Journal of Microbiology

Volume 57(11); November 2019

Review

[Minireivew]Microbial consortia including methanotrophs: some benefits of living together: Rajendra Singh , Jaewon Ryu , Si Wouk Kim; J. Microbiol. 2019;57(11):939-952. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9328-8

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Abstract: With the progress of biotechnological research and improvements made in bioprocessing with pure cultures, microbial consortia have gained recognition for accomplishing biological processes with improved effectiveness. Microbes are indispensable tool in developing bioprocesses for the production of bioenergy and biochemicals while utilizing renewable resources due to technical, economic and environmental advantages. They communicate with specific cohorts in close proximity to promote metabolic cooperation. Use of positive microbial associations has been recognized widely, especially in food industries and bioremediation of toxic compounds and waste materials. Role of microbial associations in developing sustainable energy sources and substitutes for conventional fuels is highly promising with many commercial prospects. Detoxification of chemical contaminants sourced from domestic, agricultural and industrial wastes has also been achieved through microbial catalysis in pure and co-culture systems. Methanotrophs, the sole biological sink of greenhouse gas methane, catalyze the methane monooxygenasemediated oxidation of methane to methanol, a high energy density liquid and key platform chemical to produce commodity chemical compounds and their derivatives. Constructed microbial consortia have positive effects, such as improved biomass, biocatalytic potential, stability etc. In a methanotroph- heterotroph consortium, non-methanotrophs provide key nutrient factors and alleviate the toxicity from the culture. Non-methanotrophic organisms biologically stimulate the growth and activity of methanotrophs via production of growth stimulators. However, methanotrophs in association with cocultured microorganisms are in need of further exploration and thorough investigation to study their interaction mode and application with improved effectiveness.

Journal Articles

Cohnella abietis sp. nov., isolated from Korean fir (Abies koreana) rhizospheric soil of Halla mountain: Lingmin Jiang , Sophea Pheng , Keun Chul Lee , Se Won Kang , Jae Cheol Jeong , Cha Young Kim , Hyeong Cheol Park , Dae-Hyuk Kim , Suk Weon Kim , Song-Gun Kim , Jiyoung Lee; J. Microbiol. 2019;57(11):953-958. Published online August 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9136-1

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Abstract: A strictly aerobic, motile, endospore-forming, rod-shaped bacterium, designated HS21T, was isolated from rhizospheric soil of the Korean fir tree (Abies koreana) from Halla mountain on Jeju island, Korea. Growth of strain HS21T was observed at pH 6.0–8.0 (optimum: pH 7.0), 0–2% (w/v) NaCl and 4–30°C (optimum: 25°C). A comparative analysis of 16S rRNA gene sequences showed that strain HS21T was most closely related to Cohnella luojiensis HY-22RT (97.6%), followed by C. lupini RLAHU4BT (97.4%) and C. collisoli NKM- 5T (97.2%). The genome of strain HS21T comprised a circular chromosome of 7,059,027 bp with 44.8% G + C content. The DNA-DNA relatedness values between strain HS21T and C. luojiensis HY-22RT and C. lupini RLAHU4BT were 18.1% and 13.8%, respectively. The major cellular fatty acids (> 5%) of the isolate were anteiso-C15:0, iso-C16:0, C16:0, and iso-C15:0. The polar lipids present were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, lysylphosphatidylglycerol, and three unidentified aminophospholipids. Based on its phenotypic, phylogenetic, genomic, and chemotaxonomic properties, strain HS21T represents a novel species of the genus Cohnella, for which the name Cohnella abietis sp. nov. is proposed. The type strain is HS21T (= KCTC 43028T = CCTCC AB 2019010T).

Methylobacterium terrae sp. nov., a radiation-resistant bacterium isolated from gamma ray-irradiated soil: Jiyoun Kim , Geeta Chhetri , Inhyup Kim , Hyungdong Kim , Myung Kyum Kim , Taegun Seo; J. Microbiol. 2019;57(11):959-966. Published online August 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9007-9

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Abstract: A Gram-stain-negative, asporogenous, aerobic rods, motile by means of a single polar flagellum, catalase- and oxidase-positive, methylotrophic bacterium, designated 17Sr1-28T, was isolated from gamma ray-irradiated soil. The 16S rRNA gene sequence analysis showed that strain 17Sr1-28T was phylogenetically related to Methylobacterium currus PR1016AT (96.8%), Methylobacterium platani PMB02T (96.2%), Methylobacterium aquaticum DSM 16371T (96.3%), Methylobacterium tarhaniae N4211T (96.4%), Methylobacterium frigidaeris IER25-16T (95.8%), and Methylobacterium organophilum JCM 2833T (92.7%). The G+C content calculated based on genome sequence was 71.6%. The average nucleotide identity and in silico DNA-DNA hybridization values between strain 17Sr1- 28T and M. currus, M. platani, M. aquaticum, M. tarhaniae, M. frigidaeris, and M. organophilum were 77.7–90.4% and 22–39.6%, respectively. The major fatty acids of strain 17Sr1- 28T were summed feature 8 (C18:1 ω7c and/or C18:1 ω6c), and summed feature 3 (C16:1 ω7c and/or C16:1 ω6c). The predominant quinone was ubiquinone 10 and the major polar lipids were diphosphatidylglycerol, phosphatidylcholine, phosphatidylethanolamine, and phosphatidylglycerol. On the basis of the data from phenotypic tests and genotypic differences between strain 17Sr1-28T and its close phylogenetic relatives, strain 17Sr1-28T represents a new species belonging to the genus Methylobacterium, for which the name Methylobacterium terrae sp. nov. (= KCTC 52904T = NBRC 112873T) is proposed.

Mucilaginibacter limnophilus sp. nov., isolated from a lake: Shih-Yi Sheu , Yi-Ru Xie , Wen-Ming Chen; J. Microbiol. 2019;57(11):967-975. Published online August 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9146-z

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Abstract: A polyphasic taxonomy approach was used to characterize strain YBJ-36T, isolated from a freshwater lake in Taiwan. Phylogenetic analyses, based on 16S rRNA gene sequences and coding sequences of an up-to-date bacterial core gene set (92 protein clusters), indicated that strain YBJ-36T formed a phylogenetic lineage in the genus Mucilaginibacter. 16S rRNA gene sequence similarity indicated that strain YBJ-36T is closely related to species within the genus Mucilaginibacter (93.8–97.8% sequence similarity) and is most similar to Mucilaginibacter fluminis TTM-2T (97.8%), followed by Mucilaginibacter roseus TTM-1T (97.2%). Microbiological analyses demonstrated that strain YBJ-36T is Gram-negative, aerobic, non-motile, rod-shaped, surrounded by a thick capsule, and forms pink-colored colonies. Strain YBJ-36T grew between 20–40°C (optimal range, 35–37°C), pH 5.5–7.0 (optimal pH of 6) and 0–2% NaCl (optimal concentration, 0.5%). The predominant fatty acids of strain YBJ-36T are iso-C15:0 and summed feature 3 (C16:1 ω7c and/or C16:1 ω6c), the major polar lipid is phosphatidylethanolamine, the major polyamine is homospermidine, and the major isoprenoid quinone is MK-7. The draft genome is approximately 4.63 Mb in size with a G+C content of 42.8 mol%. Strain YBJ-36T exhibited less than 35% DNA-DNA relatedness with Mucilaginibacter fluminis TTM-2T and Mucilaginibacter roseus TTM-1T. Based on phenotypic and genotypic properties and phylogenetic inference, strain YBJ-36T should be classified in a novel species of the genus Mucilaginibacter, for which the name Mucilaginibacter limnophilus sp. nov. is proposed. The type strain is YBJ-36T (= BCRC 81056T = KCTC 52811T = LMG 30058T).

Martelella lutilitoris sp. nov., isolated from a tidal mudflat: Young-Ju Kim , Soon Dong Lee; J. Microbiol. 2019;57(11):976-981. Published online September 25, 2019; DOI: https://doi.org/10.1007/s12275-019-9259-4

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Abstract: A novel, Gram-stain-negative, marine bacterium, designated GH2-6T, was isolated from a rhizosphere mudflat of a halophyte (Carex scabrifolia) collected in Gangwha Island, the Republic of Korea. The cells of the organism were strictly aerobic, oxidase- and catalase-positive, non-flagellated rods. Growth occurred at 20–45°C, pH 5–10, and 0.5–9 (w/v) NaCl. The requirement of Na+ for growth (0.5–3%) was observed. The major respiratory quinone was Q-10. The major polar lipids were phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, an aminolipid and a glycolipid. The predominant fatty acids were C18:1 ω7c, C18:0, C16:0, C19:0 cyclo ω8c, C18:1 ω7c 11-methyl and summed feature 2 (C14:0 3-OH and/or C16:1 iso I). The genome size was 4.45 Mb and the G+C content of the genomic DNA was 61.9 mol%. Phylogenetic analyses based on 16S rRNA gene sequences revealed that strain GH2-6T belonged to genus Martelella and formed a tight cluster with M. radicis BM5-7T and M. endophytica YC6887T. Levels of 16S rRNA gene sequence similarity between the novel isolate and members of the genus were 99.3–95.5%, but strain GH2-6T possessed an extended loop (49 nucleotides in length) between positions 187 and 213 of the 16S rRNA gene sequence (E. coli numbering). DDH values in vitro between the novel isolate and the closest relatives were 23.2±12.8 – 46.3±5.2%. On the basis of polyphasic data presented in this study, the type strain GH2-6T (= KACC 19403T = KCTC 62125T = NBRC 113212T) represents a novel species of the genus Martelella for which the name Martelella lutilitoris sp. nov. is proposed.

Isolation and genome analysis of Winogradskyella algicola sp. nov., the dominant bacterial species associated with the green alga Dunaliella tertiolecta: Jaeho Song , Yeonjung Lim , Hye-Jin Jang , Yochan Joung , Ilnam Kang , Seong-Joo Hong , Choul-Gyun Lee , Jang-Cheon Cho; J. Microbiol. 2019;57(11):982-990. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9378-y

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Abstract: Microalgae and bacteria are known to be closely associated in diverse environments. To isolate dominant bacterial species associated with a green alga, Dunaliella tertiolecta, a photoreactor culture of the microalga was investigated using culture- based and culture-independent approaches. The bacterial community structure of the algal culture showed that the most abundant bacterial species under the culture conditions was related to the genus Winogradskyella. The closely related amplicon sequences, showing ≥ 99.5% 16S rRNA gene sequence similarity to one of the isolates, designated IMCC- 33238T, constituted > 49% of the bacterial community and was therefore regarded as the most dominant species in the algal culture. Strain IMCC33238T was characterized by Gramstaining- negative and orange-colored rods. Phylogenetic analyses of the 16S rRNA genes as well as whole genome sequences revealed that strain IMCC33238T belonged to Winogradskyella and shared more than 97.2% 16S rRNA gene sequence similarity with Winogradskyella species. The strain contained iso-C15:1 G, iso-C15:0, iso-C15:0 3-OH, and summed feature 3 (C16:1 ω6c and/or C16:1 ω7c) as major fatty acids and MK-6 as the predominant quinone. The polar lipids found in strain IMCC33238T were phosphatidylethanolamine, two unidentified aminolipids, and three unidentified lipids. The genome of strain IMCC33238T was 3.37 Mbp in size with 33.9 mol% G + C content and proteorhodopsin. Many genes encoding folate and vitamin production are considered to play an important role in the bacteria-algae interaction. On the basis of phylogenetic and phenotypic characteristics, strain IMCC33238T represents a novel species in the genus Winogradskyella, for which the name Winogradskyella algicola sp. nov. is proposed. The type strain is IMCC33238T (= KACC 21192T = NBRC 113704T).

Brevibacillus antibioticus sp. nov., with a broad range of antibacterial activity, isolated from soil in the Nakdong River: Ahyoung Choi , Young Ho Nam , Kiwoon Baek , Eu Jin Chung; J. Microbiol. 2019;57(11):991-996. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9325-y

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Abstract: A Gram-stain-positive, aerobic, motile, and rod-shaped bacterial strain designated TGS2-1T was isolated from sediment soil in the Nakdong River, Republic of Korea. The optimal growth of strain TGS2-1T was observed at 28°C and pH 7.0 without NaCl supplementation. Strain TGS2-1T revealed antibiosis against various bacteria, including Staphylococcus aureus KCCM 4051, CCARM 3089 (methicillin resistant strains), Enterococcus faecalis KCCM 11814, Escherichia coli KCTC 2443, Candida albicans KACC 7270, and Filobasidium neoformans KCTC 7902. Phylogenetic analyses based on the 16S rRNA gene sequences indicated that strain TGS2-1T belonged to the genus Brevibacillus and shared 93.8–99.7% sequence similarity with Brevibacillus species. Whole-genome sequencing of strain TGS2-1T revealed a genome size of 6.2 Mbp and DNA G + C content of 47.0 mol%. The TGS2-1T genome shared an average nucleotide identity and digital DNA-DNA hybridization of 74.6–93.3% and 18.6–67.1%, respectively, with six related Brevibacillus genomes. The major fatty acid constituents of strain TGS2-1T were anteiso-C15:0 (62.3%) and anteiso-C17:0 (10.8%). Cells of strain TGS2-1T contained diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, seven unidentified aminophospholipids, and five unidentified lipids. The isoprenoid quinone detected in the strain was menaquinone-7 (MK-7). Based on data obtained from this polyphasic taxonomic study, strain TGS2-1T represents a novel species belonging to genus Brevibacillus, for which the name B. antibioticus sp. nov. is proposed. The type strain is TGS2-1T (= KCCM 90326T = NBRC 113840T = FBCC-B2501).

Salicibibacter halophilus sp. nov., a moderately halophilic bacterium isolated from kimchi: Young Joon Oh , Joon Yong Kim , Hyo Kyeong Park , Ja-Young Jang , Seul Ki Lim , Min-Sung Kwon , Hak-Jong Choi; J. Microbiol. 2019;57(11):997-1002. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9421-z

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Abstract: A Gram-stain-positive, rod-shaped, alkalitolerant, and halophilic bacterium–designated as strain NKC3-5T–was isolated from kimchi that was collected from the Geumsan area in the Republic of Korea. Cells of isolated strain NKC3-5T were 0.5–0.7􍾘μm wide and 1.4–2.8 μm long. The strain NKC3-5T could grow at up to 20.0% (w/v) NaCl (optimum 10%), pH 6.5–10.0 (optimum pH 9.0), and 25–40°C (optimum 35°C). The cells were able to reduce nitrate under aerobic conditions, which is the first report in the genus Salicibibacter. The genome size and genomic G + C content of strain NKC3-5T were 3,754,174 bp and 45.9 mol%, respectively; it contained 3,630 coding sequences, 16S rRNA genes (six 16S, five 5S, and five 23S), and 59 tRNA genes. Phylogenetic analysis based on 16S rRNA showed that strain NKC- 3-5T clustered with bacterium Salicibibacter kimchii NKC1-1T, with a similarity of 96.2–97.6%, but formed a distinct branch with other published species of the family Bacillaceae. In addition, OrthoANI value between strain NKC3-5T and Salicibibacter kimchii NKC1-1T was far lower than the species demarcation threshold. Using functional genome annotation, the result found that carbohydrate, amino acid, and vitamin metabolism related genes were highly distributed in the genome of strain NKC3-5T. Comparative genomic analysis revealed that strain NKC3-5T had 716 pan-genome orthologous groups (POGs), dominated with carbohydrate metabolism. Phylogenomic analysis based on the concatenated core POGs revealed that strain NKC3-5T was closely related to Salicibibacter kimchii. The predominant polar lipids were phosphatidylglycerol and two unidentified lipids. Anteiso- C15:0, iso-C17:0, anteiso-C17:0, and iso-C15:0 were the major cellular fatty acids, and menaquinone-7 was the major isoprenoid quinone present in strain NKC3-5T. Cell wall peptidoglycan analysis of strain NKC3-5T showed that meso-diaminopimelic acid was the diagnostic diamino acid. The phenotypic, genomic, phylogenetic, and chemotaxonomic properties reveal that the strain represents a novel species of the genus Salicibibacter, for which the name Salicibibacter halophilus sp. nov. is proposed, with the type strain NKC3-5T (= KACC 21230T = JCM 33437T).

Preliminary study on microeukaryotic community analysis using NGS technology to determine postmortem submersion interval (PMSI) in the drowned pig: Cheol-ho Hyun , Heesoo Kim , Seongho Ryu , Won Kim; J. Microbiol. 2019;57(11):1003-1011. Published online September 25, 2019; DOI: https://doi.org/10.1007/s12275-019-9198-0

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Abstract: While several methods for determining postmortem submersion interval (PMSI) in drowning cases have been suggested, the estimation of PMSI remains difficult. Next-generation sequencing (NGS) technology enables simultaneous identification of multiple taxa from environmental samples. Although NGS has been applied to estimate time since death, this application has been mainly focused on terrestrial cases. As a case study, we investigated microeukaryotic biodiversity and community structures in submerged car bonnet and drowned pig using NGS technology. NGS analysis showed that the microeukaryotic biodiversity in pig carcass was relevantly lower than that in car bonnet. NGS results also revealed that water molds and algae were related to decomposition. Relative abundances of Filobasidium, Achlya, Saprolegnia, Hydrodicton, Lobosphaera, and Scenedesmus varied with decomposition period. This data indicated that these taxa might be useful as good indicators to estimate PMSI. This study showed microeukaryotic community analysis using NGS technology may help solve drowning cases in forensic investigation.

Pten gene deletion in intestinal epithelial cells enhances susceptibility to Salmonella Typhimurium infection in mice: Cody Howe , Jonathon Mitchell , Su Jin Kim , Eunok Im , Sang Hoon Rhee; J. Microbiol. 2019;57(11):1012-1018. Published online September 25, 2019; DOI: https://doi.org/10.1007/s12275-019-9320-3

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Abstract: Although phosphatase and tensin homolog (PTEN) is typically considered a tumor-suppressor gene, it was recently suggested that PTEN regulates TLR5-induced immune and inflammatory responses in intestinal epithelial cells (IECs), suggesting an immunomodulatory function of PTEN in the gut. However, this alternative function of PTEN has not yet been evaluated in an in vivo context of protection against enteropathogenic bacteria. To address this, we utilized IECrestricted Pten knockout (PtenΔIEC/ΔIEC) and littermate Pten+/+ mice. These mice were subjected to the streptomycin-pretreated mouse model of Salmonella infection, and subsequently given an oral gavage of a low inoculum (2 × 104 CFU) of Salmonella enterica serovar Typhimurium (S. Typhimurium). This bacterial infection not only increased the mortality of PtenΔIEC/ΔIEC mice compared to Pten+/+ mice, but also induced deleterious gastrointestinal inflammation in PtenΔIEC/ΔIEC mice manifested by massive histological damage to the intestinal mucosa. S. Typhimurium infection upregulated pro-inflammatory cytokine production in the intestine of PtenΔIEC/ΔIEC mice compared to controls. Furthermore, bacterial loads were greatly increased in the liver, mesenteric lymph node, and spleen of PtenΔIEC/ΔIEC mice compared to controls. Together, these results suggest that IEC-restricted Pten deficiency renders the host greatly susceptible to Salmonella infection and support an immuneregulatory role of PTEN in the gut.

Propionate, together with triple antibiotics, inhibits the growth of Enterococci: Soyoung Jeong , Yunjae Lee , Cheol-Heui Yun , Ok-Jin Park , Seung Hyun Han; J. Microbiol. 2019;57(11):1019-1024. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9434-7

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Abstract: Enterococci are Gram-positive facultative anaerobic bacteria that colonize the oral cavity and gastrointestinal tract. Enterococcal infections, mainly caused by Enterococcus faecalis and Enterococcus faecium, include apical periodontitis, endocarditis, and bloodstream infections. Recently, vancomycinresistant Enterococci are considered major pathogens that are common but difficult to treat, especially in nosocomial settings. Moreover, E. faecalis is closely associated with recurrent endodontic infections and failed endodontic treatment. In this study, we investigated the effects of short-chain fatty acids (SCFAs), acetate, propionate, and butyrate, which are metabolites fermented by gut microbiota, on the growth of Enterococci. Enterococci were cultured in the presence or absence of acetate, propionate, or butyrate, and the optical density at 600 nm was measured to determine bacterial growth. The minimum inhibitory concentration/minimum bactericidal concentration test was conducted. Bacteria were treated with a SCFA, together with clinically used endodontic treatment methods such as triple antibiotics (metronidazole, minocycline, and ciprofloxacin) and chlorhexidine gluconate (CHX) to determine the effects of combination treatment. Of the SCFAs, propionate had a bacteriostatic effect, inhibiting the growth of E. faecalis in a dose-dependent manner and also that of clinical strains of E. faecalis isolated from dental plaques. Meanwhile, acetate and butyrate had minimal effects on E. faecalis growth. Moreover, propionate inhibited the growth of other Enterococci including E. faecium. In addition, combination treatment of propionate and triple antibiotics led to further growth inhibition, whereas no cooperative effect was observed at propionate plus CHX. These results indicate that propionate attenuates the growth of Enterococci, suggesting propionate as a potential agent to control Enterococcal infections, especially when combined with triple antibiotics.

Comparative portrayal of ocular surface microbe with and without dry eye: ZhenHao Li , Yufang Gong , ShuZe Chen , SiQi Li , Yu Zhang , HuiMin Zhong , ZhouCheng Wang , YiFan Chen , QiXin Deng , YuTing Jiang , LiYing Li , Min Fu , GuoGuo Yi; J. Microbiol. 2019;57(11):1025-1032. Published online August 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9127-2

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Abstract: To compare the ocular surface (OS) microbial communities and diversity between dry eye (DE) and non-DE (NDE). Furthermore, we compared meibomian gland dysfunction (MGD) and non-MGD (NMGD) among DE subjects. The V3-V4 region of 16S rRNA gene high-throughput sequencing was performed in the conjunctival swab samples to investigate the composition of the OS bacterial community in DE (n=35) and NDE (n=54) and compared the composition of MGD (n=25) and NMGD (n=10) among DE subjects. Deep sequencing of OS 16S rDNA from DE (n=35) and NDE (n=54) demonstrated great a difference in alpha and beta diversity between the OS bacterial flora (P < 0.05). The similar OS microbial structures were shown at the phylum and genus levels by bioinformatics analysis between them, and in LEfSe (linear discriminant analysis effect size) analysis, Bacteroidia and Bacteroidetes were enriched in DE, while Pseudomonas was plentiful in NDE (linear discriminant analysis [LDA] > 4.0). Among the DE group, there was no significant difference in α and β diversity between MGD and NMGD (P > 0.05). Surprisingly, Bacilli was the dominant microbe in MGD, and Bacteroidetes was the superior bacteria in NMGD among DE subjects (LDA > 4.0). Different diversity of OS bacteria composition between DE and NDE and the altered diversity of OS bacteria may play an important role in DE. Moreover, the lower dominance of OS bacteria in DE may be associated with the occurrence and development of DE. Although there was no significant difference in alpha and beta analysis, the OS dominant microbe between MGD and NMGD among DE was different.

Increase in the genetic polymorphism of varicella-zoster virus after passaging in in vitro cell culture: Hye Rim Hwang , Seok Cheon Kim , Se Hwan Kang , Chan Hee Lee; J. Microbiol. 2019;57(11):1033-1039. Published online October 28, 2019; DOI: https://doi.org/10.1007/s12275-019-9429-4

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Abstract: Primary infections with the varicella-zoster virus (VZV) result in varicella, while latent reactivation leads to herpes zoster. Both varicella and zoster can be prevented by live attenuated vaccines. There have been reports suggesting that both clinical VZV strains and those in vaccine preparations are genetically polymorphic, containing mixtures of both wild-type and vaccine-type sequences at certain vaccine-specific sites. In this study, the genetic polymorphism of the VZV genome was examined by analyzing the frequencies of minor alleles at each nucleotide position. Next-generation sequencing of the clinical VZV strain YC02 passaged in an in vitro cell culture was used to identify genetically polymorphic sites (GPS), where the minor allele frequency (MAF) exceeded 5%. The number of GPS increased by 7.3-fold at high passages (p100) when compared to low passages (p17), although the average MAF remained similar. GPS were found in 6 open reading frames (ORFs) in p17, 35, and 54 ORFs in p60 and p100, respectively. GPS were found more frequently in the dispensable gene group than the essential gene group, but the average MAF was greater in the essential gene group. The most common two major/minor base pairs were A/g and T/c. GPS were found in all three passages at 16 positions, all located in the reiterated (R) region. The population diversity as measured by Shannon entropy increased in p60 and p100. However, the entropy remained unchanged in the R regions.

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