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. 2021 Jun 7;30(6):843–851. doi: 10.1007/s10068-021-00920-0

Characteristics on host specificity, infection, and temperature stability of Weissella phages from watery kimchi

Soomin Lee 1, Jong-Hyun Park 1,✉
PMCID: PMC8225752  PMID: 34249390

Abstract

Three bacteriophages (phage), ΦWC53, ΦWC54, and ΦWC56, of Weissella were isolated from watery kimchi and characterized. ΦWC53 belonged to Siphoviridae and ΦWC54 and ΦWC56 belonged to Myoviridae family. By one-step growth, the burst sizes were 5–260 particles/infected cells and the latent periods were 20–45 min. The phages infected Weissella spp., Leuconostoc mesenteroides, and Lactobacillus spp., differently by showing clear or turbid plaques. The phage adsorption rates on lactic acid bacteria were high on Weissella and low on Leuconostoc and Lactobacillus. However, the adsorption of ΦWC53 occurred variously among Weissella spp. and Weissella host grew well in the liquid culture without lysis after challenging by ΦWC53. Tolerances of these phages to temperature showed more various than those to pH. ΦWC53 was stable at 7 °C and 30 °C, but ΦWC54 and ΦWC56 were stable only at 7 °C. Therefore, three Weissella phages belonged to the different families and indicated diverse infection patterns on Weissella, Leuconostoc, and Lactobacillus with various stabilities for pH and temperature.

Keywords: Weissella, Bacteriophage, Plaque, Temperature stability, Kimchi fermentation

Introduction

Kimchi, a traditional Korean food, is produced by fermenting vegetables with lactic acid bacteria (LAB). Kimchi is mainly composed of cabbage and radish with garlic, onion, ginger, salt, and red pepper (Jung and Lee, 2014). The taste of kimchi is related to the components of the metabolites of LAB, such as organic acids, carbohydrates, amino acids, and other products that influence microbial communities during fermentation (Choi et al., 2002; Ha et al., 1989). Bacteria-infecting bacteriophages (phages) exist abundantly and ubiquitously at 1031 particles in the natural environment, which may be 10 times greater than bacterial counts on Earth (Weitz et al., 2013). Many phages also exist in fermented food as the hosts of LAB. Studies on phages in fermented foods have focused on phenomenal analyses and phage therapy by controlling the phages during fermentation. Recently, the microbiota of kimchi was analyzed through pyrosequencing, and many phage sequences were detected in kimchi (Jung et al., 2011). Weissella phages from Thai pork sausage (Nham), Pediococcus phages from cucumber pickle starter, and Weissella, Lactobacillus, and Leuconostoc phages from sauerkraut critically interfere in fermentation (Kleppen et al., 2012; Lu et al., 2003; Pringsulaka et al., 2011). Phages may interact with the host bacteria during fermentation and affect the genetic diversity, dynamics, evolution, and microbial succession of the host bacteria (Lu et al., 2012). Kimchi is becoming an international fermented food due to its taste and health benefits. However, the microbial community changes due to phages and taste-change factors are currently unknown. Most commercial kimchi relies on natural fermentation; thus, an understanding of the influencing factors during kimchi fermentation is essential. The aim of this study was to investigate the characteristics of Weissella phages isolated from watery kimchi and effects toward the hosts generally emerged in the early fermentation in kimchi.

Materials and methods

Isolation of bacteriophages

Two different Dongchimi samples were manufactured, filtered with a 0.22-μM pore size, and plaque formation was identified with 10 LAB strains and 192 isolated bacterial strains from each Dongchimi sample using a spot assay. Various strains were cultured in de Man-Rogosa-Sharp (MRS) media (Oxoid, Basingstoke, UK) and incubated under anaerobic conditions at 30 °C for 18 h. To obtain a phage solution, Dongchimi was produced and kept in a sampling filter bag (3 M, St. Paul, MN, USA). Then, the filtered sample was centrifuged at 8000 × g for 10 min and the supernatant was filtered again under a 0.22-μM pore size (Millipore, Billerica, MA, USA) to exclude initial bacteria in Dongchimi. The solution was collected every day and the filtered sample and host bacteria were inoculated at 2% in 5 mL of MRS broth and incubated for 4 h at 30 °C. After incubation, the culture solution was centrifuged at 8000 × g for 10 min and the aliquot was filtered through a 0.22-μM filter (Millipore). A plaque assay was performed to identify the presence of phages.

Transmission electron microscopy (TEM) analysis

The phage solution was concentrated to 109–10 PFU/mL using 20% PEG (MW 8000). To remove damaged phage from the concentrated phage solution, CsCl ultracentrifugation at 28,000 × g was performed for 1 h. Each phage sample solution was purified and attached to a carbon-coated copper grid (200 mesh, Ted Pella, Redding, USA), negatively stained with 2% uranyl acetate (pH 4.0), and washed with sterilized distilled water. The samples were observed by TEM (h-7600, HITACHI, Tokyo, Japan) at an operating voltage of 80 kV for 3000 × magnification (Ackermann et al., 2009). Isolated phages were identified and classified based on the International Committee on Taxonomy of Viruses guidelines (Adriaenssens and Brister, 2017; Lefkowitz et al., 2017).

Determination of host ranges for phages by spot assay and efficiency of plating (EOP)

Thirty LAB isolated from two different Dongchimi and Baek-kimchi and 57 LAB from the Lab. Culture Collections were used to determine the host ranges of phage isolation. Host bacteria were incubated at 30 °C for 18 h in MRS media. Each culture of bacteria (2%) was inoculated into 5 mL of 0.6% MRS soft agar then overlaid on MRS agar plates. Phage solution was spotted on the prepared double-layered agar and incubated at 30 °C for 18 h. After incubation, plaque clarity was confirmed according to a previous study (Clokie and Kropinski, 2009). The EOP was adopted as a another host range determination and counted as the ratio of PFU/mL for the phage to the initial host strain and PFU/mL for the same phage to other bacteria (Pujato et al., 2017). The variety of LAB strains was determined according to the results of the spot assay. Finally, the number of plaques in the plate was counted and compared to the host bacteria of the phage from which the relative efficiency was calculated (Ackermann, 1998).

Adsorption rates of phages

Adsorption rates were identified to determine the phage ability to attach to the bacteria (Sinha et al., 2018). Bacteria were cultured in MRS broth and grown under O.D.600 0.6 (exponential growth phase). The bacterial culture was centrifuged at 8000 × g for 10 min and suspended in phage solution (1.0 × 108–1.4 × 109) then incubated at 30 °C for 20 min due to reaching adsorption. After adsorption, the mixture of phages and bacteria was centrifuged at 10,000 × g for 5 min to obtain a precipitant of bacteria that were adsorbed with phages. The supernatants of phages that were not adsorbed to the bacteria were identified, and the number of phages adsorbed to bacteria was estimated as the proportion of phages adsorbed to the initial phage count (Pujato et al., 2017). The adsorption rate analysis was performed in triplicate by independent trials.

Phage susceptibility of bacterial strains in liquid culture

Weissella cibaria KCTC 3807, W. cibaria CMU, Leuconostoc mesenteroides KCCM 11,325, and Lactobacillus plantarum MGB 0106 were sub-inoculated into 100 mL of fresh MRS broth, and the culture was incubated at 30 °C under anaerobic conditions. After reaching the early exponential growth phase (OD600 = 0.18) (Chang, 2016), ΦWC53 by multiplicity of infection (MOI) of 10 as well as ΦWC54 and ΦWC56 by MOI of 1 were inoculated into the MRS broth and incubated at 30 °C for up to 16 h. The growth of the host strain was monitored for 1 h intervals at a wavelength of 600 nm (Lee et al., 2016). All experiments were performed in triple trials.

Stability of phages at different pH values and temperatures

Isolated phages from Dongchimi were exposed to different pH values by hydrochloride. The pH was calibrated with a pH meter (Model 750P, Istek, Seoul, Korea) to pH 3–5. Each phage was inoculated in different concentrations of acidity and incubated at 7 °C and 30 °C for 48 h. The phages were counted by spot assay (Szafrański et al., 2017) above the double-layered MRS plate, and the amount of extinction was counted.

Statistical analysis

Analysis of variance (ANOVA) was used to analyze the results, and additional analysis was conducted by applying Tukey's multiple comparisons test. All statistical analyses were performed with SAS software version 9.4 (SAS Institute, Cary, NC, USA), and significance was identified at p < 0.05. All measurements were performed in duplicate.

Results and discussion

Isolation and characterization of phages

A total of 21 phages were isolated on 202 acid-producing bacteria from two Dongchimi samples. Among them, three phages infecting the Weissella indicator were selected based on clear plaque morphologies. The phages were named as ΦWC53, ΦWC54, and ΦWC56 after the Weissella spp. TEM indicated that the phage ΦWC53 could be classified into Siphoviridae, and ΦWC54 and ΦWC56 into Myoviridae family, which was similar to the results of previous studies (Hoai et al., 2018; Kong and Park, 2020) (Fig. 1). In addition, analyses by restriction enzyme mapping and SDS-PAGE showed different patterns that the phages were confirmed as different phages (Fig. 2). One-step growth was analyzed to characterize the phages. The burst sizes were 5–260 particles/infected cell and the latent periods were 20–45 min, which were within the ranges of the known Weissella phages (Kong and Park, 2020; Pringsulaka et al., 2011).

Fig. 3.

Fig. 3

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Phage-susceptibility assay of ΦWC53 (WCP53), ΦWC54 (WCP54), and ΦWC56 (WCP56) to Weissella hosts in liquid culture by phage challenging after 3 h at 30 °C with triplicate trials

Fig. 4.

Fig. 4

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Stability of phages ΦWC53 (A), ΦWC54 (B), and ΦWC56 (C) at different pH values (pH 5, 4, and 3) for two days at 7 °C (I) and 30 °C (II)

Fig. 1.

Fig. 1

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Morphology of ΦWC53 in the family Siphoviridae (A), ΦWC54 and ΦWC56 in the family Myoviridae (B, C) by transmission electron microscopy (3000 × magnification)

Fig. 2.

Fig. 2

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Analyses of protein pattern by SDS-PAGE (I) and restriction map by EcoRI (II). Symbols: (I) M; pre-stained protein marker (Bio-rad); A-ΦWC53; B-ΦWC54; C-ΦWC56, (II) M1, Lambda DNA/HindIII marker; M2, 1 kb size marker; A-ΦWC53; B-ΦWC54; C-ΦWC56

Host range and plaque morphology for phages

The host range of the phage was examined by spot assay and EOP for Weissella spp. and other LAB. ΦWC53, ΦWC54, and ΦWC56 might infect species of the major genera of kimchi, such as Weissella spp., L. mesenteroides, and Lactobacillus spp. (Table 1 and 2). Phages showed very broad growth-inhibitory spectra toward LAB. Kong and Park (2020) reports that ΦWC51 infects the three genera and Lu et al. (2012) also shows that Φ3.2.27 and Φ3.8.18 infect three different genera. The phages of Φ3.2.27 and Φ3.8.18 from the commercial fermented cucumber infect multiple hosts, such as W. cibaria, L. plantarum, and L. brevis. Pujato et al. (2017) reports that phages infect cross-species hosts of Leu. mesenteroides and Leu. pseudomesenteroides. Ross et al. (2016) suggests that the phage host range may not be a fixed property of each species. Hosts can show unexpected genome plasticity by horizontal gene transfer that comes from transformation, transduction, and conjugation. Among them, transduction is mostly effective because of viral tropism and DNA infection mechanisms into the recipient. The recipients get the foreign genes for superinfection immunity and resistance to the environmental stresses or induce the destruction of the principal genes by phage transduction into prophage (Fortier and Sekulovic, 2013; Modi et al., 2013). Sometimes, prophage may switch from lysogenic to lytic cycle into phage multiplication and host death (Gandon S., 2016). Phages generally play a part role in the ecology as well as the bacterial evolution through several interactions between the host and phage genomes (Nasir et al., 2017). The close relatives like lactic acid bacteria are also more easy to share the same habitats and the organisms can exchange genes through the sharing environments (Matte-Tailliez et al., 2002; Philippot et al., 2010).

Table 1.

Host range determination of ΦWC53, ΦWC54, and ΦWC56 to Weissella, Leuconostoc, and Lactobacillus by spot assay (SA) and efficiency of plating (EOP)

Host strains Phages
ΦWC53 ΦWC54 ΦWC56
SA EOP SA EOP SA EOP
W. cibaria CMU ++++* 1** ++++ 1 ++++ 0.62
W. cibaria KCTC 3807 ++++ 2.53 × 10–3 ++++ 0.3 ++++ 1
W. cibaria B005 ++ < 3.8 × 10–8 + < 1.5 × 10–9 ++ < 3.9 × 10–8
W. cibaria B130 – – – – ++ < 3.9 × 10–7
W. cibaria B248 ++ < 3.8 × 10–6 + 2.0 × 10–2 ++ < 2.7 × 10–6
W. cibaria D004 ++ < 3.8 × 10–8 + < 1.0 × 10–9 + < 3.9 × 10–8
W. kimchi KCCM 41,287 + < 3.8 × 10–6 + < 2.0 × 10–9 + < 3.9 × 10–6
W. koreensis KCCM 41,517 ++ < 3.8 × 10–6 ++ < 1.5 × 10–9 ++ < 3.9 × 10–7
L. mesenteroidesKCCM11325 + < 3.8 × 10–6 + < 1.5 × 10–9 + < 3.9 × 10–6
Lac. plantarum KCTC 12,116 + < 3.8 × 10–6 + < 2.5 × 10–9 + < 3.9 × 10–5
Lac. plantarum MGB 0459 + < 3.8 × 10–8 – – – –
Lac. plantarum MGB 0106 + < 3.8 × 10–7 + < 1.3 × 10–9 + < 3.9 × 10–7
Lac. reuteri KCTC 40,417 + < 3.8 × 10–7 + < 1.5 × 10–9 + < 4.0 × 10–2
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*Symbols: ++++, clear plaque (complete lysis); ++, light turbid plaque; +, deep turbid plaque; -, no plaque.

**Number (%); plaque of the strain/plaque of the indicator strain. Grey shading corresponds to the indicator strain for each phage.

Table 2.

Plaque morphology of ΦWC53, ΦWC54, and ΦWC56 on Weissella, Leuconostoc, and Lactobacillus by spot assay

graphic file with name 10068_2021_920_Tab2_HTML.jpg

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*Symbols of plaque morphology: clear plaque (CCP); light turbid plaque (LTP); deep turbid plaques (DTP); no plaque (NP)

The host range is usually defined by what it can lyse thus, determining the range of a specific phage can be difficult (Hyman and Abedon, 2010; Labrie et al., 2010). Spot testing sometimes causes false positives because of residual endolysin, bacteriocins, or other mechanisms (Abedon, 2011). Pujato et al. (2017) also recommends the use of another assay in addition to a spot assay to reduce incorrect determination. Therefore, the most infective hosts based on clear plaque by spot and EOP assays were W. cibaria CMU for ΦWC53 and ΦWC54 and W. cibaria KCTC 3807 for ΦWC56. The plaque morphologies differed by clear turbid plaques on LAB, which might indicate different infection mechanisms or resistance systems (Table 2). According to the degree of growth, the clear plaque might indicate complete lysis of the bacteria of W. cibaria CMU and KCTC 3807, while the turbid plaques for other Weissella spp., L. mesenteroides, and Lactobacillus spp. might show partial lysis of the host by lysogenicity or growth inhibition by other cellular components. Interestingly, the plaque of typical bulls-eye appearance by lysogenicity and greater turbidity at the center (Jurczak-Kurek et al., 2016) was confirmed in the turbid plaques of L. plantarum MGB0106 by ΦWC53 and ΦWC54. Therefore, the phages interacted differently with LAB that the plaque appearance from different hosts, phages, and environmental conditions must be considered to determine the host range as narrow or broad. Plaques with different morphologies must be studied further to confirm the infection mechanism and the host mortality by phages during kimchi fermentation for LAB ecology.

Adsorption of phages onto the host

Adsorption analysis was conducted to determine the attachment to the host surface by the phages (Table 3). ΦWC53 and ΦWC54 showed the highest adsorption on W. cibaria CMU at 72% and 97%, respectively. ΦWC56 showed the highest adsorption on W. cibaria KCTC 3807 at 99%. However, all had a low adsorption rate toward other Weissella spp., L. mesenteroides, and Lactobacillus spp. ΦWC53 generally showed a low adsorption level compared to the other phages. No correlation between clear plaque and adsorption rate was established as in another study (Pujato et al., 2017).

Table 3.

Adsorption ability on the hosts of lactic acid bacteria by ΦWC53, ΦWC54, and ΦWC56

Host strains Adsorption rate
ΦWC53 ΦWC54 ΦWC56
W. cibaria CMU 72.3 ± 2.0* 97.1 ± 0.4 97.7 ± 0.2
W. cibaria KCTC 3807 49.3 ± 0.8 96.3 ± 0.1 99.4 ± 0.1
W. cibaria B005 76.2 ± 4.3 88.7 ± 1.4 61.5 ± 6.6
W. cibaria B130 – – 51.0 ± 11.7
W. cibaria B248 31.2 ± 4.8 98.4 ± 0.2 99.7 ± 0.1
W. cibaria D004 31.2 ± 0.3 86.3 ± 1.3 79.9 ± 0.2
W. kimchi KCCM 41,287 28.4 ± 4.5 82.5 ± 3.3 38.5 ± 1.9
W. koreensis KCCM 41,517 7.9 ± 5.7 97.5 ± 0.3 98.1 ± 0.1
L. mesenteroidesKCCM11325 10.1 ± 1.8 43.6 ± 8.3 4.0 ± 1.7
Lac. plantarum KCTC 12,116 30.7 ± 1.8 86.2 ± 0.6 72.9 ± 0.2
Lac. plantarum MGB 0459 12.8 ± 5.5 – –
Lac. plantarum MGB 0106 6.9 ± 5.7 35.9 ± 9.1 17.3 ± 9.3
Lac. reuteri KCTC 40,417 21.1 ± 4.4 8.3 ± 19.9 35.0 ± 5.5
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*Number: adsorption rate (%) by adsorbed phage to total phages with triplicate trials

Phage-susceptibility of bacterial strains in liquid culture

To confirm bacterial growth in the presence of ΦWC53, ΦWC54, and ΦWC56, phage-susceptibility assays were conducted. Host bacteria were pre-incubated until the OD value reached 0.18 at 600 nm. The phages of ΦWC53 by 10 MOI and ΦWC54 and ΦWC56 by 1 MOI were incubated in the host media for up to 16 h at 30 °C. According to the results of ΦWC53 to W. cibaria CMU, the bacterial growth was slightly inhibited after 2 h just after phage challenge time at 3 h fermentation. However, the host grew in similar growth to that of the non-treated control group (Fig. 2). ΦWC53 with clear plaque (complete lysis) by spot assay on the solid media showed different patterns in the phage-susceptibility assay in liquid culture. Growths of W. cibaria CMU by ΦWC54 and W. cibaria KCTC 3807 by ΦWC56 were inhibited after challenging at 3 h fermentation. ΦWC54 lysed its host bacteria very effectively until 12 h to an OD of 0.18. L. mesenteroides KCCM 11,325 and L. plantarum MGB 0106 showing turbid plaques grew well, but at a slightly lower level. Studies regarding phage infection for Gram ( +) bacteria have reported that they may recognize their hosts in a two-step manner as follows: reversible interaction via a saccharide moiety on the surface and then irreversible interaction via the receptor (Baptista et al., 2008). The phage interaction on LAB has been related to strain-specific decoration or side chain formation of cell surface polysaccharides (Ainsworth et al., 2014). Surface polysaccharides, such as capsules and slime, are not covalently attached to the peptidoglycan and may be loosely associated with the cell wall (Guglielmotti et al., 2009; Räisänen et al., 2004). Environmental factors, such as temperature and pH, influence surface polysaccharide production and phage-bacteria contact efficiency (Corbett and Roberts, 2008; Fister et al., 2016; Rodríguez et al., 2008). Infection of ΦWC53 to W. cibaria CMU seemed to be different from the solid culture shown as the plaque and liquid culture not as a lytic form because of host surface condition.

Stability of phages at different pH values and temperatures

As kimchi is fermented, the pH of kimchi decreases as LAB grow. To identify phage stability in the kimchi environment, three phages were exposed to three different acidic conditions at two different temperatures and assessed for their survival. All phages at 7 °C were stable at any pH. When exposed to temperatures of 30 °C, only ΦWC53 was stable and only slightly decreased at pH 3 for 48 h, while ΦWC54 and ΦWC56 were unstable and decreased substantially at pH 3. Sensitivities of those phages to temperature were higher than those to pH. Interestingly, the stability of ΦWC53 at pH 3 was remarkably higher than those of ΦWC54, ΦWC56, PWc, and ΦWC005 in the previous studies (Hoai et al., 2018; Kong and Park, 2020). Therefore, fermentation conditions may be related to LAB phage stability, which influences to the kind of LAB strain and population in the kimchi microecosystem.

Acknowledgements

This research was supported by the National Research Foundation of Korea (grant 2020R1F1A107000111).

Declaration

Conflict of interest

The authors have no financial conflict of interest to declare.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Soomin Lee, Email: leesoomin@kfri.re.kr.

Jong-Hyun Park, Email: p5062@gachon.ac.kr.

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