Effects of ultraviolet irradiation on quality and bacterial diversity of fresh-cut cabbage during storage

Abstract

The effect of ultraviolet C (UV-C) radiation on the physicochemical properties and the bacterial diversity of fresh-cut cabbage was investigated over 12 days of storage at 5 °C. The color index (L*, a* and b*), decrease in weight, and content of soluble sugar, chlorophyll, ascorbic acid, total phenol, and malondialdehyde were measured. The structure of the bacterial community was also clarified by high-throughput sequencing analysis. After irradiation, the weight loss of fresh-cut cabbage during storage was reduced, and the content of antioxidant-related components, such as total phenols, ascorbic acid, and malondialdehyde, was increased. The results showed that the dominant phylum of bacteria in fresh-cut cabbage was Proteobacteria, and the dominant genus was Pseudomonas. A β-diversity analysis showed that the composition of the bacterial community of the irradiated and control treatments was different.

Introduction

Cabbage (Brassica oleracea var. capitata) belongs to the cruciferous family of vegetables, and is rich in nutrients, such as vitamins and dietary fiber, as well as total phenol, glucosinolates, and anti-ulcer agents (vitamin U) that can accelerate wound recovery. Long term consumption of cabbage can also prevent hypertension, enhance immunity, prevent cancer, and act as an antioxidant (Ağagündüz et al., 2022; Carvalho et al., 2011; Favela-González et al., 2020). Cabbage originates along the Mediterranean coast; however, due to its rich nutritional value, cold resistance, strong adaptability, and ease of storage and transportation, it is produced and consumed globally (Chrysargyris et al., 2019).

In a fast-paced lifestyle, consumers tend to prefer a fast and healthy diet. Salads or minimally processed vegetables have the advantages of freshness, convenience, and nutrition, which has promoted the rapid development of the fresh-cut market (Ragaert et al., 2004). However, fresh-cut vegetables can be damaged by mechanical processing, and direct contact between wounds and air can accelerate the evaporation of water in tissue cells, and promote juice leakage, enzymatic browning, and rapid proliferation of microorganisms, leading to spoilage, softening, and browning (Fukuyama et al., 2009). They may also be contaminated by foodborne pathogens, leading to food poisoning (Kim and Min, 2021). The short shelf life of vegetables prepared in this manner greatly restricts the development of the fresh-cut fruit and vegetable industries. The shelf life of fresh-cut cabbage that is sold in supermarkets is typically only 2–4 days, and it is necessary to extend the shelf life to increase economic value and reduce waste. Therefore, it is particularly important to develop safe and efficient fresh-cut fruit and vegetable preservation technologies.

The demand for fresh-cut vegetables and salads is increasing, and they are mostly sold in plastic bags or containers in supermarkets. At present, most research has focused on the treatment of fresh-cut vegetables using non thermal processing techniques, such as refrigeration, acidic electrolytic water treatment, and modified atmosphere packaging, which can reduce the adverse effects of heat treatment on vegetables and extend their shelf life (Conte et al., 2011; Huang et al., 2021; Jeon et al., 2023; Naka et al., 2020). However, these preservation methods may promote the formation of chemical residues, increase production costs, and have other associated other drawbacks. Irradiation by light in the ultraviolet-C region is a widely used physical, non-thermal preservation method. UV-C destroys microbial DNA and promotes cross-linking between thymine and cytosine, hindering DNA transcription and replication, and leading to loss of function and the death of microbial cells. The method has the advantages of not leaving any residues, low cost, safety, and sterilization (Chun et al., 2010; Franz et al., 2009; Park et al., 2020). UV-C irradiation has been shown to inhibit vegetable decay, increase tomato hardness, and enhance antioxidant activity (Choi et al., 2015; Mansourbahmani et al., 2017b). Moreover, UV-C treatment can reduce amylase activity and browning of fresh-cut lilies (Huang et al., 2017), as well as destroy the virus that causes COVID-2019 (Gokmen and Ismail, 2020). In recent years, numerous studies have shown that applying appropriate doses of UV-C radiation can improve the antioxidant activity of postharvest fruits and vegetables (Erkan et al., 2008; Maurer et al., 2017; Zhang et al., 2016). However, there is limited information on the effects of UV-C irradiation on the storage quality and microorganisms of fresh-cut cabbage. Hence, this study aimed to investigate the effect of different storage times at 5 °C on the quality and bacterial community of fresh-cut cabbage treated with UV-C irradiation.

Materials and Methods

Experimental materials  Cabbage obtained from a retail supermarket in Kagoshima city was used in this study. A couple of outer leaves were removed and the shredded cabbage was prepared by slicing into 1 cm slices using a knife. Samples were rinsed using sterilized deionized water, and excess water was removed using a salad spinner. The prepared sample was placed in the refrigerator until used for the irradiation test. Two 253.7 nm UV-C lamp tubes (GL6, Sankyo Denki. Co., Ltd., Japan) were positioned above the samples in the refrigerator. A UV light meter (UVC-254, Lutron Asuka Co., Ltd., Japan) was placed in the same location as the sample to ensure that the irradiation intensity was the same in each trial. After 5 min of irradiation, samples were turned over and irradiated for a further 5 min. Total irradiation energy for 10 min was 1.05 kJ/m². No significant change was observed within 10 min of irradiation; however, leaves showed severe browning after 10 min. Therefore, a 10 min irradiation period was considered to be sufficient for assessing fresh-cut cabbage in preliminary experiments. The treated sample was sealed and packaged in PE(Polyethylene) bags and stored in a refrigerator at 5 °C. On days 0, 3, 6, 9, and 12, samples were collected for analysis of the following physicochemical parameters; non-irradiated samples were used as control samples.

Physicochemical analysis  The color (L*, a*, and b* values) of the analytical sample was measured using a color reader (CR-20, Konica-Minolta, INC., Japan). The weight changes of the samples were recorded during storage. The sugar content was measured as described in a previous study with minor modifications (Wang et al., 2022). 1.0 g of sample was homogenized with 10 mL of HCl (FUJIFILM Wako Pure Chemical Co., Osaka), and the filtrate was heated with boiling water for 10 min. 1.0 mL of extract was mixed with 1.0 mL of deionized water, 0.5 mL of anthrone-ethyl acetate and 5 mL of sulfuric acid in glass tube. After heating in the water bath, the absorbance at 620 nm was measured using a spectrophotometer (U-2900, Hitachi High Technologies Co., Tokyo). The spectrophotometer was also used to determine the chlorophyll content. Briefly, the chlorophyll was acetone-extracted from the sample and the absorbance was recorded at 652 nm. The ascorbic acid content was determined by a reflectometer (RQflex20, Merck KGaA, Darmstadt, Germany) according to the manufacturer’s instructions. The total phenol content of samples was determined by the Folin–Ciocalteu method with minor modifications, as described by Shi et al. (2019), and a calibration curve was created using gallic acid (0–60 μg/mL). The malondialdehyde content in the samples was determined by a spectrophotometric method based on the thiobarbituric acid reaction.

Extraction of microorganisms  50 g of cabbage sample was frozen in liquid nitrogen and homogenized with bacterial cell extraction (BCE) buffer (50 mM of Tris-HCl at pH 7.5 and 1% of Triton X-100) and 2-mercaptoethanol using a mixer (TMV1000, TESCOM, Tokyo). The homogenized sample was filtered through cotton gauze to remove any residue, and then centrifuged (500 ×g for 5 min, 10 °C) to obtain a supernatant. The remained bacterial cell in the centrifuged precipitate was completely suspended in BCE buffer, and centrifuged (8000 ×g for 10 min, 10 °C) to collect the bacterial cell fraction. The precipitated extract obtained was suspended in sterile distilled water, and the DNA concentration was measured with a nanophotometer (C40, IMPLEN GmbH, München, German). The DNA from the sample was stored in a −20 °C freezer until it was used for high-throughput sequencing.

High-throughput sequencing  A two-step tailed PCR was performed. Bacterial 16S rRNA gene amplicons were amplified using primers of 341F (CCTACGGGNGGC WGCAG) and 805 R (GACTACHVGGGTATCTAATCC), targeting the V3–V4 specific region. The thermocycling conditions consisted of an initial denaturation step at 94 °C for 2 min, followed by 30 cycles at 98 °C for 10 s, 55 °C for 30 s and 68 °C for 30 s, then a final elongation step at 68 °C for 7 min. The second PCR consisted of an initial denaturation step at 94 °C for 2 min, followed by 10 cycles at 98 °C for 10 s, 60 °C for 30 s and 68 °C for 30 s, then a final elongation step at 68 °C for 2 min. All amplified PCR products were purified, and sequencing was performed using an Illumina MiSeq system (Illumina, Inc.). Sequencing analysis was outsourced to Bioengineering Lab. Co., Ltd. (Kanagawa, Japan).

Bioinformatics analysis  Chimeric sequences were discarded using the DADA2 plugin for QIIME2 (ver. 2023.5) and the representative sequence and amplicon sequence variant (ASV) tables were output. Good quality reads were clustered into operational taxonomic units (OTUs) at a 97 % similarity level using the Greengene (ver. 13.8) reference sequence database.

Statistical analysis  The experimental results of the physicochemical analyses were presented as the mean ± standard deviation. Origin 2018 and SPASS 25 software were used for the analysis of significance and statistical results. Statistical differences were evaluated using Duncan tests (p < 0.05). Principal coordinate analysis (PCoA) was completed using the Wekemo Bioincloudⁱ⁾.

Results and Discussion

Color  Color is an important factor affecting the quality of fresh-cut cabbage. The color parameters for the irradiation and control groups are listed in Table 1. The L* value for the irradiation group decreased with increasing storage period as the surface of the samples turned darker. The L* value for the control group was directly correlated with storage duration. This result is similar to that for red cabbage (Zhang et al., 2016). The a* values for both the control group and the irradiation group increased over time. Low-intensity irradiation caused a delay in the development of a red color (Pinheiro et al., 2014; Liu et al., 2009). After 6 days at 5°C, a significant (p < 0.05) decrease was observed in the lowest b* value (29.13) for the control group. At the end of storage, the control group showed an increase in yellowness. The b* value for the irradiation group showed a trend of first increasing and then decreasing, reaching its highest value (27.37 ± 0.35) at day 6.

Table 1. Effect of irradiation treatment on the color of fresh-cut cabbage

Group	Time/day	L*	a*	b*
	0	69.40 ± 0.35a	−7.35 ± 0.07a	30.43 ± 0.25ab
	3	69.65 ± 0.07ab	−7.00 ± 0.14b	29.7 ± 0.22cd
Control	6	70.10 ± 0.26b	−7.00 ± 0.14b	29.13 ± 0.33d
	9	70.05 ± 0.21b	−7.07 ± 0.12b	30.08 ± 0.60bc
	12	71.00 ± 0.30c	−6.93 ± 0.06b	30.80 ± 0.20a
	3	69.35 ± 0.40a	−6.15 ± 0.21ab	25.55 ± 0.65a
	6	68.70 ± 0.18ab	−6.40 ± 0.10a	27.37 ± 0.35c
Irradiation	9	68.00 ± 0.14b	−6.05 ± 0.07b	27.13 ± 0.15c
	12	67.13 ± 0.59c	−5.70 ± 0.10c	26.26 ± 0.35b

Different letters (a, b, and c) indicate significant differences (p < 0.05).

Weight loss  The weight loss ratio for the fresh-cut cabbage in the control and irradiation groups increased during storage (Fig. 1). The weight loss ratio was lower in the irradiation group than in the control group during storage. The ratio for the control group was 9 % on the 6th day, while the irradiation group reached a similar ratio on the 12th day. For fresh tomato, it has been reported that UV-C treatment also influenced the weight loss ratio significantly (Pinheiro et al., 2014). Plants lose moisture during storage due to respiration and transpiration reactions, resulting in a decrease in their weight. However, appropriate irradiation treatment could suppress respiratory effects (Rivera et al., 2013).

Each data represents the mean ± SD of three independent experiments. Different letters (a, b and c) of two groups indicate significant differences (p < 0.05). The same below.

Fig. 1

Effects of irradiation on weight loss during storage.

Soluble sugar  The changes in soluble sugar content are shown in Fig. 2. The soluble sugar content in the control and irradiation groups was initially 35.46 mg/g. However, it decreased significantly after storage, and the results were similar to those of a study on storage (Chen et al., 1983). On the 12th day of storage, the soluble sugar content in the irradiation group was slightly higher than that in the control group. Previous studies have shown that UV-C treatment suppressed starch degradation and total soluble sugar by inhibiting α-amylase, β-amylase and starch phosphorylase (Huang et al., 2017). Similar results were also reported in broccoli and potato (Lemoine et al., 2007; Herman et al., 2016).

Fig. 2

Effects of irradiation on soluble sugar content during storage.

Chlorophyll  Chlorophyll, which is the most widely distributed pigment in green vegetables, is mainly involved in photosynthesis. Changes in chlorophyll content affect the color and quality of vegetables, causing yellowing. Fig. 3 shows the changes in chlorophyll content during storage in the control and irradiation groups. Chlorophyll content in both irradiation groups and the control groups decreased after storage, especially at 3 days of storage, when a significant decrease was observed. The changes in the irradiation group and the control group were similar. However, the dose of irradiation used in our study did not achieve the effect of inhibiting chlorophyll degradation, as reported previously (Liao et al., 2016). This was likely because different dose of irradiation had positive or negative effects on chlorophyll content (Martínez-Hernández et al., 2011; Wen et al., 2019).

Fig. 3

Effects of irradiation on chlorophyll content during storage.

Ascorbic acid  Ascorbic acid is a powerful antioxidant that is widely found in fruits and vegetables. Fig. 4. shows the change in ascorbic acid content in the control and irradiation groups during storage. The ascorbic acid content in each group decreased to different levels in the latter stages of storage. The ascorbic acid content in the irradiation group was higher than that in the control group on the 9th and 12th day of storage. The decrease in ascorbic acid might be caused by adverse biochemical reactions related to incisions caused by cabbage processing. UV-C promotes an increase in ascorbic acid peroxidase activity (Xu et al., 2016), so the ascorbic acid content in the irradiation group was higher than that in the control group in the later stage of storage. These data also confirmed previous studies which indicated that the ascorbic acid content had a positive impact through irradiation treatment (Abdipour et al., 2019).

Fig. 4

Effects of irradiation on ascorbic acid content during storage.

Total phenol  Total phenols act as antioxidants in fruits and vegetables like ascorbic acid, preventing cancer and clearing oxygen free radicals (Zhang et al., 2016). The total phenol content of the irradiation group initially decreased slightly, and then increased significantly to 13.09 mg/g on the 12th day (Fig. 5). The total phenol content of the control group showed a decreasing trend, and decreased to 11.03 mg/g in the latter storage period. Irradiation has a significant impact on the total phenol content compared to the control group (Alothman et al., 2009; González-Villagra et al., 2020). Irradiation has been proven to induce the phenylpropanoid metabolic pathway, significantly increasing the activity of key enzymes, such as phenylalanine ammonia lyase and promoting the synthesis and accumulation of secondary metabolites such as total phenols and flavonoids (Liu et al., 2018; Mansourbahmani et al., 2017a; Rivera-Pastrana et al., 2014). Therefore, increasing the total phenol content of vegetables through irradiation has considerable benefits for vegetable quality, human health, and the food industry.

Fig. 5

Effects of irradiation on total phenol content during storage.

Malondialdehyde  Generally, the increase in malondialdehyde content is a manifestation of increased membrane lipid peroxidation and membrane injury, which exacerbates aging. Therefore, it can be used as an important indicator to measure the oxidation of cells in fresh-cut fruits and vegetables. The effect of irradiation on the content of malondialdehyde is shown in Fig. 6. The content of malondialdehyde in both the irradiation group and the control group showed a decreasing trend during storage. At day 3 of storage, the rate of decrease in malondialdehyde in the control group slowed, while at day 6 of storage, the malondialdehyde in the irradiation group decreased to 6.94 nmol/g. The reason for the decrease in malondialdehyde content might be that the samples were stored in a low-temperature environment, which had a certain protective effect on cell membrane peroxidation, and irradiation could enhance that positive effect (Wang et al., 2017). Free radicals directly or indirectly stimulate cell membrane lipid peroxidation, leading to an increase in malondialdehyde content (Zhang et al., 2023). However, it is considered that appropriate doses of irradiation effectively avoided excessive stimulation of cell membrane lipid peroxidation processes. However, with the extension of storage time, the content of malondialdehyde in the irradiation group was significantly lower than that in the control group. Therefore, these results indicated that irradiation treatment is an effective approach to maintain antioxidant capacity.

Fig. 6

Effects of irradiation on malondialdehyde content during storage.

α-diversity analysis  The α-diversity, expresses bacterial species diversity in samples, and is also explained by Simpson’s, Shannon’s, and Chao1 indices. As shown in Table 2, according to the coverage index, the coverage ratio for each sample was greater than 99 %, indicating that the sequencing depth was sufficient and could well reflect the true situation of the sample microorganisms. The highest Chao1 was observed on the 12th day of irradiation in the control group, indicating a higher species richness in the latter stages of storage. However, the species in the control group were more abundant. Combining Shannon’s and Simpson’s indices, it can be concluded that the bacterial community diversity of the control group initially decreased and then increased during storage, while that in the irradiation group initially increased and then decreased. Finally, the bacterial community diversity of the irradiation group was lower than that of the control group. Based on these indices, it can be inferred that irradiation treatment affected the species richness and diversity of bacterial communities during the storage period for fresh-cut cabbage.

Table 2. Richness and diversity indices of bacterial communities in different groups

Group	Time/day	Simpson	Shannon	Chao1	Coverage/%
	0	0.91	4.35	60	99.99
Control	6	0.82	3.28	53	99.99
	12	0.88	3.81	68	99.99
Irradiation	6	0.93	4.71	73	99.99
	12	0.84	3.34	51	99.99

Analysis of bacterial species and abundance  To analyze the differences in bacterial communities at the phylum and genus levels, the column charts in Fig. 7 are shown with abundance as the vertical axis. At the level of the phylum, Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes were detected in both groups, but there were some differences in abundance. The most abundant phylum among all groups was Proteobacteria, with an abundance of over 94 %. On the 12th day of storage in the irradiation group, abundance reached 99 %, with 94.10 % on the sixth day of storage; the control group maintained a relatively high level. However, the experimental results indicated that irradiation treatment inhibited the growth of Proteobacteria during the initial storage period. Compared to gram-positive bacteria (Firmicutes, Actinobacteria), Bacteroidetes showed a more significant decrease after irradiation, which might be due to gram-positive bacteria having thicker peptidoglycan cell wall structure (Ahmed et al., 2022) and the ability to resist irradiation (Gholami and Etemadifar, 2015).

Fig. 7

Differences in bacterial communities at the phylum level.

Control-0, Control-6, and Control-12 represent the 0, 6, and 12 days in storage of the non-irradiated group, respectively. Irradiation-0, Irradiation-6, and Irradiation-12 represent the 0, 6, and 12 days in storage of the irradiation group, respectively. The same below.

The differences in bacterial communities among different groups during storage at the genus level are shown in Fig. 8. Pseudomonas, Agrobacterium, Roseomonas, Stenotrophomonas, Pantoea, Paenibacillus, and Rhodococcus were detected in all groups, but their abundance varied. Pseudomonas was most abundant in the control group (91.31 %) on day 6. Ragasová et al. (2020) also reported that after harvesting, the most prevalent bacterial genus in cabbage was Pseudomonas. The abundance of Pseudomonas decreased significantly after irradiation, but the abundance of Agrobacterium and Roseomonas increased. At the genus level, irradiation treatment had a significant impact on the main bacterial genera (Pseudomonas and Agrobacterium), and the composition of bacterial communities also underwent changes during storage. The non-significant decrease of the gram-positive Paenibacillus bacterium after irradiation also confirmed the discussion at the phylum level. Zeng et al. (2022) reported that the levels of microbiota in eluates of irradiated broccoli were variable.

Fig. 8

Differences in bacterial communities at the genus level.

β-diversity analysis  The bacterial communities of different groups and storage times were analyzed and a PCoA diagram was plotted (Fig. 9). The results of the PCoA analysis based on the Bray-Curtis distance algorithm indicated that bacterial communities were relatively similar and that the distances between the control groups on the 6th and 12th days of storage were relatively close. The control group (on the 6th and 12th day of storage) formed one group, also indicating that the bacterial community of fresh-cut cabbage may be affected by storage time, as samples from the same treatment have similar environmental conditions. However, there were significant differences in the bacterial community composition structure between the irradiated group stored for 12 days and other samples. The impact of irradiation might increase with prolonged storage time.

Fig. 9

Principal coordinate analysis of bacterial community among different storage duration with/without UV irradiation.

Conclusions

This study focused on exploring the impact of irradiation on fresh-cut cabbage and the quality changes during storage (0–12 days). The bacterial diversity in different samples was researched using high-throughput sequencing technology. Irradiation treatment reduced the L* value for fresh-cut cabbage. However, it significantly reduced the weight loss rate during storage. Irradiation played a positive role in maintaining the content of antioxidant components. At the phylum level, the dominant bacterial group in all samples was Proteobacteria, while at the genus level, Pseudomonas, Agrobacterium, and Roseomonas were the dominant genera. The results are considered helpful for better understanding of the bacterial community structure of fresh-cut cabbage, for controlling harmful bacterial taxa, and maintaining benevolent bacterial communities. It is considered that the research scope of this study was limited by the fact that only a single dose (1.05 kJ/m²) of UV-C was used. In the future, we aim to explore the effects of different doses of radiation on fresh-cut cabbage, as well as more specific changes in microbial communities during storage.

Acknowledgements  We thank all members of the team for their efforts. This research was supported by Kagoshima University in Japan and the China Scholarship Council.

Conflict of interest  There are no conflicts of interest to declare.

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• i) https://www.bioincloud.tech/task-meta (Sep 08, 2023) (in Chinese)