Deciphering the role of bacterial antimicrobial compounds in the Biocontrol of plant pathogenic fungi

Introduction

Pathogen infection is one of the major causes of yield loss in agricultural and horticultural crops. The rapid increase of antimicrobial resistance in plant pathogens urged researchers to develop new fungicide molecules. Antagonistic bacteria are considered as ideal biocontrol agents due to their aggressive colonization and rapid growth in the rhizosphere. These bacteria mediate biocontrol by several mechanisms. A primary mechanism of pathogen inhibition is by the production of antimicrobial peptide compounds and other factors such as siderophore production and microbial cyanide, and lytic enzymes (O’Sullivan and O’Gara, 1992).

Antimicrobial peptides (AMP) are a diverse class of naturally occurring molecule produced as a first line of defense by the bacteria with broad spectrum of activity against plant pathogens. These are the biologically active secondary metabolite compounds that possess antimicrobial and antifungal activities. Secondary metabolites (SM) produced by certain microorganisms induce plant defense reactions leading to a systemic resistance to pathogen infection.

In recent days, AMPs are acting as an attractive alternative to traditional antibiotics due to their physicochemical properties and their wide array of activities. AMP kill the pathogenic fungi by interacting with their intracellular components. Characterization of the mode of action of AMP is essential to improve their activity and to accelerate their use as an effective antimicrobial agent.

Antimicrobial compounds are specific in killing microorganisms. They cause no harm to the environment.

Role of antimicrobial compounds produced by bacteria

Phenazines are group of aromatic heterocyclic compounds produced by Bacteria as a strategy to compete for nutrients or to improve other survival conditions (Laursen and Nielsen,2004) (Table 1). They interfere with electron flow and functional enzymes related to cellular respiration. Phenazine-1-carboxylic acid (PCA), a bright lemon-yellow pigment, was first isolated and identified from Pseudomonas aureofaciens in the 1930’s by Dr. Kluyver.

Pyrrole are the antimicrobial compounds produced during secondary metabolism in some bacteria, by the genera Pseudomonas and Burkholderia. Pyrrolnitrin was first isolated in the 1960s by Arima et al., (1964) from Pseudomonas pyrrocinia. Pyrrolnitrin inhibits fungal growth by inhibiting the respiratory electron transport system.

Siderophores are compounds of low molecular weight (around 400–2000 Da). The genus Pseudomonas produces a diverse variety of siderophores. Burkholderia genus also produces pyochelin (Meyer et al.,1995). Pyochelin (Pch) and pyoverdin (Pvd) have been most intensively studied. Siderophores regulate other virulence factors of pathogens and promote plant growth (Fedrizzi, 2006). They capture iron and make unavailable to the pathogens (Neilands, 1995). They control biofilm formation of the pathogens.

Hydrogen cyanide (HCN) is an extremely volatile compound. Its mechanism of action involves inhibition of the activity of cytochrome c oxidase, preventing production of adenosine triphosphate (ATP) (Spence et al., 2014). In addition to antimicrobial activity, this compound shows nematicidal activity. The presence of HCN together with pyrrolnitrin another antimicrobial compound, contributed to the death of the model nematode, Caenorhabditis elegans (Nandi et al. (2015).

Diacetyl phloro glucinol (2,4-DAPG) is a phenolic compound of natural origin produced mainly by the genus Pseudomonas (Meyer et al., 2009). Besides stimulating ISR (Weller et al., 2012) it stimulates exudate production by plant roots (Combes Meynet et al., 2011), becoming an important protector in disease-suppressive soils. Xylocandins or cepacidins are a complex of antifungal peptides isolated originally from Burkholderia cepacia (Bisacchi et al. 1987; Meyers et al. 1987) (Table 2).

Burkholdines are octapeptide compounds which possess antifungal activity by interfering with electron flow responsible for cellular respiration. The cyclic peptide compounds, iturins are subdivided into iturin, bacillomycin, and mycosubtilin, which cause cell leakage by forming pores in the cytoplasmic membrane.

Fengycins, which are also called plastathins, are composed of a hydroxylated fatty acid and ten amino acids, comprising fengicins A and B. The antifungal activity of fengycins is due to their ability to interact with lipid components of the fungal cytoplasmic membrane, such as ergosterol, which alter its structure and permeability in a dose-dependent manner, with an interesting application in biological control of fruit diseases (Toure et al. 2004., Ongena et al. 2005).

Surfactins are composed of a hydroxylated fatty acid and seven amino acids. These are not fungitoxic by themselves, but they express some antifungal activity in synergism with iturin A, which is essential for formation of a biofilm matrix and has surfactant properties, with the capacity to increase penetration of some substances (Deravel et al. 2014; Yanez-Mendizabal et al. 2012; Gong et al. 2014). Low concentrations of surfactin have been shown to induce several plant defense events in tobacco cells (Jourdan et al. 2009; Chowdhury et al. 2015).

A natural antimicrobial product named after Hollywood actor, Keanu Reeves is effective against fungi that cause diseases in both plants and humans, according to a study. The research, published in the Journal of the American Chemical Society, describes how the natural product group of “Keanumycins”, produced by the bacteria of the genus Pseudomonas, works against plant pests. Scientists have shown that the Keanumycins work “effectively” against the plant pest Botrytis cinerea which triggers gray mold rot and causes immense harvest losses every year. Studies have also found that the active ingredient in the Keanumycin molecules can inhibit the growth of fungi dangerous to humans like Candida albicans. This group of molecules, can act as an “environmentally friendly alternative” to chemical pesticides, and may also offer an alternative in the fight against drug-resistant fungi. The latest findings, shed more light on the mode-of-action of this potential natural product and may potentially aid the development of new pharmaceutical and agrochemical antifungals.

Table 1. Different types of antimicrobial compounds produced by bacteria

Table 2. Bacterial antimicrobial compounds acting against fungi

Conclusion 

Microbial metabolism has inspired a large number of studies of bioactive compounds that can be used in biological control of plant diseases. The vast majority of natural antimicrobials come from microbial secondary metabolism, which provides benefits for the plants. These metabolites have the potential to be used in agro industry, especially in relation to pathogen control and environmental sustainability. There is a significant demand for production of new bioactive compounds that will replace the agrochemicals currently used in control of plant diseases due to increasing microbial resistance to currently used chemicals, confirming the need for development of new biological agents, from natural sources, that can be used in control of plant diseases.

Future researchable areas 

Studies on investigating new compounds from beneficial microbes against pathogenic organisms are required to develop the novel biomolecules formulation against the plant pathogens. It can be done in association with biotechnological studies by altering genome of beneficial organisms to develop more new antimicrobial compounds.

References

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Content contributors

1. Sk. Menaaz Fathima, Department of Plant Pathology, College of Agriculture, Rajendranagar, Professor Jayashankar Telangana State Agricultural University, Hyderabad, Telangana, India.
2. K. Sankari Meena, Indian Institute of Oilseeds Research, Hyderabad,
3. B. Vidya Sagar, Department of Plant Pathology, College of Agriculture, Rajendranagar, Professor Jayashankar Telangana State Agricultural University, Hyderabad, Telangana, India