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. 2019 Jul 29;56(11):4992–4999. doi: 10.1007/s13197-019-03971-8

Postharvest biocontrol of Colletotrichum gloeosporioides on mango using the marine bacterium Stenotrophomonas rhizophila and its possible mechanisms of action

J J Reyes-Perez 1,2, L G Hernandez-Montiel 3,✉, S Vero 4, J C Noa-Carrazana 5, E E Quiñones-Aguilar 6, G Rincón-Enríquez 6
PMCID: PMC6828899  PMID: 31741523

Abstract

The marine bacterium Stenotrophomonas rhizophila was assessed in vitro and in vivo as biocontrol agent against anthracnose disease of mango fruit caused by Colletotrichum gloeosporioides. The results showed that in vitro inhibition of the colony diameter and spore germination of the phytopathogen was due to the production of VOCs, competition for nutrients, and lytic enzymes. When a concentration of 1 × 108 cells ml−1 of the antagonist bacterium was applied to the fruit, disease incidence was reduced by 95%, and the lesion diameter of anthracnose decreased by 85%, which offered greater protection than the synthetic fungicide. This is the first report of antagonistic mechanisms of the marine bacterium S. rhizophila against anthracnose disease in mango, which in this study was found to be more effective than the synthetic fungicide.

Keywords: Biological control, Marine bacterium, Postharvest disease, Stenotrophomonas rhizophila

Introduction

Mango (Mangifera indica L.) is a popular fruit appreciated around the world for its flavor, color and nutritional value (Sharma and Rao 2017). Most the world’s mango production is concentrated in regions of Asia and the Pacific with close to 70%, followed by Latin America and the Caribbean with more than 10% and Africa with 9%, among others. In Latin America, Mexico is the main mango exporter country with more than 1.8 million annual tons, which are mainly exported to the United States, Canada, Russia, Australia, Norway, Spain, France, Italy and the United Kingdom. Mango is cultivated mainly in regions with tropical and sub-tropical climates with high relative humidity (Levin et al. 2018), conditions that also favor the development of diverse fungal phytopathogens. One of the most problematic in negatively affecting production is Colletotrichum gloeosporioides, the causal agent of anthracnose, considered the most common disease for fruit worldwide (He et al. 2017). This disease harms mango fruit, limiting sales both nationally and internationally (Bally et al. 2009). At world level, anthracnose has caused losses of up to 60% in mango production (Madhu and Pradeep 2016).

Conventional methods of control of anthracnose are based mainly on the application of synthetic fungicides; nonetheless, their common use has caused new generations of phytopathogens resistant to treatment (Gotor-Vila et al. 2017). In addition to this limitation on effectiveness of synthetic fungicide, there is growing interest of consumers for healthier food without dangerous chemical residues. Thus, there is growing interest in the development of non-fungicide control methods for reducing postharvest fruit losses caused by phytopathogens (Zhang et al. 2017).

Biological control with microbial antagonists has become a promising alternative for controlling fungi causing diseases at the postharvest level (Dukare et al. 2018). Microorganisms with this potential are very diverse, among which epiphytic bacteria stand out (Ahmed et al. 2014), specifically, those isolated on fruit surface or fruit lesions (Gava et al. 2018). Nonetheless, there are other environments, such as the marine ecosystem that represents an important biological resource for searching for new antagonistic microbial agents toward phytopathogens (Chi et al. 2010). However, some studies have demonstrated that microorganisms from other environments, such as the marine ecosystem, could be also highly efficient for the control of fungal plant pathogens (Wang et al. 2010).

In the last years, agricultural interest in the bacterium Stenotrophomonas rhizophila has been growing because of its capacity for promoting plant growth, fixing nitrogen, conferring resistance to saline stress, as well as its antagonism toward soil phytopathogens (Egamberdieva et al. 2016), such as Pythium ultimum, Botrytis cinerea, Fusarium solani and Rhizoctonia solani (Jakobi et al. 1996; Kai et al. 2007). Antagonistic strains of S. rhizophila have been isolated from soil or plant rhizosphere; however the bacteria can also be found in marine environments. In a detection program performed by our laboratory to test marine microorganisms with potential application in biocontrol, the marine bacterium S. rhizophila was selected for its capacity to inhibit more than 90% of spore germination of C. gloeosporioides and the incidence of anthracnose and severity of lesions in more than 80 and 90%, respectively in mango fruit (Hernandez-Montiel et al. 2017). Despite S. rhizophila is a promising marine bacterium as biological control agent; its antagonistic mechanisms toward phytopathogens on fruit during postharvest period are still unknown. The aims of this study, was to determine in vitro the ability of S. rhizophila to inhibit C. gloeosporioides by volatile organic compounds (VOCs), lytic enzymes, siderophores, competition for nutrients, and quantify the reduce of anthracnose in mangoes.

Materials and methods

Fruit

Mangoes (M. indica, cv. Ataulfo) were harvested when they reached commercial maturity from an orchard in San Jose del Cabo, Baja California Sur, Mexico. Mangoes were selected for uniformity of size, ripeness, and absence of apparent injury or infection.

Phytopathogen and marine bacterium

Colletotrichum gloeosporioides and the marine bacterium S. rhizophila were obtained from the Phytopathology Laboratory, CIBNOR. Fungal spores were obtained from 10-day-old potato-dextrose-agar (PDA) cultures incubated at 25 °C, and the marine bacterium was cultivated in tryptic soy broth (TSB) at 27 °C for 12 h on a rotary shaker at 100 rpm. The concentration of the fungus was determined with a hematocytometer, and cell suspension of S. rhizophila was adjusted using an UV/Vis spectrophotometer at 660 nm and absorbance of 1.

Lytic enzymes activity

Fungal cell wall

The cell wall of C. gloeosporioides was obtained as indicted by Hernandez-Montiel et al. (2018). Briefly, C. gloeosporioides was cultured in a rotary shaker with yeast extract sucrose for 2 weeks at 25 °C, centrifuged 20 min at 8000 rpm, supernatant discarded and product was washed with water distilled and sterile, and left to dried in oven at 48 h, 60 °C.

In vitro culture of S. rhizophila with cell wall of C. gloeosporioides

The marine bacterium was cultivated in mineral salt medium (MSM) supplemented with 1 mg ml−1 of fungal cell wall and incubated at 25 °C for 15 days on a rotary shaker at 100 rpm. The supernatant was collected to determinate β-1,3-glucanase and chitinase activity.

To determine β-1,3-glucanase

β-1,3-Glucanase activity was detected using laminarin as indicated by Hernandez-Montiel et al. (2018) in triplicate for each treatment and carried two times. Briefly, the kit used for measuring the release of glucose was Randox Glucose (GOD-PAP) at pH 5 (37 °C).

To determine chitinase

The enzyme kit (No. CS0980, SIGMA) was used to assess the activities of β-N-acetylglucosaminidase, chitobiosidase and endochitinase according to the kit instructions and conducted twice with 3 replicates as specified by Hernandez-Montiel et al. (2018). Absorbance was measured at 405 nm, where one unit (IU) of chitinase was defined as the generation of one μmol of p-nitrophenol/min at a pH 4.8 at a temperature of 37 °C.

Activity of the marine bacterium volatile compounds against C. gloeosporioides

In vitro antagonistic assay

The experimental assay was based on a dual culture method as proposed by Rouissi et al. (2013) where antagonistic activity of the S. rhizophila VOCs against pathogenic fungus was tested. A plug of target fungus was placed in the center of Petri dishes with tryptic soy agar (TSA). At the same time, 30 μl of S. rhizophila (1 × 108 cells ml−1) were streaked in other dishes. Each inoculated plate was placed mouth-to-mouth, sealed (parafilm) and incubated at 25 °C for 7 days. Growth diameter of C. gloeosporioides was quantified (mm), and radial growth reduction was calculated. The control treatment was represented by the Petri dishes inoculated only with C. gloeosporioides. There were ten replicates for each treatment, and the experiment was done twice.

In vivo antagonistic assay

Mangoes were placed on plastic trays, which contained a thin layer of TSA (250 ml) in the bottom inoculated 2 days before with 500 μl of a suspension of 1 × 108 cells ml−1 of S. rhizophila and incubated at 25 °C. To avoid direct contact and possible contaminations of the fruit with the substrate, they were separated using a sterile grid. Two 1-mm lesions in depth were performed in each fruit with a sterile scalper, and each wound was deposited with 20 μl of a suspension of 1 × 104 spores ml−1 of C. gloeosporioides. The trays were sealed immediately with parafilm.

The control treatment was a group of inoculated fruit only with phytopathogen and stored on trays at 28 °C for 7 days. Disease incidence (%) and lesion diameter (cm) were quantified after 7 days of incubation. The experimental design was completely randomized; the sample unit consisted of six boxes (containing three fruit with two wounds each) per treatment, and the experiment was done twice.

Siderophore production

Siderophore production by S. rhizophila was inoculated on chrome azurol S (CAS) agar Petri dishes and incubated at room temperature for 24 h (Schwyn and Neilands 1987). The formation of bright yellowish fluorescent color zone by the culture in the medium indicated siderophore production (Teintze et al. 1981).

Competition for carbohydrates

A total of 100 μl of S. rhizophila (1 × 108 cells ml−1) and 100 μl of the C. gloeosporioides (1 × 104 spores ml−1) were mixed in 5 ml of sterile mango juice (SMJ) (90% v v−1 mango juice and 10% distilled water), incubated at 25 °C for 24 h on a rotary shaker at 150 rpm to calculated saccharose (Bruner 1964), fructose (Taylor 1995), and glucose (Barham and Trinder 1972) as detailed by Hernandez-Montiel et al. (2018). There were three replicates for each treatment, and the experiment was done twice.

Effect of different concentrations of S. rhizophila on control of C. gloeosporioides in mango

All fruits were surface-disinfected with sodium hypochlorite at 2% (v v−1) for three min. Two artificial wound of 1 mm in depth were made with a sterile scalpel. An aliquots of 10 μl of S. rhizophila (1 × 104, 1 × 106, 1 × 108 cells ml−1) was pipetted into each wound. Mangoes were left to dry for 2 h; then each lesion was inoculated with 20 μl of a spore suspension (1 × 104 spores ml−1) of C. gloeosporioides. A group of fruit was inoculated with the phytopathogenic fungus and treated with synthetic fungicide (Tecto 60) at a concentration of 1000 ppm. Another group was inoculated only with C. gloeosporioides. The fruit were placed on plastic trays at 28 °C and 90% of RH and after 7 days disease progression was quantified. The experimental design was completely randomized, consisting of three replicates of five fruits per replicate for treatment, and the experiment was done twice.

Data analysis

The data were analyzed by one-way analysis of variance (ANOVA), and the post hoc LSD Fisher test (p < 0.05) was used for separation of means. Prior to the analysis of variance, percentages were arcsine-square-root converted.

Results

Enzyme production of the marine bacterium

The marine bacterium S. rhizophila showed a high lytic activity, 200 IU ml−1 of β-1,3-glucanase and 77 IU ml−1 for chitinase enzyme was measured.

Inhibition of C. gloeosporioides by volatile organic compounds

The results showed in vitro and in vivo inhibition of C. gloeosporioides by the marine bacterium S. rhizophila VOCs production (Fig. 1a, b). With respect to the fungal radial growth, a significant reduction of 55% was quantified with the marine bacterium in the dual cultivations. The results of the in vivo assay corroborated the in vitro antagonistic effect of the VOCs produced by S. rhizophila toward C. gloeosporioides, significantly reducing disease incidence (90%) and lesion diameter (80%) caused by anthracnose fruit.

Fig. 1.

Fig. 1

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In vitro inhibition of C. gloeosporioides by VOCs of S. rhizophila. a In vitro antagonism, b in vivo Antagonism. For a, the experiment consisted of ten replicates per treatment and the Petri dishes were incuated at 25 °C for 7 days. For b, the experiment consisted of six boxes (containing three fruit with two wounds each) per treatment, and the fruits were incubated at 28 °C for 7 days. Values followed by different letters were significantly different according to the post hoc LSD Fisher test (p < 0.05)

Siderophore

The formation of a brilliant fluorescent yellow area on the plates with CAS inoculated with the marine bacterium indicated the qualitative production of siderophores (Fig. 2).

Fig. 2.

Fig. 2

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Production of siderophores by S. rhizophila in chrome azurol S medium (CAS). a Petri dish without the marine bacterium. b Presence of a fluorescent yellow zone around the colony of S. rhizophila, indicative of positive for the production of siderophores (Teintze et al. 1981)

Carbohydrate content

The content of saccharose, glucose and fructose were significantly lower when C. gloeosporioides and S. rhizophila were inoculated at the same time in SMJ when compared with the treatments individually inoculated with each microorganism (Table 1). A reduction of 87% in saccharose, 52% in glucose and 69% in fructose contained in SMJ inoculated with the phytopathogen fungus and the marine bacterium was quantified. Competence for carbon sources inhibited at 91% spore germination of phytopathogen fungus in the presence of S. rhizophila.

Table 1.

Content of carbohydrates in medium sterile mango juice (SMJ) inoculated with the marine bacterium and C. gloeosporioides

Treatmentx Carbohydrate rate (mg ml−1)v
Saccharose Glucose Fructose
C. gloeosporioidesy 7.2 b 10.5 b 8.1 b
S. rhizophilaz 5.4 c 8.7 c 5.7 c
C. gloeosporioides + S. rhizophila 1.2 d 5.8 d 3.2 d
SMJ 10.6 a 12.1 a 10.3 a
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XThe microorganisms were inoculated in Falcon tube that contained 5 ml of SMJ (90% v v−1 mango juice and 10% distilled water)

YThe phytopathogen fungus was inoculated with 1 × 104 spores ml−1

ZThe marine bacterium was inoculated with 1 × 108 cells ml−1

VValues are the means of carbohydrate rate of three replicates after 24 h at 25 °C. Means within the same column that are followed by different letters are significantly different (p < 0.05) according to the post hoc LSD Fisher

Mangoes protection

Although at different levels, all tested different dosage of S. rhizophila on papaya fruit significantly decreased the disease incidence and lesion diameter compared with fruit treated with the synthetic fungicide and control with only C. gloeosporioides (Fig. 3). The application of a high cell dose (1 × 108 cells ml−1) of the marine bacterium reduced 95% of anthracnose presence on mango and decreased 85% of lesion diameter. All doses of the marine bacterium applied on fruit were more effective in anthracnose control than the protection exerted by a commercial synthetic fungicide used by mango packing companies against C. gloeosporioides.

Fig. 3.

Fig. 3

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Biocontrol of anthracnose caused by C. gloeosporioides by S. rhizophila in mango fruits cv. Ataulfo. The experiment consisted of three replicates of five fruits per replicate for treatment. Values followed by different letters were significantly different according to the post hoc LSD Fisher test (p < 0.05)

Discussion

This study observed that the application of different cell doses of the marine bacterium S. rhizophila were efficient in postharvest control of anthracnose caused by C. gloeosporioides in mango cv. Ataulfo, going beyond the protector effect of the synthetic fungicide. The application of bacteria as biological control agents has been considered one of the most promising alternatives to protect fruit against infection by phytopathogens, minimizing the use of synthetic fungicides (Di Francesco et al. 2016).

Diverse mechanisms of antagonistic bacteria have been involved in plant phytopathogen suppression. In our study, the marine bacterium S. rhizophila inhibited vitro C. gloeosporioides growth in vitro and on fruit through the production of VOCs. Moreover, the production of extracellular enzymes involved in the hydrolysis of fungal cell walls, by the antagonistic bacteria was also demonstrated. Previous studies have reported the capacity of S. rhizophila isolated from plant rhizosphere to antagonize different pathogens in vitro, such as Verticillium dahliae, Pythium ultimum Rhizoctonia solani, Botrytis cinerea, Sclerotinia sclerotiorum, among others (Jakobi et al. 1996; Kai et al. 2007) and from marine isolations for biological control of anthracnose in mango (Hernandez-Montiel et al. 2017). Nonetheless, this is the first study that describes the antagonistic mechanisms of the marine bacterium S. rhizophila toward C. gloeosporioides.

Hydrolytic enzyme production is one of the antagonistic mechanisms used by bacteria to inhibit phytopathogen growth (Subbanna et al. 2018). The detection of protease (Vida et al. 2017), β-1,3-glucanase (Bibi et al. 2012) and chitinase (Afzal et al. 2015) have already been reported for S. rhizophila; however, detection tests of these enzymes have been based on changes in color or halo formation in the culture medium used. In our study, we detected the production of β-1,3-glucanase and chitinase by the marine bacteria in culture medium containing the phytopathogen cell walls as the only carbon source, which demonstrated the induction of the hydrolytic enzymes in presence of the phytopathogen (Ashwini and Srividya 2014). The enzymes β-1,3-glucanase and quitinase hydrolize specifically the glucan and chitin present in fungal cell walls, producing oligosaccharides of smaller size that are used as energy for antagonist microorganisms (Liu et al. 2017).

VOCs production by S. rhizophila has already been identified as an antagonist mechanism toward phytopathogens, mainly by the production of β-phyenylethanol and dodecanal although there are still different VOCs produced by bacteria that have not been identified yet (Kai et al. 2007; Chandra 2017). Particularly in the case of β-feniletanol, its antimicrobial effects have been reported to alter permeability of the plasma membrane, modify amino acid and sugar transport system and inhibit macromolecular synthesis, inhibiting phytopathogen growth (Etschmann et al. 2002).

Competence for space and nutrients is another antagonist mechanism that bacteria express to limit phytopathogen growth (Di Francesco et al. 2016). Inhibition on spore germination of C. gloeosporioides by S. rhizophila is related with low content of saccharose, glucose and fructose in the medium of sterile mango juice (SMJ) inoculated with both microorganisms. The bacterium limits the content of the necessary carbon sources to initiate spore germination by having a greater growth rate than phytopathogens (Laslo et al. 2012). In the competence of the host between the marine bacterium and the phytopathogen, lesser presence of anthracnose was observed when different cell doses of S. rhizophila were applied increasingly on mangoes, providing a greater protection of the fruit as the antagonist dose increased (Wang et al. 2010).

The detection in vitro of siderophores by S. rhizophila encourages further studies to determine their effect on biological control of diseases caused by phytopathogens. Siderophores are iron chelators of low molecular weight whose fundamental role is bacterial antagonisms toward phytopathogen fungi by limiting iron content in the environment, which is an element required for fungal spores germination and consequently for the beginning of mycelial growth (Yu et al. 2017; Veldman et al. 2018).

In conclusion, this study showed that the application of different cell doses of the marine bacterium S. rhizophila on mango cv. Ataulfo decreased significantly the incidence of anthracnose caused by C. gloeosporioides. The antifungal effect of the marine bacterium involved the production of hydrolytic enzymes, VOCs, siderophore, competing for space and nutrients. The treatment of the mangoes with S. rhizophila was more efficient against anthracnose than the application of synthetic fungicides, making the marine bacterium a more effective, economic and environmentally safe alternative for the control of C. gloeosporioides. Further studies shall determine the production of biofilms, identification of siderophore and VOCs of S. rhizophila, and resistance induction of the host.

Acknowledgements

This work was supported financially by a Grant Project from Problemas Nacionales 2015-01-352 of CONACYT (Consejo Nacional de Ciencia y Tecnología, México). We also acknowledge Ernesto Diaz and R. Galicia for their technical support, and Dr. Michael Cordoba a native English speaking editor for editing the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

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