Abstract
The rising demand for sustainable agriculture necessitates alternative methods to using chemical pesticides for controlling plant pathogens. Biocontrol involves the use of natural antagonists, such as bacteria, as an alternative to synthetic chemical pesticides, which can be harmful to human health and the environment. This review discusses the potential of Bacillus, Streptomyces, Pseudomonas and Serratia as biocontrol agents (BCAs) against various plant pathogens. These bacteria suppress pathogen growth via various mechanisms, such as antibiosis, nutrient and space competition and systemic resistance, and significantly contribute to plant growth. We provide an overview of the secondary metabolites, plant interactions and microbiota interactions of these bacteria. BCAs offer a promising and sustainable solution to plant pathogens and help maintain the one-health principle.
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Background
The use of natural antagonists, such as bacteria, as biocontrol agents (BCAs) has gained considerable attention in recent years as a sustainable approach to managing pests, pathogens and diseases in agriculture. Bacillus, Streptomycetes, Pseudomonas and Serratia species are key players in biocontrol. Given the rising demand for sustainable agriculture, this review discusses the potential of these bacteria as BCAs against various plant pathogens.
Bacillus
Bacillus are gram-positive rod-shaped bacteria which can either be aerobes or anaerobes (Turnbull 1996). As BCAs, specifically plant growth-promoting rhizobacteria, Bacillus protect plants through antibiosis, signal interference, induced systemic resistance and niche competition (Todorova and Kozhuharova 2010; Blake et al. 2021). Furthermore, Bacillus improve nutrient availability, alter plant growth hormone homeostasis and reduce abiotic stress to promote growth, offering an advantage for commercial use (Blake et al. 2021).
Interactions with Plants
Biocontrol Mechanisms
Bacillus are one of the most widely researched rhizobacteria and highly promising option for agricultural uses. They possess various direct and indirect mechanisms against phytopathogens. The main biocontrol secondary metabolites produced by Bacillus and their corresponding functions are outlined in Fig. 1 and Table 1.
Multifaceted roles of biocontrol agents and their metabolites in enhancing plant immunity and growth. BCAs secrete metabolites that directly or indirectly boost plant immunity. Metabolites such as chitinase and HCN can directly attack plant pathogens. Many VOCs can inhibit pathogen growth or enhance plant immunity. Some metabolites, such as acetoin, can enhance plant growth. A Bacillus can inhibit plant pathogens, such as Ralstonia, Penicillium and Erwinia. Bacillus amyloliquefaciens (BA) secretes volatile organic compounds (VOCs) to inhibit Penicillium digitatum and Ralstonia solanacearum. B. subtilis BS-1 produces AiiA, which can decrease the symptoms of disease caused by Erwinia carotovora. B Streptomycetes can inhibit plant pathogens, such as Fusarium, Rhizoctani, Gaeumannomyces, and Magnaporthe. Streptomyces lydicus WYEC108 produces chitinase to lyse the cell wall of fungi, such as Pythium. C Pseudomonas can inhibit plant pathogens, such as Pantoea, Thielaviopsis, Clavibacter and Hyaloperonospora. Pseudomonas protegens Pf-5 secretes pyoluteorin, which can reduce the growth of Pantoea ananatis DZ-12. Brassicacearum LBUM300 uses HCN against Clavibacter michiganensis and Thielaviopsis basicola. D Serratia can inhibit plant pathogens, including Staphylococcus, Didymella, Agrobacterium and Rhizoctani. Prodigiosin, produced by Serratia, has antagonistic effects on methicillin-resistant Staphylococcus aureus (MRSA), Staphylococcus epidermidis, Staphylococcus saprophyticus, Streptococcus pyogenes, Enterobacter faecalis, Bacillus cereus, Acinetobacter anitratus, Agrobacterium tumefaciens and Bacillus licheniform (ORSA). Serratia marcescens produces Serrawettin W2, which has anti-bacterial activity against Staphylococcus aureus
Induced Systemic Resistance
Aside from direct inhibition of pathogens, Bacillus enhances plant defences through induced systemic resistance (ISR). When beneficial bacteria are inoculated in the roots, the defence capacity of the entire plant against various pathogens is enhanced (Kloepper et al. 2004).
B. subtilis generates many compounds which can elicit ISR. Tomato and bean leaves with high levels of surfactin- and fengycin-producing B. subtilis in their roots are more resistant to diseases caused by Botrytis cinerea than those without B. subtilis (Ongena et al. 2007). For instance, BA strain S13-3 triggers plant defence in strawberry leaves by generating iturin A and surfactins (Yamamoto et al. 2015a). The absence of B. subtilis in the leaves shows that disease reduction is via ISR (Yamamoto et al. 2015b). Furthermore, BA strains can trigger ISR by producing VOCs such as 2,3-butadial and 3-hydroxy-2butanone(acetoin) and stimulating defence enzymes (Farag et al. 2013).
Plant Growth Promotion
Bacillus promotes plant growth via diverse mechanisms, such as providing important plant trace elements and nutrients. Nitrogen, which is an inaccessible form in the natural environment, must be mobilised into an accessible form like nitrate or ammonium ions before being used (Hayat et al. 2010). B. subtilis can fix unavailable atmospheric nitrogen to a usable form for plants. It also helps nodulation by other bacteria, leading to the colonisation of native symbiotic rhizobacteria (Elkoca et al. 2007).
Bacillus not only improves nutrient availability but also alters plant growth hormone homeostasis to promote plant growth. It can promote plant growth and cell division by producing growth hormones themselves or by inducing plant production via secreted compounds (Arkhipova et al. 2005). Acetoin (3-hydroxy-2-butanone) and 2,3-butanediol are VOCs produced by B. subtilis that can affect cytokinin and ethylene homeostasis. The leaf size of Arabidopsis thaliana significantly increases when inoculated with B. subtilis and pure 2,3-butanediol but not when inoculated with mutants of the cytokinin and ethylene pathways (Ryu et al. 2003). Furthermore, BA contains the genes patB, dhaS, yclB, yclC, yhcX and ysnE, which are implicated in indole-3-acetic acid (IAA) production. IAA can control several plant growth processes, including elongation, cell division, fruit development and root hair production stimulation (Baard et al. 2023; Schulten and Schnitzer 1997; Chen et al. 2017). IAA can also boost the quantity and length of main and lateral roots, increasing plant water and nutrient absorption (Beyeler et al. 1999; Zhang et al. 2014; Wang et al. 2023a).
Bacillus can also indirectly promote plant growth by reducing abiotic stresses. Two major restrictions for modern agriculture, water and salt stresses can be reduced by Bacillus (Li et al. 2009; Woo et al. 2020). Inoculating B. subtilis GOT9 in A. thaliana and Brassica campestris enhances tolerance to drought and salt stresses. It regulates the expression of plant genes such as phosphoethanolamine N-methyltransferase (PEAMT), especially those associated with abscisic acid, which is a key hormone for regulating stress in plants (Zhang et al. 2010). The main metabolites produced by Bacillus, which promote plant growth, and their corresponding functions are outlined in Fig. 1 and Table 2.
Interactions with the Microbiota
Antibiosis
Bacillus produce different anti-microbial compounds, including lipopeptides, exoenzymes and volatile organic compounds (VOCs) (Wang et al. 2015).
Lipopeptides, such as surfactin, protect plants against pathogens (Sansinenea and Ortiz 2011). Given its amphiphilicity, surfactin disrupts the cell membranes of other organisms by integrating into the lipid layers and, thus, reducing surface tension (Ongena and Jacques 2008). The survival rate of Arabidopsis thaliana remarkably increases when infected with Pseudomonas syringae and inoculated with surfactin-producing Bacillus subtilis but not when inoculated with a surfactin mutant strain (Putri et al. 2023). Fan et al. (2017) found that B. subtilis 9407, a surfactin producer, exerts strong anti-bacterial activity against Acidovorax citrulli and efficient biocontrol on melon seedlings in controlled greenhouse tests.
Bacillus produce exoenzymes, such as proteases and chitinases, which can decompose the fungal cell wall (Blake et al. 2021). Chitinase is one of the main anti-fungal components produced by Bacillus. Greenhouse and field test results showed that inoculating plants with chitinase-producing B. subtilis strain significantly reduces the incidence of diseases by 20–35% (Yan et al. 2011).
Bacillus also produce volatiles which can inhibit the spore germination and hyphal growth of phytopathogens in a contact-independent manner on agar plates (Grahovac et al. 2023). Bacillus amyloliquefaciens (BA) strains produce anti-microbial VOCs (Luo et al. 2022). For example, BA strains JBC36, SQR-9 and T-5 produce VOCs such as pentadecane, ethyl benzene and benzothiazole, which can inhibit Penicillium digitatum and Ralstonia solanacearum growth (Yu et al. 2012; Raza et al. 2016).
Signal Interference
Bacillus can also reduce disease intensity by reducing pathogen virulence (Pan et al. 2008). Interfering with quorum sensing (QS) signals could be an effective strategy to prevent diseases (Helman and Chernin 2015). B. subtilis produces AiiA, an enzyme which inactivates QS autoinducers (Pan et al. 2008; Dong et al. 2000; Lyng and Kovács 2023). B. subtilis BS-1, which produces AiiA, can decrease symptoms of potato soft rot caused by Erwinia carotovora, a pathogen dependent on autoinducers for virulence (Pan et al. 2008).
The rhizosphere harbours up to \({10}^{11}\) microbial cells per gram, representing more than 30,000 species (Berendsen et al. 2012). Most studies have been conducted in highly controlled conditions, which complicate replicating their results in natural environments. One of the crucial reasons for natural field variabilities is plant microbiomes. Numerous variables affect the microbial communities found in soil and around roots; consequently, these variables may also affect the efficacy of biocontrol methods (Rousk et al. 2010; Pershina et al. 2018). These elements can be broadly classified into two types. First, abiotic factors can affect microbial assemblages, including soil type (which is determined by properties such as water content, nutrient levels, pH and trace metals), climate and farming practices, such as fertilisation, tillage, irrigation and pre-cropping (Rousk et al. 2010; Pershina et al. 2018). Second, biotic parameters include host genetics, host crop species, root exude characteristics, plant age at application and competing microbes already present in the plant microbiome (Haichar et al. 2008; Turner et al. 2013; Bressan et al. 2009; Micallef et al. 2009; Chaparro et al. 2014; Edwards et al. 2018; Bakker et al. 2015). Interactions between microbes, whether cooperative or competitive, can either enhance or impede the colonisation of Bacillus on roots or even determine its success (Blake et al. 2021).
Bacillus to be used as BCAs should adapt to natural ecology and preserve the original microorganisms. Indeed, adding Bacillus to a natural rhizosphere has minimal impact on the natural rhizosphere bacterial community. A previous study inoculated B. subtilis PTS-394 into tomatoes; results showed that the bacterial community 1 day after inoculation is distinct from that in the control, but the bacterial community 14 days after inoculation is similar to that in the control (Qiao et al. 2017). This result indicates that Bacillus do not spoil the natural existing plant microbiome. However, the effects of the natural plant microbiome on Bacillus warrant further investigation.
Streptomycetes
Streptomycetes, a gram-positive genus belonging to Actinobacteria, has drawn considerable attention owing to its potential as a sustainable BCA (Pacios-Michelena et al. 2021). Streptomyces species in plant root microbiomes produce inhibiting metabolites against pests and pathogens.
Interactions with Plants
Biocontrol Mechanisms
Streptomyces are soil bacteria which serve as BCAs via several ways. They produce anti-microbials, enzymes, VOCs and anthelmintic compounds. They also indirectly inhibit phytopathogens (Newitt et al. 2019a). The main biocontrol secondary metabolites produced by Streptomyces and their corresponding functions are outlined in Fig. 1 and Table 1.
Induced Systemic Resistance
Streptomyces can indirectly suppress plant pathogens through competitive exclusion and activation of host resistance mechanisms (Ebrahimi-Zarandi et al. 2022). ISR promotes various changes, including the accumulation of defence-related chemicals, localised cell death and cell wall reinforcements, resulting in an enhanced and more efficient response to future pathogenic onslaught (Viaene et al. 2016; Lugtenberg and Kamilova 2009; Kurth et al. 2014). Inoculating oak trees with Streptomyces sp. AcH505 upregulates the expression of pathogenesis-related proteins (Kurth et al. 2014).
Plant Growth Promotion
When searching for novel BCAs, Streptomyces are becoming a more visionary choice because of their capacity to colonise plant roots and ability to create strong anti-microbial secondary metabolites (Díaz-Díaz et al. 2023). This is especially true given that members of this genus promote plant growth under normal and stressful environmental conditions, such as high salinity, and protect plants from diseases (Viaene et al. 2016; Chater 2006; Palaniyandi et al. 2014; Tripathi and Singh 2018). These additional advantages may serve as the basis for highly desirable BCAs which can promote plant growth and protect against diseases (Newitt et al. 2019a).
Interactions with the Microbiota
Disease-Suppressive Soil
Streptomyces can directly protect plant hosts against infections in the soil, rhizosphere and endosphere by producing anti-microbial chemicals or particular enzymes, including cellulases, chitinases and proteases (Meij et al. 2017). Disease-suppressive soils are well-known examples of microbial-based protection against soil-borne pathogens (Weller et al. 2002). Streptomyces species are enriched in these soils and strains have been utilised to create the biofungicide Mycostop®, which is effective against diverse crop diseases, including wheat head blight caused by Fusarium (Lahdenperä et al. 1991).
Antibiosis
In addition to disease-suppressive soils, Streptomyces can act as BCAs by producing anti-microbials, exoenzymes, VOCs and anthelmintic compounds (Newitt et al. 2019b).
Streptomyces can inhibit Magnaporthe oryzae, Gaeumannomyces graminis var. tritici, Fusarium species and Rhizoctani solani in vitro (Dean et al. 2012; Law et al. 2017). Administration of Streptomyces BN1 (isolated from Fusarium-contaminated rice grains) to seeds as a spore preparation ameliorates the reduction in seedling length caused by Fusarium (Jung et al. 2013). Streptomyces are promising BCAs for take-all wheat disease because of its saprotrophic and spore-forming lifestyle, which allows it to persist under harsh environments (Meij et al. 2017; Coombs et al. 2004).
Streptomyces encode a huge number of secreted proteins with a wide range of extracellular functions; for instance, they can produce chitinases, which breakdown chitin (Wang et al. 2023b). Chitinases are gaining popularity as BCAs because of their capacity to suppress a wide range of phytopathogenic fungi and oomycetes (Chater et al. 2010). Purified chitinase from Streptomyces lydicus WYEC108 can lyse the cell walls of numerous phytopathogenic fungi, including Pythium, which may cause root rot in cereal crops (Mahadevan and Crawford 1997).
Streptomyces is a prolific generator of VOCs, which are small molecules with low weights and high vapour pressures (Mendes et al. 2013; Cordovez et al. 1081; Wheatley 2002). Several VOCs exert anti-bacterial activities against phytopathogenic organisms, such as R. solani (Mendes et al. 2013; Chapelle et al. 2016). These compounds may be utilised as biofumigants to restrict the growth of pathogenic organisms and prevent soil-borne diseases (Newitt et al. 2019a). Some studies suggested the use of VOCs as biofumigants (Gong et al. 2022). However, further research is necessary to confirm whether these chemicals are synthesised in vivo in the plant root system and effective under natural settings (Newitt et al. 2019a).
Streptomyces generate effective anthelmintic chemicals, such as avermectin, which may kill cereal cyst nematodes (Burg et al. 1979; Huang et al. 2014). Some Streptomyces species can regulate nematode populations (Nour et al. 2003; Samac and Kinkel 2001; Zhang et al. 2020).
The antagonistic behaviour of strains which prevent the establishment of plant pathogenic microbes in soil can exclude beneficial species and disturb important biogeochemical cycles, among other unintended consequences (Chaparro et al. 2014). Some Streptomycetes species produce antibiotics and prevent the formation of nodules by nitrogen-fixing bacterial species in the roots of leguminous plants and the beginning of plant host symbioses with mycorrhizal fungus (Gregor et al. 2003; Samac et al. 2003; Schrey and Tarkka 2008). However, other Streptomyces species can promote mycorrhizal development and nodulation while inhibiting pathogenic growth. Therefore, candidate biocontrol species must be selected and screened carefully (Gregor et al. 2003).
Pseudomonas
Pseudomonas is a genus of the Gammaproteobacteria (Battistuzzi and Hedges 2009). Some of their characteristics are useful in plant growth promotion and biocontrol (Peix et al. 2009). Many Pseudomonas strains can directly stimulate plant development in no pathogen condition by enhancing mineral nutrient availability and uptake through phosphate solubilisation. Moreover, they can enhance root growth by synthesising phytohormones or increasing tolerance to abiotic stress. They are effective soil-borne disease controllers and good root colonisers. Certain Pseudomonas strains can also prevent leaf diseases through ISR in plants. Typically, Pseudomonas biocontrol strains do not survive well on above-ground plant parts, with the exception of a few strains from P. syringae.
Interactions with Plants
Biocontrol Mechanisms
Pseudomonas have several mechanisms that can suppress plant disease. They can secrete antibiosis, compete with other bacteria for nutrients or space, and trigger ISR. Particularly, secondary metabolites of Pseudomonas are key players in the biocontrol of plant diseases. The main biocontrol secondary metabolites produced by Pseudomonas and their corresponding functions are outlined in Fig. 1 and Table 1.
Induced Systemic Resistance
Some secondary metabolites mentioned earlier can trigger ISR. In many plants, phenazines cause ISR (Ma et al. 2016). DAPG can trigger ISR in Arabidopsis by inducing jasmonate- and ethylene-mediated defence responses to the mildew pathogens Hyaloperonospora parasitica, Pseudomonas syringae pv. tomato and Botrytis cinerea (Iavicoli et al. 2003; Weller et al. 2012; Chae et al. 2020). Siderophores, along with other bacterial secretions, can trigger ISR in plants. Specifically, Pseudomonas aeruginosa 7NSK2 produces the siderophores pyoverdine and pyochelin. These compounds have demonstrated effectiveness in protecting plants from diseases caused by pathogens such as Pythium splendens and Botrytis cinerea (Aznar and Dellagi 2015). In addition, this bacterium secretes pyocyanin, a phenazine compound. Notably, it has been found that pyocyanin, in conjunction with pyochelin, can induce ISR, thereby protecting tomatoes against diseases caused by B. cinerea through the promotion of ROS accumulation (Audenaert et al. 2002).
Plant Growth Promotion
Pseudomonas strains can promote plant growth through several mechanisms. DAPG interferes with the auxin-dependent signalling system and promotes root branching in tomatoes, and it can stimulate amino acid exudation from plant roots (Phillips et al. 2004; Brazelton et al. 2008). Biosurfactants are secondary metabolites involved in root growth, nutrient availability, swarming movement, biofilm formation, environmental adaptation and nutrient cycling (D'Aes et al. 2010; Oni et al. 2015; Raaijmakers et al. 2010). The main metabolites produced by Pseudomonas, which promote plant growth, and their corresponding functions are outlined in Fig. 1 and Table 2.
Interactions with the Microbiota
Pseudomonas strains are commonly found in natural environments, particularly soil. P. chlororaphis isolates have been found from the soil and rhizosphere of crops, such as potato, tomato, radish, beet, maize, soja, alfalfa, sugarcane and clover (Biessy et al. 2019). Rhizopus and brown rot diseases on peaches can be successfully suppressed by P. syringae isolates MA-4 and NSA-6 from the phyllosphere of apples in Canada (Yang and Hong 2020). P. protegens 1B1, P. clororaphis 48G9 and P. brassicacearum 93G8 can reduce the incidence of hairy root disease caused by Agrobacterium rhizogens by up to 95% on Kalanchoe, soybean and tomato (Freitas and Taylor 2023).
In addition, Pseudomonas can form synergistic relationships with other species. In the cucumber rhizosphere, syntrophic cooperation between Bacillus velezensis SQR-9 and Pseudomonas stutzeri is highly dependent on the environment and involves pathways for the biosynthesis of branched-chain amino acids. The relationship, which promotes plant growth and reduces salt stress, is dependent on Bacillus biofilm matrix components (Sun et al. 2022).
Several studies have investigated the impact of Pseudomonas strains on non-target organisms, particularly microbial species and total microbial populations. Wild-type and genetically modified DAPG-overproducing Pseudomonas BCAs do not interfere with arbuscular mycorrhizal fungi symbiosis, which establish symbiotic partnerships with the majority of land plants (Barea et al. 1998; Edwards et al. 1998; Vázquez et al. 2000). The effect of the native culturable bacterial and fungal populations on the cucumber rhizosphere has been studied using the wild-type P. fluorescens strain CHA0-Rif and a derivative CHA0-Rif/pME3424 which overproduces DAPG and pyoluteorin. Some researchers found no changes in the frequency of dominant bacterial groups (Natsch et al. 1998). Others noted a discernible impact on the population of culturable fungi, but it was smaller than the results of consistently producing cucumbers in the same soil (Girlanda et al. 2001).
Antibiosis
Secondary metabolites from Pseudomonas can exert anti-microbial and insecticidal activities. In most cases, a single type of secondary metabolite exhibits pleiotropic effects. One of the most conserved metabolites is phenazines. Pseudomonas produce phenazines, which are tricyclic compounds that contain nitrogen and are redox-active (Mavrodi et al. 2006). Biocontrol strains mainly generate 2-hydroxyphenazine (1-OH-PHZ, brick-red) or 2-hydroxyphenazine-1-carboxylic acid (PCA, citrus yellow) (2-OH-PCA, orange). The production of phenazines in Pseudomonas is regulated by QS, which involves the GacS/GacA two-component signal transduction system. Phenazines have a broad-spectrum action against bacterial, fungal and oomycete diseases, including those caused by Rhizoctonia solani, Streptomyces scabies and Phytophthora infestans (Thomashow and Weller 1988; Jaaffar et al. 2017; Arseneault et al. 2015; Morrison et al. 2017).
Another well-conserved metabolite among Pseudomonas strains is 2,4-diacetylphloroglucinol (DAPG). This polyketide antibiotic is predominantly synthesised by P. protegens and P. corrugata, along with a limited number of strains from other taxonomic families (Almario et al. 2017). DAPG is effective against bacteria, nematodes, oomycetes and fungi, making it crucial in the biocontrol of diseases in the roots and seedlings. Pseudomonas sp. LBUM300 produces DAPG, which exhibits antagonistic activity against Clavibacter michiganensis subsp. michiganensis in vitro and in planta (Lanteigne et al. 2012).
Pseudomonas strains, particularly P. protegens and a few P. aeruginosa isolates, produce pyoluteorin (Ramette et al. 2011; Hu et al. 2005). In Pantoea ananatis DZ-12, which causes maize brown rot on leaves, P. protegens Pf-5 exhibits biocontrol activity and extracts a crude extract that includes pyoluteorin. Pyoluteorin significantly prevents DZ-12 growth and causes cytoplasmic extravasations and cell hollowing (Gu et al. 2022).
Hydrogen cyanide (HCN) produced by Pseudomonas exhibits multifaceted effects on pathogens owing to its cellular function. The respiratory toxin HCN prevents many species from producing cytochrome c oxidase, which is the final link in the respiratory chain. P. aeruginosa and different subsets of P. fluorescens contain recognised HCN producers. In Pseudomonas, HCN production is often associated with DAPG synthesis, particularly in the P. corrugate, P. protegens and P. chlororaphis subgroups. Tobacco black root rot induced by Thielaviopsis basicola is prevented by HCN produced by P. protegens CHA0 (Voisard et al. 1989). Additionally, Pseudomonas-produced HCN suppresses root-knot nematodes, aphids, termites and other insects (Siddiqui et al. 2006; Kang et al. 2019; Devi and Kothamasi 2009; Flury et al. 2017).
Few Pseudomonas bacteria can generate various strain-specific bioactive compounds. Rhizoxins, which are generated by a few isolates of P. protegens and P. chlororaphis MA342, are active against oomycetes and fungi (Ligon et al. 2000). The biocontrol species Pseudomonas sp. CMR12a is the only one that produces the anti-microbial cyclic lipopeptide sessilin (D'Aes et al. 2014). Pseudomonas putida RW10S1 produces the anti-bacterial promysalin, which attacks gram-positive and gram-negative bacteria (Li et al. 2011; Kaduskar et al. 2017). P. fluorescens SBW25 secretes the non-proteinogenic amino acid l-furanomycin, which suppresses gram-negative plant pathogenic bacteria (Trippe et al. 2013).
Serratia
Serratia marcescens, the type species for the newly discovered genus, was first reported in 1823 (Bizio 1823). Serratia are gram-negative bacteria from the Enterobacteriaceae family and classified into 18 specie. This group of bacteria includes biologically and ecologically diverse species, ranging from those which are useful to economically beneficial plants to pathogenic species which are harmful to humans. Serratia are remarkable for their secondary metabolism and their capacity to create a wide variety of natural bioactive compounds (Kai et al. 2007; Matilla et al. 2015; Domik et al. 2016a).
Interactions with Plants
Biocontrol Mechanisms
Serratia can act as BCAs in plants by competing with other pathogens directly or indirectly. The main biocontrol secondary metabolites produced by Serratia and their corresponding functions are outlined in Fig. 1 and Table 1.
Induced Systemic Resistance
Certain Serratia strains, such as Serratia marcescens CDP-13, can up-regulate ISR in plants. In water agar tests, wheat plants inoculated with S. marcescens CDP-13 exhibited significantly reduced susceptibility to diseases triggered by Fusarium graminearum (Singh and Jha 2016). Prior studies support Serratia’s ability to enhance ISR, though the specific mechanism of plant disease resistance remains elusive. Therefore, future research should concentrate on the tissue-specific induction of systemic resistance and its correlation with the reduction of plant pathogen susceptibility (Singh and Jha 2016).
Plant Growth Promotion
Specific Serratia strains are known to promote plant growth. They can produce IAA, which positively influences plant growth, especially when exposed to elevated levels of metalloids such as arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), manganese (Mn), nickel (Ni), and lead (Pb) (Mondal et al. 2022). Greenhouse experiments demonstrated that plants bacterized with S. marcescens NBRI1213 showed significant increases in shoot length, shoot dry weight, root length and root dry weight compared to untreated control plants.
Interactions with the Microbiota
Antibiosis
The unique trait of Serratia is the production of prodigiosin (2-methyl-3-pentyl-6-methoxyprodiginine) (Han et al. 2021), a bioactive compound from the prodiginine family. Prodigiosin is a tripyrrole red pigment secreted into the culture medium as a secondary metabolite (Han et al. 2021). Only four species—S. marcescens, S. plymuthica, S. nematodiphila and S. rubidaea—can produce prodigiosin (de Murguia 2018). The bacterial plasma membrane is the prodigiosin's primary target (Suryawanshi et al. 2017). As a chaotropic stressor, prodigiosin disrupts the bacterial plasma membrane and causes the loss of vital intracellular components, such carbohydrates, amino acids, proteins and \({K}^{+}\) ions, from cells exposed to it (Suryawanshi et al. 2017). Prodigiosin has broad-spectrum anti-bacterial properties against methicillin-resistant Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus saprophyticus, Streptococcus pyogenes, Enterobacter faecalis, Bacillus cereus, Acinetobacter anitratus, Agrobacterium tumefaciens and Bacillus licheniform (ORSA) (Nguyen et al. 2022; Yip et al. 2021). Prodigiosin is also effective against other pathogens, including insects, nematodes and phytopathogenic fungi, which affect crops (Choi et al. 2021; Nguyen et al. 2021).
Antibiotics of the carbapenem group are also produced by Serratia isolates (Moellering et al. 1989). Carbapenems are a broad group of b-lactam antibiotics characterised by strong anti-bacterial and b-lactamase-inhibitory activity (Moellering et al. 1989). As anti-microbial agents, they have a wide range of uses and are particularly useful in infections caused by bacteria that are resistant to different drugs (Moellering et al. 1989). In Serratia sp. And S. marcescens, carbapenem production and regulation have been extensively researched (McGowan et al. 1996).
According to Soberon-Chavez and Maier, Serratia produces biosurfactants called serrawettins (Soberón-Chávez and Maier 2011). They lack amino acid residues with ionic hydrophilicity, making them non-ionic (Matsuyama et al. 2011). They can alter the hydrophobicity of the cell surface, which is crucial for the adherence of these bacteria to diverse surfaces and helps promote the surface spreading of bacteria in environments with low nutrient availability (Su et al. 2016; Zhang et al. 2021). Serrawettin W1, W2 and W3 are molecular species that have been identified. Serrawettin W1 promotes swarming motility and exhibits a broad-spectrum anti-microbial action, which may help the bacterium survive antibiotics and move into more advantageous microenvironments (Kadouri and Shanks 2013; Lapenda et al. 2015). Serrawettin W2, a biosurfactant which can disperse Caenorhabditis elegans and exert anti-bacterial activity against Staphylococcus aureus, was initially isolated from S. marcescens in 1986 (Pradel et al. 2007). Many S. marcescens strains simultaneously generate prodigiosin and serrawettin W1 (Soo et al. 2014). S. surfactantfaciens YD25 may simultaneously synthesise prodigiosin and serrawettin W2 (Su et al. 2016). In contrast to serrawettins W1 and W2, serrawettin W3 has only been partially characterised (Matsuyama et al. 1986).
Althiomycin is a secondary metabolite of Serratia. The non-pigmented model insect pathogen S. marcescens strain Db10 produces althiomycin (Gerc et al. 2012). B. subtilis grows slowly due to the presence of this diffusible metabolite (Fujimoto et al. 1970).
Anti-fungal
Natural anti-fungal substances have been identified in Serratia. Because of its powerful bioactivity against plant pathogenic oomycetes, oocydin A, a chlorinated macrolide, was originally isolated from the plant epiphytic strain S. marcescens MSU97 in 1999 (Strobel et al. 1999). Oocydin A is a polyketide-type natural product with anti-fungal activity. S. plymuthica strains A153, 4Rx5 and 4Rx13 generate oocydin A (Matilla et al. 2015). The potential of Serratia sp. B1_6 to prevent the plant disease caused by Verticillium dahliae may be linked to its capacity to produce oocydin A. Several S. plymuthica strains exert in vitro anti-fungal activities against fungal infections (Berg 2000). However, the chemical nature of these anti-fungal products remains to be determined.
VOCs
Sodorifen, a recently discovered VOC, is another distinctive substance generated by S. plymuthica isolates (Domik et al. 2016b; Weise et al. 2014). Sodorifen, also known as 1,2,4,5,6,7,8- heptamethyl-3-methylenebicyclo[3.2.1]oct-6-ene, is a rare and unique volatile hydrocarbon (Reuß et al. 2010). The biological function of sodorifen remains unknown, although it may result from terpene metabolism, and the gene cluster in charge of its manufacture has been located (Domik et al. 2016a). S. plymuthica PRI-2C produces sodorifen when exposed to VOCs released by the fungus Fusarium culmorum (Schmidt et al. 2017). Dimethyl is also a VOC secreted by Serratia. Serratia ureilytica and S. bockelmannii can synthesise dimethyl disulphide in vitro (Abreo et al. 2021). The growth of Pythium cryptoirregulare is inhibited by bacterial and exogenous dimethyl disulphide. As a result, P. cryptoirregulare-induced damping-off of tomato seedlings is reduced by S. ureilytica (Abreo et al. 2021).
The soil is a complex and highly competitive ecosystem, and many soil bacteria react to complex and highly competitive conditions in different ways. Some of these bacteria outcompete other species in their capacity to (1) utilise a wide range of frequently resistant carbon compounds and (2) grow efficiently on those substrates, giving rise to vast populations in a short amount of time (Varivarn et al. 2013). To fight potential competitors, natural soil bacteria frequently use ‘chemical warfare’, generating and secreting bioactive, inhibiting chemicals (Czaran et al. 2002; Hibbing et al. 2010). Some Serratia isolates, particularly those coming from soil, have adopted this strategy (de Murguia 2018). The root and foot rot of Piper betle caused by the oomycete Phytophthora nicotianae can be biologically controlled by S. marcescens NBRI 1213 (Lavania et al. 2006). Wheat fungal infections are reduced by S. marcescens CDP-13 (Singh and Jha 2016). S. plymuthica HRO-C48 can inhibit the pathogens V. dahlia in strawberries, oilseed rapeseed and olive and Rhizoctonia solani in lettuce (Kai et al. 2007; Grosch et al. 2005; Kurze et al. 2001). It also produces mVOCs with detrimental effects on the mycelial proliferation of R. solani (Kai et al. 2007; Grosch et al. 2005; Kurze et al. 2001). S. plymuthica S13 is antagonistic toward Didymella bryoniae, the causal agent of black rot in pumpkins under field conditions (Fürnkranz et al. 2012; Muller et al. 2013). S. plymuthica 4Rx13 has anti-fungal activities and produces mVOCs, especially sodorifen (Kai et al. 2007; Domik et al. 2016b; Weise et al. 2014). S. proteamaculans 1–102 can act as a BCA against V. dahliae (Alström 2001).
Concluding Remarks and Future Perspectives
Bacillus, Streptomycetes, Pseudomonas and Serratia show great potential as effective BCAs against various plant pathogens. They use different mechanisms, including antibiosis, competition for nutrients and space, induction of systemic resistance and plant growth promotion, to suppress pathogen growth. However, several improvements, such as optimising formulation techniques and delivery methods, scaling up production, meeting regulatory requirements and increasing cost-effectiveness, are necessary before they can be successfully implemented in the field. Nevertheless, the use of bacterial BCAs provides a promising and sustainable solution to the plant pathogen problem in agriculture, and their potential applications in promoting plant growth and enhancing soil health make them an important tool in maintaining the one-health principle. Further research and development of these BCAs is essential for the future of sustainable agriculture.
Data Availability
Not applicable.
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Acknowledgements
We would like to express our gratitude to the members of the IMGN lab, with a special acknowledgement to Se Jin Choi for valuable comments. This research was supported by a grant from Kyung Hee University in 2022 (KHU-20220792) and by the Institute for Basic Science (IBS-R021-D1-2023-a00).
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Kyung Hee University (KHU-20220792); Institute for Basic Science (IBS-R021-D1-2023-a00).
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JL, SK and HJ contributed to the writing of the main manuscript text. SK was responsible for the creation of figures, while HJ developed the tables. B-KK, JAH and H-SL provided supervision for the project. The concept for the project was formulated by H-SL.
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Lee, J., Kim, S., Jung, H. et al. Exploiting Bacterial Genera as Biocontrol Agents: Mechanisms, Interactions and Applications in Sustainable Agriculture. J. Plant Biol. 66, 485–498 (2023). https://doi.org/10.1007/s12374-023-09404-6
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DOI: https://doi.org/10.1007/s12374-023-09404-6