Debaryomyces nepalensis reduces fungal decay by affecting the postharvest microbiome during jujube storage

https://doi.org/10.1016/j.ijfoodmicro.2022.109866Get rights and content

Highlights

  • D. nepalensis delayed fungal decay and maintained the quality of jujube.

  • D. nepalensis affected the diversity and composition of the jujube microbiome.

  • The abundance of pathogenic fungi was reduced by D. nepalensis.

  • The abundance of D. nepalensis was associated with the quality of jujube fruit.

Abstract

Microbial antagonists are effective and environmentally friendly in controlling postharvest diseases of fruit. The present study investigated the influence of D. nepalensis on epiphytic microbiome and postharvest decay of jujube. Results showed that D. nepalensis notably reduced fungal decay, maintained the fruit firmness and delayed discoloration. The epiphytic microbiome revealed that D. nepalensis changed the fungal communities, but few influence on bacterial communities were observed. D. nepalensis, as the dominant population in the treatment group, decreased the abundance of pathogenic fungi of Alternaria, Penicillium, Fusarium and Botrytis, while increased the beneficial bacteria of Pantoea. The canonical correspondence analysis revealed that Debaryomyces was negatively correlated with the decay rate, whereas Penicillium, Acremonium, Rhodosporidiobolus and Hansfordia were positively correlated. In conclusion, D. nepalensis altered the successional process of fungal and bacterial communities to reduce the decay rate of jujube during storage.

Introduction

Jujube is a good source of vitamins, phenolics, flavonoids, minerals and other nutrients, that is favored by a large number of consumers (Gao et al., 2013). But fresh jujubes are very susceptible to postharvest pathogenic infections, causing huge postharvest losses each year (Zhang et al., 2021b). Currently, the applications of chemicals are the most common and effective strategies to prevent the postharvest diseases of jujube (Estiarte et al., 2017). But in recent decades, antagonistic yeasts have attracted frequent attentions as a promising alternative to chemical agents and fungicides, and their antagonistic mechanisms include antifungal metabolites, competition for space and nutrients, biofilm formation, etc. Recently, a novel mechanism has been proposed through which the antagonistic yeast remodels and interacts with the epiphytic communities on the surface of fruits and vegetables, which are neglected in most previous studies (Wisniewski and Droby, 2019; Zhang et al., 2021a).

Fruit microbial community structure refers to the microbial species closely related to the host and their relative abundance in the community. Several reviews have emphasized the importance of microbiome on postharvest control (Droby et al., 2009; Wisniewski and Droby, 2019; Zhang et al., 2021b; Zhang et al., 2020). The classification and metabolism of plant-related microbiome can be directly related to the presence of nutrients in specific parts of the plant, and the epiphytic communities on the surface of fruits and vegetables have a significant influence on fruit quality, nutrition and disease resistance (Korlevic et al., 2021). For example, the carbohydrate metabolism and ripening process of watermelon fruit can be significantly influenced by microbiome (Saminathan et al., 2018). Similarly, the peel color of mango can be affected by fungal and bacterial communities (Diskin et al., 2017), and the changes in microbial abundances can affect the storage rot of sugar beets (Kusstatscher et al., 2019). Besides, study on rhizosphere microbiome has shown that healthy samples have more robust rhizosphere and internal networks that contain more beneficial bacteria associated with antibiotic production, pollution degradation, nutrient acquisition (Yin et al., 2020).

Postharvest preservation processing in turn can also influence the microbial communities. For example, gas regulation (Lampert et al., 2017), transportation and cold storage (Chen et al., 2019) can change the microbial structure during postharvest storage. Antagonistic microorganisms treatment may also significantly change the epiphytic community, and then improve the fruit quality. As presented in a previous study, Lactobacillus delbrueckii subsp. bulgaricus F17 and Leuconostoc lactis H52 reduce the rot rate of strawberry fruits by altering the microbial community structure (Fang et al., 2019). As an antagonist yeast, Pichia kudriavzevii could effectively control postharvest diseases of cherry tomatoes, even though P. kudriavzevii was not the dominant population during storage, indicating the changes on microbial community may be beneficial for the fruits (Liu et al., 2020).The results of these studies suggest that a deeper understanding of the changes in the epiphytic microbial community can be helpful to better explore the mechanism of yeast, and provide new solutions for the prevention and control of postharvest diseases on fruits and vegetables.

D. nepalensis is an antagonist yeast that could effectively control postharvest anthracnose of mango fruit and black spot rot of jujube by biofilm production and compete for nutrient and space with the pathogen. In this study, an yeast D. nepalensis isolated from jujube leaves was utilized on jujube fruit to control postharvest rot decay. The epiphytic microbial community was also explored to reveal the possible mechanisms therein.

Section snippets

Antagonistic yeast

The yeasts utilized in the study were isolated from the surface of jujube leaves and identified as D. nepalensis based on physiological analysis, biochemical properties, as well as the internal transcribed spacer (ITS) ribosomal DNA (rDNA) region sequence (GenBank accession number: KY694999). Before use, the yeast was activated on Yeast Extract Peptone Dextrose Medium (YEPD) plate for two generations, and then incubated in YEPD liquid medium at 28 °C with shaking at 200 rpm. The cells were

Decay incidence

The effects of D. nepalensis on the decay rate of jujube was presented in Fig. 1. At 20 d of storage, the decay rate of D. nepalensis treated group was only 2 %, which was much lower than that in control group at 14 % (Fig. 1). At the end of storage (40 d), the decay rate in the control group was about 34 %, but it was reduced by 20 % when treated with D. nepalensis. These results showed that D. nepalensis treatment can significantly reduce postharvest rot rate and effectively control

Discussion

Plants have a highly diverse and dynamic microbial community which plays an important role in the health and quality of host (Mitter et al., 2019). In recent years, antagonistic yeasts were found to be effective agents to control the postharvest decay of fruit (Cabanas et al., 2020; Delali et al., 2021; Mukherjee et al., 2020). The antifungal mechanisms of these yeast include formation of biofilms, competition for space and nutrition, as well as other mechanisms (Wang et al., 2020). However,

Conclusions

In this study, D. nepalensis was effective to decrease postharvest rot of jujube fruit and maintain fruit quality. Fungal community composition was more sensitive to the D. nepalensis treatment than bacterial communities. Debaryomyces, as the dominant genera, significantly decreased the abundance of pathogenic fungi in jujube fruit. Potentially beneficial bacteria, such as Pantoea, were found on the fruit surface, and its abundance in D. nepalensis group was significantly higher than that in

Declaration of competing interest

No conflict of interest exits in the submission of this manuscript, and manuscript is approved by all authors for publication. Neither the entire paper nor any part of its content has been published or has been accepted elsewhere.

Acknowledgment

This research was supported by the National Key Research and Development Program of China (2019YFD1002300).

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