Elsevier

Pedosphere

Volume 32, Issue 1, February 2022, Pages 15-38
Pedosphere

Hydrogen cyanide production by soil bacteria: Biological control of pests and promotion of plant growth in sustainable agriculture

https://doi.org/10.1016/S1002-0160(21)60058-9Get rights and content

ABSTRACT

Currently, plant diseases and insect infestations are mainly controlled by the extraneous application of pesticides. Unfortunately, the indiscriminate use of such agrochemicals can cause ecological and environmental problems, as well as human health hazards. To obviate the potential pollution arising from the application of agrochemicals, biological control of soilborne pathogens or insect pests using antagonistic microorganisms may be employed. Certain soil bacteria, algae, fungi, plants and insects possess the unique ability to produce hydrogen cyanide (HCN), which plays an important role in the biotic interactions of those organisms. In particular, cyanogenic bacteria have been found to inhibit the growth of various pathogenic fungi, weeds, insects, termites and nematodes. Thus, the use of HCN-producing bacteria as biopesticides offers an ecofriendly approach for sustainable agriculture. The enzyme, HCN synthase, involved in the synthesis of HCN, is encoded by the hcnABC gene cluster. The biosynthetic regulation of HCN, antibiotics and fluorescent insecticidal toxins through the conserved global regulatory GacS/GacA system is elaborated in this review, including approaches that may optimize cyanogenesis for enhanced pest control. In addition, the effects of bacterially synthesized HCN on the production of indole acetic acid, antibiotics and fluorescent insecticidal toxins, 1-aminocyclopropane-1-carboxylate deaminase utilization and phosphate solubilization may result in the stimulation of plant growth. A more detailed understanding of HCN biosynthesis and regulation may help to elaborate the precise role of this compound in biotic interactions and sustainable agriculture.

Section snippets

INTRODUCTION

The most common yield-limiting constraints in agriculture are plant diseases, insect infestations, weeds and abiotic stress conditions, all of which can have a profound negative effect on the growth of plants, potentially resulting in heavy losses of plant biomass. Diseases caused by various plant pathogens and insects account for 20%–40% of annual yield losses in various cereal and legume crops worldwide (Ross and Lembi, 1985; Alexandratos and Bruinsma, 2012; Sindhu et al., 2017a). In an

MICROBIAL COMMUNITY IN RHIZOSPHERE

Plants have co-evolved with specific communities of microorganisms (i.e., the plant microbiome) that play crucial roles in the host's development and health (Berg et al., 2017; Olanrewaju et al., 2017; Mohanram and Kumar, 2019; Kour et al., 2020). However, the interactions between plants and their surroundings are dynamic processes in which plants monitor their environment and react to changes in the microbial community through signal exchange (Sindhu et al., 2017b; Phour et al., 2020). The

HYDROGEN CYANIDE PRODUCTION BY DIFFERENT MICROORGANISMS AND QUANTIFICATION OF HCN PRODUCED

Hydrogen cyanide is produced by bacteria through the metabolic pathway of bacterial cyanogenesis (Blumer and Haas, 2000; Zdor, 2015). Bacterial production of HCN has been associated with growth suppression and killing of other living organisms (Zdor, 2015). A number of bacterial species produce cyanide as a secondary metabolite, although it is mainly Pseudomonas spp. and Bacillus spp. that have the potential to produce HCN (Subramanian and Satyan, 2014; Pourbabaee et al., 2018; Anand et al.,

ROLE OF HCN IN BIOLOGICAL CONTROL

Bacterial strains for biocontrol typically have more than one mechanism to inhibit the growth of pathogens, weeds or pests. Hydrogen cyanide is usually synthesized by PGPB in small quantities, which ensures that fungi do not develop resistance to the other bacterially synthesized antifungal metabolite(s), thereby enhancing the effectiveness of the biocontrol strain (Olanrewaju et al., 2017). Various microbial strains, including fluorescent Pseudomonas and Bacillus strains, have been reported to

EFFECTS OF CYANOGENIC BACTERIA ON PLANT GROWTH AND DISEASE CONTROL

Pseudomonas fluorescens and related species, including P. protegens, P. chlororaphis and P. corrugata, as well as species like P. putida and P. cepacia are widely recognized for their biocontrol potential and beneficial associations with diverse plant hosts (Mercado-Blanco and Bakker, 2007; Avis et al., 2008; Couillerot et al., 2009; Dorjey et al., 2017). The biocontrol ability of these species has been attributed to the secretion of HCN, 2,4-diacetylphloroglucinol, pyoluteorin, pyrrolnitrin,

ATTRIBUTES OF HCN-PRODUCING BACTERIA LEADING TO GROWTH PROMOTION OF PLANTS

The majority of the bacterial strains isolated from the rhizosphere possess the ability to produce IAA, siderophores, phosphate solubilization activity and HCN (Table I). Correlation analysis between the existing plant beneficial traits measured across selected rhizobacterial isolates revealed a clear pattern of co-occurrence of these traits within diverse rhizobacterial species.

BIOSYNTHESIS OF HCN AND ITS REGULATION

Some bacterial strains contain a membrane-bound flavoenzyme, HCN synthase that oxidizes glycine to HCN and carbon dioxide, under low oxygen levels during the early stationary phase of growth (Laville et al., 1998; Zdor, 2015). On the other hand, synthesis of HCN in P. aeruginosa occurs via the oxidative decarboxylation of glycine by HCN synthase enzyme (Blumer and Haas, 2000). This process also produces four electrons and four hydrogen ions per glycine molecule. Cyanogenesis, in relation to P.

PERSPECTIVES AND FUTURE CONSIDERATIONS

Stressed environments and fertilization with nitrogenous and phosphatic fertilizers have been found to enhance HCN synthesis in sorghum plants. In pathogenic bacteria, biotic stress can cause the synthesis of virulence factors in pathogens (Heeb and Haas, 2001). Under abiotic stress conditions, enhanced synthesis of HCN occurs in bacteria as well as sorghum plants through the GacS/GacA regulon. This regulon also controls the biosynthesis of antibiotics and the fluorescent insecticidal toxins,

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