review. Op Acc J Bio Sci & Res 5(1)-2020
Background: The plants are part of a complex environment that includes microorganisms in the soil and covers different ecological interactions. Filamentous plant pathogens can attack plants to explore host tissues to obtain nutrients for growth and reproduction. The soil chemical and physical attributes within its complex microbial communities and the production of its bioactive compounds currently represent a promising perspective for searching novel functions of biotechnological interest. Certain bacteria of the microbiota can protect plants against pathogens using different mechanisms. The protective effect can be directly due to antibiotic compounds production or indirect by promoting plant defense as induced systemic resistance. This mini-review describes some aspects of the direct effect. The production of antibiotic compounds to maintain suppressive soil is needed as an action related to antagonist bacteria, mainly of the genus Bacillus, Burkholderia, and Pseudomonas.
Keywords: Antagonist Bacteria; Plant Disease; Volatile Compounds and Antibiotic Peptides.
The plants are part of a rich ecosystem in the soil , where bacteria generally colonize the plant rhizosphere and, sometimes, the endosphere. Some beneficial effects for plants may include assistance in getting nutrients and promoting plant growth by modulating growth-related hormones . Other benefits include the reduction of damage caused by phytopathogen . Filamentous plant pathogens can severely attack plants, and in agriculture, this could lead to high economic annual losses . The suppressive soils support soil microorganisms as the first defense against soilborne pathogens. General suppressive soils have a high total microbial biomass, resulting in low protection against multiple pathogens. This strategy is dependent on the quality and quantity of soil organic matter and cover crops that enhance populations of beneficial microbes intended to antagonize associated crop pathogens primarily by occupying plant infection sites . However, specific suppressive soils have a high concentration of specific microbial species and result in high protection against specific pathogens .
Cultural practices in agriculture have a strong influence on soil health through physicochemical characteristics and soil microbial communities. Beneficial cultural practices are used to improve soil health and can, in some cases, increase soil disease suppression . According to Schlatter et al. , the relationship between soil properties and soil suppressiveness has not been deeply studied. Many different abiotic or biotic soil characteristics have been used to describe suppressiveness, but there is a lack of reliable descriptors.
The plant protection of certain bacteria against pathogens includes a wide range of mechanisms: antibiosis, competition for colonization sites, nutrients and minerals, parasitism, and cell lysis . The protection can be caused by direct action due to antibiotic compounds or indirectly by promoting plant defense as induced systemic resistance . The biological activity is also related to secondary metabolites production, low molecular mass products not essential for bacteria survival produced by secondary metabolism during the late growth phase (idiophase) . These compounds are generally involved in the antibiosis or perform synergism with other inhibitors .
This mini-review focuses on some conditions needed to maintain a suppressive soil and the antibiotic compounds produced by the most studied bacteria groups. Because of these molecules' wide diversity, the classification is complex, and several criteria could be taken . In this overview, the work description considers the bioactive metabolites as volatile compounds and non-ribosomal peptides in an integrated and general way
Physicochemical Characteristics and Antimicrobial Compounds from the Most Studied Bacteria Groups of Suppressive Soils
The suppressive effect could be more likely related to a combination of biotic and abiotic parameters in soils . Chemical and physical attributes of soil, including pH, organic matter, and clay content, can impact soil microbial activity . The degree of suppressiveness is related to physical soil conditions, fertility level, biodiversity, water supply, and populations of soil organisms and soil management . Soil texture and structure affect holding capacity, nutrient status, gas exchange, and root growth related to the percentage of sand, silt, and clay particles in the soil . A significant negative correlation between the sand content of soil and its suppressiveness to Fusarium wilts of flax and Armillaria root disease on lodgepole pine was found . Poor soil aeration was associated with cavity spot (Pythium spp.) disease in carrot. The pea root rot complex (Fusarium spp.) is also affected by soil compaction .
Soil organisms are concentrated in the top 10 cm of soil; the minimum tillage use maintains the biota near the surface instead of diluting them through a greater depth . Rotations that include a break crop significantly reduce root disease in cereals, for example . Stubble retention has an essential effect on the level of organic material (carbon). Carbon-based material represents an energy source for soil biota, helps in fast multiplication of the soil population, and reduces moisture evaporation that also benefits some antagonist organisms . The general suppression in soils is not related to a specific group of microorganisms; many factors and populations cooperate to inhibit the pathogen or the disease's development. The disease suppression might be related to soil microorganisms specific functions; many authors have found consistent correlations among specific functional parameters and disease suppression. One of the best examples is the production of antibiotic compounds .
Bacteria from the plant environment can produce different molecules with antagonist activity against fungal and oomycetes plant pathogens. Many of these beneficial microorganisms can be selected with a relatively high effectivity and multiplied on artificial media  to study its compounds. However, in vitro cultures' main disadvantage is that metabolites' production depends on medium nutrient concentration and composition, generally higher in culture media than in natural habitats, conditions that could not correctly predict the real antagonism effect [19,20]. Nonetheless, there has been an increasing interest in discovering the metabolites of biocontrol agents for plant disease control. According to Colavolpe et al. (b) , the use of active compounds can overcome the challenge associated with the use of living microorganisms for the biocontrol purpose.
Bacteria from the Bacillus genus inhabit many different habitats  and offer many compounds displaying a broad range of antagonist functions . This enormous versatility increases the industrial and environmental interest, especially in B. subtilis strains . The volatile compounds include benzene compounds, pentadecane, tetradecane, and some ketones, which are of particular interest due to their long-distance action [25,26]. Volatile fatty acids and their derivatives are the most important produced by microbes, and in the case of B. subtilis, represent up to 87% of known antimicrobial produced by the bacteria .
According to Méndez-Bravo et al. , a bacteria isolate (A8a) closely related to B. acidiceler can inhibit the oomycete Phytophthora cinnamomi growth in vitro by 76% through the production of volatile compounds identified as 6,10-dimethyl-5,9-undecadien-2-one, 2,3,5-trimethylpyrazine, and 3-amino-1,3-oxazolidin-2- one. The total ion chromatogram of isolate A8a displayed components identified to belong to the chemical categories of ketones, aldehydes, alkyls, sulfoxides, pyrazines, and alcohols . The strain G341 of B. velezensis produced antifungal volatiles and inhibited the mycelial growth of S. sclerotiorum, R. solani, and B. cinerea. Volatile profiles indicated that strain G341 produces three volatile compounds: dimethylsulfoxide, 1-butanol, and 3-hydroxy2-butanone (acetoin) .
Some of the more diverse plant-associated bacteria are β-proteobacteria belonging to the genus Burkholderia . The volatile profile of B. tropica strain MTo431 was studied by Tenorio-Salgado et al. , and different compounds were identified, including sulfur metabolites, dimethyldisulfide, toluene, and terpenoid compounds, such as α-pinene, limonene, and ocimene. Several of these volatile compounds have been previously detected in cultures of many strains of Pseudomonas spp and Burkholderia cepacia . Many soil-derived Pseudomonas strains are potentially useful biocontrol agents of oomycetes. These include P. putida, P. fluorescens, Pseudomonas sp. SH-C52 and P. chlororaphis . Dimethyl disulfide and other sulfur-containing compounds emitted by Pseudomonas species were recently shown to stop the growth of Phytophthora infestans. Other volatile compounds, such as 1-Undecene , can also reduce sporangia formation and zoospores' release in P. infestans. The volatile compound 2-phenyl ethanol inhibited the mycelial growth of Penicillium digitatum, P. italicum, and B. cinerea. Additionally, the 2,3,5-trimethylpyrazine compound has been identified as an abundant component in several volatile profiles from fungistatic soils against Rhizoctonia and Fusarium phytopathogens .
Important bioactive molecules from the genus Bacillus are non-ribosomally synthesized peptides , metabolites with very complex biosynthesis mechanisms catalyzed by non-ribosomal peptide synthetases, large enzyme modular structure complexes, each module being in charge of incorporating particular amino acid . B. subtilis and B. amyloliquefaciens can produce different lipopeptides in which antifungal activity varies according to the targeted phytopathogen . The representative lipopeptides can be classified into three families based on their amino acid configuration: surfactin, iturins (mycosubtilin, iturin A, and bacillomycin), and fengycin. Both iturins and fengycin have antifungal activities ; meanwhile, the surfactin family has antiviral activity. Some antifungal activity presents synergistic actions when applied in combination with iturin A or fengycin . B. amyloliquefaciens synthesizes iturin and fengycin and can inhibit the growth of Alternaria panax, Botrytis cinerea, Colletotrichum orbiculare, Penicillium digitatum, Fusarium oxysporum, F. solani, Verticillium dahlia, Phytophthora parasitica , Ralstonia solanacearum, and Rhizoctonia solani . Most important molecules from this group, circular lipopeptides from surfactin, iturin, and fengycin families (Asari et al., 2017), affect the target cells of the pathogens on the membrane level .
Another antibiotic lipopeptide, called viscosinamide, is produced by Pseudomonas fluorescens. It has been shown to increase membrane permeability in plant cells facilitating pectolytic attack and has been further reported to act as a biosurfactant. Pythium ultimum and R. solani resulted in inhibited by specific Pseudomonas in vitro antagonism . Antibiotics isolated from strains of P. cepacia include cepacin A, cepacin B, altericidins, 2-[2-heptenyl]-3- methyl-4-quinolinol, pyrrolnitrin [3-chloro-4- (2'-nitro-3'- chlorophenyl)-pyrrole], and 2-[2- nonenyl)-3-methyl-4- quinolinol .
The analysis of fungal pathogens co-cultivated with antagonistic bacteria producing the mentioned compounds shows changes in hyphal morphology, including hyphal swelling, distortion, large amounts of balloon-shaped cells, and cytoplasm protoplasm aggregation. Degradation of fungal cell walls, cell breakage, leakage of intracellular substances, alterations in hyphal morphology, lysis of fungal hyphae, vacuolization, granulation in mycelium structures, and ruptured of mycelia were also detected changes . These effects on pathogen cells result from direct defense due to the production of antibiotic compounds by bacteria. This potent inhibition leads to thinking that specific bacteria antagonistic compounds are key for supporting future biotechnological research in controlling plant disease.
Chemical and physical attributes of soil can impact soil microbial activity in suppressive soils due to the promotion of bacteria groups with antagonistic effects. These effects can be directly to plant pathogens as a result of the action of bacterial antibiotic compounds. This mini-review concludes that the antagonistic compounds of bacteria mainly of the genus Bacillus, Burkholderia, and Pseudomonas, represent crucial tools for supporting future biotechnological research in controlling plant disease. The production of antibiotic compounds is necessary to preserve the health and the suppressiveness of soils against plant pathogens.
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