The power of the smallest: The inhibitory activity of microbial volatile organic compounds against phytopathogens

Abstract

Plant diseases caused by phytopathogens result in huge economic losses in agriculture. In addition, the use of chemical products to control such diseases causes many problems to the environment and to human health. However, some bacteria and fungi have a mutualistic relationship with plants in nature, mainly exchanging nutrients and protection. Thus, exploring those beneficial microorganisms has been an interesting and promising alternative for mitigating the use of agrochemicals and, consequently, achieving a more sustainable agriculture. Microorganisms are able to produce and excrete several metabolites, but volatile organic compounds (VOCs) have huge biotechnology potential. Microbial VOCs are small molecules from different chemical classes, such as alkenes, alcohols, ketones, organic acids, terpenes, benzenoids and pyrazines. Interestingly, volatilomes are species-specific and also change according to microbial growth conditions. The interaction of VOCs with other organisms, such as plants, insects, and other bacteria and fungi, can cause a wide range of effects. In this review, we show that a large variety of plant pathogens are inhibited by microbial VOCs with a focus on the in vitro and in vivo inhibition of phytopathogens of greater scientific and economic importance in agriculture, such as Ralstonia solanacearum, Botrytis cinerea, Xanthomonas and Fusarium species. In this scenario, some genera of VOC-producing microorganisms stand out as antagonists, including Bacillus, Pseudomonas, Serratia and Streptomyces. We also highlight the known molecular and physiological mechanisms by which VOCs inhibit the growth of phytopathogens. Microbial VOCs can provoke many changes in these microorganisms, such as vacuolization, fungal hyphal rupture, loss of intracellular components, regulation of metabolism and pathogenicity genes, plus the expression of proteins important in the host response. Furthermore, we demonstrate that there are aspects to investigate by discussing questions that are still not very clear in this research area, especially those that are essential for the future use of such beneficial microorganisms as biocontrol products in field crops. Therefore, we bring to light the great biotechnological potential of VOCs to help make agriculture more sustainable.

Keywords: bioactive compounds; biological control; biotechnology; microbial volatile organic compounds; phytopathogens; sustainability.

Figure 1

Biotechnological aspects of microbial volatile organic compounds (VOCs). They are produced by fungi and bacteria and belong to diverse chemical classes that can be identified by several techniques, such as gas chromatography coupled to mass spectrometry (GC–MS). These molecules have great biotechnology potential as plant growth promoters and phytopathogen inhibitors, and many studies have demonstrated such effects in vitro and in vivo. Therefore, it has become possible to develop bioproducts to be applied in the field and thereby reduce the use of agrochemicals. Nevertheless, some questions about the use of microbial VOCs as biotechnological products need to be answered. Moreover, although several beneficial microorganisms and bioactive VOCs have been described, the molecular mechanisms of action of these compounds remain poorly understood.

Figure 2

Microbial VOCs affect the morphology and physiology of phytopathogens. Through diverse approaches, it is possible to understand the changes that microbial VOCs cause in phytopathogens. Microscopy analyses revealed changes in the morphology of the colonies, loss of intracellular components, vacuolization, and cell rupture. In addition, omics-approaching studies have shown that many genes and proteins are up-and downregulated under the effects of VOCs, thus interfering with several important metabolic pathways, such as carbon metabolism and oxidative stress. GLU, glucose; SOD, superoxide dismutase; ABC, ATP-binding cassette; CAZymes, carbohydrate-activated enzymes; CE, carbohydrate esterases; GH, glycosyl hydrolases; PL, polysaccharide lyases; AA, auxiliary activities.