Journal of Microbiology

Journal Articles

The Salmonella enterica EnvE is an Outer Membrane Lipoprotein and Its Gene Expression Leads to Transcriptional Repression of the Virulence Gene msgA: Sinyeon Kim, Yong Heon Lee; J. Microbiol. 2024;62(11):1013-1022. Published online November 15, 2024; DOI: https://doi.org/10.1007/s12275-024-00183-4

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Abstract: The envE gene of Salmonella enterica serovar Typhimurium is encoded within Salmonella Pathogenicity Island-11 (SPI-11) and is located immediately upstream of the virulence gene msgA (macrophage survival gene A) in the same transcriptional orientation. To date, the characteristics and roles of envE remain largely unexplored. In this study, we show that EnvE, a predicted lipoprotein, is localized on the outer membrane using sucrose gradient ultracentrifugation. Under oxidative stress conditions, envE transcription is suppressed, while msgA transcription is induced, indicating an inverse correlation between the mRNA levels of the two neighboring genes. Importantly, inactivation of envE leads to constitutive transcription of msgA regardless of the presence of oxidative stress. Moreover, trans-complementation of the envE mutant with a plasmid-borne envE fails to prevent the induction of msgA transcription, suggesting that envE functions as a cis-regulatory element rather than a trans-acting factor. We further show that both inactivation and complementation of envE confer wild-type levels of resistance to oxidative stress by ensuring the expression of msgA. Our data suggest that the S. enterica envE gene encodes an outer membrane lipoprotein, and its transcription represses msgA expression in a cis-acting manner, probably by transcriptional interference, although the exact molecular details are yet unclear.

Comparative Transcriptomic Analysis of Flagellar‑Associated Genes in Salmonella Typhimurium and Its rnc Mutant: Seungmok Han , Ji-Won Byun , Minho Lee; J. Microbiol. 2024;62(1):33-48. Published online January 5, 2024; DOI: https://doi.org/10.1007/s12275-023-00099-5

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Salmonella enterica serovar Typhimurium (S. Typhimurium) is a globally recognized foodborne pathogen that affects both animals and humans. Endoribonucleases mediate RNA processing and degradation in the adaptation of bacteria to environmental changes and have been linked to the pathogenicity of S. Typhimurium. Not much is known about the specific regulatory mechanisms of these enzymes in S. Typhimurium, particularly in the context of environmental adaptation. Thus, this study carried out a comparative transcriptomic analysis of wild-type S. Typhimurium SL1344 and its mutant (Δrnc), which lacks the rnc gene encoding RNase III, thereby elucidating the detailed regulatory characteristics that can be attributed to the rnc gene. Global gene expression analysis revealed that the Δrnc strain exhibited 410 upregulated and 301 downregulated genes (fold-change > 1.5 and p < 0.05), as compared to the wild-type strain. Subsequent bioinformatics analysis indicated that these differentially expressed genes are involved in various physiological functions, in both the wild-type and Δrnc strains. This study provides evidence for the critical role of RNase III as a general positive regulator of flagellar-associated genes and its involvement in the pathogenicity of S. Typhimurium.

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CspA regulates stress resistance, flagellar motility and biofilm formation in Salmonella Enteritidis
Xiang Li, Yan Cui, Xiaohui Sun, Chunlei Shi, Shoukui He, Xianming Shi
Food Bioscience.2025; 66: 106237. CrossRef
Influence of Flagella on Salmonella Enteritidis Sedimentation, Biofilm Formation, Disinfectant Resistance, and Interspecies Interactions
Huixue Hu, Jingguo Xu, Jingyu Chen, Chao Tang, Tianhao Zhou, Jun Wang, Zhuangli Kang
Foodborne Pathogens and Disease.2024;[Epub] CrossRef

Azohydromonas aeria sp. nov., isolated from air: Han Xue , Chun-gen Piao , Dan-ran Bian , Min-wei Guo , Yong Li; J. Microbiol. 2020;58(7):543-549. Published online June 27, 2020; DOI: https://doi.org/10.1007/s12275-020-9423-x

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Abstract

A grey pink colored bacterium, strain t3-1-3T, was isolated from the air at the foot of the Xiangshan Mountain in Beijing, China. The cells are aerobic, Gram-stain-negative, non-sporeforming, motile and coccoid-rod shaped (0.9–1.2 × 1.9–2.1 μm). Strain t3-1-3T was catalase-positive and oxidase-negative and this strain grew at 4–42°C (optimum 28°C), a pH of 4.0–9.0 (optimum pH 7.0) and under 0–2% (w/v) NaCl (optimum 0–1% NaCl). A phylogenetic analysis based on 16S rRNA gene sequences revealed that strain t3-1-3T was closely related to Azohydromonas riparia UCM-11T (97.4% similarity), followed by Azohydromonas australica G1-2T (96.8%) and Azohydromonas ureilytica UCM-80T (96.7%). The genome of strain t3-1-3T contains 6,895 predicted protein-encoding genes, 8 rRNA genes, 62 tRNA genes and one sRNA gene, as well as five potential biosynthetic gene clusters, including clusters of genes coding for non-ribosomal peptide synthetase (NRPS), bacteriocin and arylpolyene and two clusters of genes for terpene. The predominant cellular fatty acids (> 10.0% of the total) in strain t3-1-3T were summed feature 3 (C16:1ω7c and/or C16:1ω6c, 37.8%), summed feature 8 (C18:1ω7c and/or C18:1ω6c, 29.7%) and C16:0 (17.3%). Strain t3-1-3T contained ubiquinone-8 (Q-8) as the predominant respiratory quinone. The polar lipids of strain t3-1-3T comprised phosphatidyl ethanolamine (PE), phosphatidyl glycerol (PG), diphosphatidyl glycerol (DPG), an unidentified glycolipid (GL), an unidentified aminophospholipid (APL), two unidentified phospholipid (PL1-2) and five unidentified lipid (L1-5). The DNA G + C content of the type strain is 70.3%. The broader range of growth temperature, assimilation of malic acid and trisodium citrate, presence of C18:3ω6c and an unidentified glycolipid and absence of C12:0 2-OH and C16:0iso differentiate strain t3-1-3T from related species. Based on the taxonomic data presented in this study, we suggest that strain t3-1-3T represents a novel species within the genus Azohydromonas, for which the name Azohydromonas aeria sp. nov. is proposed. The type strain of Azohydromonas aeria is t3-1-3T (= CFCC 13393T = LMG 30135T).

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The phylogeny of the genus Azohydromonas supports its transfer to the family Comamonadaceae
Ezequiel Gerardo Mogro, Juan Hilario Cafiero, Mauricio Javier Lozano, Walter Omar Draghi
International Journal of Systematic and Evolutionary Microbiology.2022;[Epub] CrossRef
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Wenxue Zhang, Yan Shi, Hu Li, Miao Yu, Jiaxuan Zhao, Hao Chen, Ming Kong
Carbohydrate Polymers.2022; 288: 119418. CrossRef
Transformation of N and S pollutants and characterization of microbial communities in constructed wetlands with Vallisneria natans
Feichao Fu, Shaobin Huang, Heping Hu, Yao Lu, Yanlin Wang, Jianqi Yuan, Zerui Gong, Jinhua Wu, Yongqing Zhang
Journal of Water Process Engineering.2021; 42: 102186. CrossRef
Azohydromonas caseinilytica sp. nov., a Nitrogen-Fixing Bacterium Isolated From Forest Soil by Using Optimized Culture Method
Ram Hari Dahal, Dhiraj Kumar Chaudhary, Dong-Uk Kim, Jaisoo Kim
Frontiers in Microbiology.2021;[Epub] CrossRef

Review

MINIREVIEW] Exopolymeric substances (EPS) from Salmonella enterica: polymers, proteins and their interactions with plants and abiotic surfaces: Rugare Maruzani , Gabriel Sutton , Paola Nocerino , Massimiliano Marvasi; J. Microbiol. 2019;57(1):1-8. Published online September 6, 2018; DOI: https://doi.org/10.1007/s12275-019-8353-y

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Abstract

When Salmonella enterica is not in a planktonic state, it persists in organised communities encased in extracellular polymeric substances (EPS), defined as biofilms. Environmental conditions ultimately dictate the key properties of the biofilms such as porosity, density, water content, charge, sorption and ion exchange properties, hydrophobicity and mechanical stability. S. enterica has been extensively studied due to its ability to infect the gastrointestinal environment. However, only during the last decades studies on its persistence and replication in soil, plant and abiotic surfaces have been proposed. S. enterica is an environmental bacterium able to effectively persist outside the human host. It does so by using EPS as tools to cope with environmental fluctuations. We therefore address this mini-review to classify those EPS that are produced by Salmonella with focus on the environment (plant, soil, and abiotic surfaces) by using a classification of EPS proposed by Flemming and collaborators in 2007. The EPS are therefore classified as structural, sorptive, surface-active, active, and informative.

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Gonzalo Tulin, Andrea A.E. Méndez, Nicolás R. Figueroa, Carol Smith, María P. Folmer, Diego Serra, Joseph T. Wade, Susana K. Checa, Fernando C. Soncini
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Antimicrobial activity of Lactobacillus spp. isolated from fermented foods and their inhibitory effect against foodborne pathogens
Athraa Oudah Hussein, Khalida Khalil, Nurul Aqilah Mohd Zaini, Ahmed Khassaf Al Atya, Wan Syaidatul Aqma
PeerJ.2025; 13: e18541. CrossRef
Inhibition of Salmonella Typhimurium biofilm and polysaccharide production via eugenol-glucosyltransferase interactions
Julian Javier Palomares-Navarro, Ariadna Thalia Bernal-Mercado, Cristóbal Joel González-Pérez, Miguel Angel Martínez-Tellez, Gustavo Adolfo Gonzalez-Aguilar, Luis Alberto Ortega-Ramirez, Jesus Fernando Ayala-Zavala
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Biocontrol characteristics and application of phage SEP4 against multidrug-resistant Salmonella biofilm on food matrix
Muhammad Imran Taj, Yifeng Ding, Yuexin Bao, Yingjie Huang, Peng Guan, Yiming Zhang, Xi Liu, Zixin Ming, Xiaohong Wang
Food Bioscience.2024; 60: 104251. CrossRef
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Saumi Pandey, Vinod K. Kannaujiya
International Journal of Biological Macromolecules.2024; 279: 135261. CrossRef
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Rebeca Leme Oliva, Carla Vogt, Tábata Aline Bublitz, Tessa Camenzind, Jens Dyckmans, Rainer Georg Joergensen
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Abhishek Kumar, Asmita Lohia, Shabirul Haque, Lokender Kumar, Azhar Khan
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The quorum sensing molecule C12-HSL promotes biofilm formation and increases adrA expression in Salmonella Enteritidis under anaerobic conditions
Deisy Guimarães Carneiro, Ananda Pereira Aguilar, Hilário Cuquetto Mantovani, Tiago Antônio de Oliveira Mendes, Maria Cristina Dantas Vanetti
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Journal Article

Direct interaction between the transcription factors CadC and OmpR involved in the acid stress response of Salmonella enterica: Yong Heon Lee , Ji Hye Kim; J. Microbiol. 2017;55(12):966-972. Published online December 7, 2017; DOI: https://doi.org/10.1007/s12275-017-7410-7

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Abstract

In Salmonella enterica serovar Typhimurium, the acid-sensing regulator CadC activates transcription of the cadBA operon which contributes to the acid tolerance response. The DNA-binding response regulator OmpR in two-component regulatory system with EnvZ binds to its own promoter for autoinduction. We previously reported that CadC exerts a negative influence on ompR transcription during acid adaptation. However, its underlying mechanisms remain to be elucidated. Here we show that the level of OmpR protein is gradually reduced by a gradual increase in the CadC level using an arabinose-inducible expression system, indicating there exists a negative correlation between the expression levels of two transcription factors. To explore the molecular basis for OmpR repression by CadC, we performed in vitro binding assays and determined that CadC directly interacts with OmpR. We further show that inactivation of cadC inhibits transcription of the fliC gene, which encodes the major flagellar subunit,
result
ing in impaired flagellar motility under acid-adaptation conditions. Together, our findings suggest that CadC may repress autoinduction of the OmpR response regulator through their direct interaction.

Citations

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Isolation and characterization of resistant variants of Salmonella Typhimurium after sequential exposure to plasma activated water (PAW)
Elisa Pagán, Foteini Pavli, Sarah Happiette, Daniel Berdejo, Ruben Gatt, Rafael Pagán, Vasilis Valdramidis, Diego García-Gonzalo
Innovative Food Science & Emerging Technologies.2024; 93: 103633. CrossRef
A current insight into Salmonella’s inducible acid resistance
Alkmini Gavriil, Ilias Giannenas, Panagiotis N. Skandamis
Critical Reviews in Food Science and Nutrition.2024; : 1. CrossRef
Molecular mechanism of proteolytic cleavage-dependent activation of CadC-mediated response to acid in E. coli
Min Chen, Ye Shang, Wenhao Cui, Xiaomeng Wang, Jiakun Zhu, Hongjie Dong, Hongwei Wang, Tiantian Su, Weiwei Wang, Kundi Zhang, Bingqing Li, Sujuan Xu, Wei Hu, Fengyu Zhang, Lichuan Gu
Communications Biology.2024;[Epub] CrossRef
Transmembrane Transcription Regulators Are Widespread in Bacteria and Archaea
Lucas M. Demey, Vadim M. Gumerov, Jiawei Xing, Igor B. Zhulin, Victor J. DiRita, Beile Gao
Microbiology Spectrum.2023;[Epub] CrossRef
Host acid signal controls Salmonella flagella biogenesis through CadC-YdiV axis
Weiwei Wang, Yingying Yue, Min Zhang, Nannan Song, Haihong Jia, Yuanji Dai, Fengyu Zhang, Cuiling Li, Bingqing Li
Gut Microbes.2022;[Epub] CrossRef
Recent advances in understanding the effect of acid-adaptation on the cross-protection to food-related stress of common foodborne pathogens
Ricardo A. Wu, Hyun-Gyun Yuk, Donghong Liu, Tian Ding
Critical Reviews in Food Science and Nutrition.2022; 62(26): 7336. CrossRef
Metabolic adaptability shifts of cell membrane fatty acids of Komagataeibacter hansenii HDM1-3 improve acid stress resistance and survival in acidic environments
Yuanjing Li, Pengfei Yan, Qingyun Lei, Bingyu Li, Yue Sun, Shuangfei Li, Hong Lei, Ning Xie
Journal of Industrial Microbiology and Biotechnology.2019; 46(11): 1491. CrossRef

Research Support, Non-U.S. Gov'ts

Immune Response Induced by ppGpp-Defective Salmonella enterica serovar Gallinarum in Chickens: Sang-Ik Park , Jae-Ho Jeong , Hyon E. Choy , Joon Haeng Rhee , Hee-Sam Na , Tae-Hoon Lee , Moon Her , Kyoung-Oh Cho , Yeongjin Hong; J. Microbiol. 2010;48(5):674-681. Published online November 3, 2010; DOI: https://doi.org/10.1007/s12275-010-0179-6

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Abstract: To protect chickens from typhoid caused by Salmonella enterica serovar Gallinarum (S. Gallinarum), the attenuated 9R strain has been used in the field as a vaccine. However, safety concerns have been raised because the mutations in 9R are undefined while its efficacy is still a question under debate. A global regulator, ppGpp, synthesized by RelA and SpoT, has been shown to induce various virulence genes in S. Gallinarum (Jeong et al., 2008). In this study, two mutant strains defective in ppGpp-synthesis were constructed in wild-type S. Gallinarum (∆ppGpp) and 9R strain (9R-∆ppGpp) backgrounds and tested as live vaccines in chickens. After oral inoculation, the LD50 values of ∆ppGpp and 9R-∆ppGpp were approximately 5×1010 colony forming unit (CFU) similarly as 9R strain, which was ~105-fold higher than that of the wildtype S. Gallinarum strain. Immunological analyses revealed immunization with either of the two attenuated ppGpp-defective strains induced significant antibody responses, the production of antibody-secreting B cells in blood, proliferation of CD4+ and CD8+ T cells in the spleen, and splenic expression of proinflammatory cytokines, such as IFN-γ and TGF-β4, at levels comparable to the 9R strain. Chickens immunized with the mutants (1×108 CFU) were 80% protected against oral challenge with 1×109 wild-type virulent bacteria (4,000-fold LD50 dose), similar to the level of protection achieved by 9R immunization. Based on these data, live attenuated ∆ppGpp-defective strains may serve as novel vaccines to control fowl typhoid in chickens.

Immunological Responses Induced by asd and wzy/asd Mutant Strains of Salmonella enterica serovar Typhimurium in BALB/c Mice: Hong Hua Piao , Vo Thi Minh Tam , Hee Sam Na , Hyun Ju Kim , Phil Youl Ryu , Soo Young Kim , Joon Haeng Rhee , Hyon E. Choy , Suhng Wook Kim , Yeongjin Hong; J. Microbiol. 2010;48(4):486-495. Published online August 20, 2010; DOI: https://doi.org/10.1007/s12275-010-0023-z

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Abstract: Attenuated bacteria have long been developed as vaccine candidates but can have some disadvantages, such as the potential for damage to immune organs due to insufficient clearance. To minimize these disadvantages, we generated Salmonella enterica serovar Typhimurium mutants SHJ2104 (asd::cm) and HTSaYA (wzy::km, asd::cm). The wzy gene codes for the O-antigen polymerase, which is involved in lipopolysaccharide (LPS) biosynthesis, and asd codes for aspartate ß- semialdehyde dehydrogenase, which participates in cell wall formation. The strains synthesized LPS with a short-chain length, and showed lower cytotoxicity and reduced intracellular proliferation in animal cells compared to wild-type bacteria. After oral infection, the mutants were cleared in immune tissues, including the Peyer’s patch, mesenteric lymph node, and spleen, within 5 days. The LD50 of the mutants in Balb/c mice was estimated to be 106 higher than wild-type bacteria when administered either via an oral or i.p. route, indicating that the two strains are highly attenuated. To compare the immune response to and protective effects of the mutants against wild-type bacterial infection, we inoculated the mutants into mice via an oral (1×1010 CFU) or i.p. (1×107 CFU) route once or twice at a two week interval. All immune responses, such as serum IgG and secretory IgA levels, cytokine production, and delayed hypersensitivity, were highly induced by two rounds of immunization. HTSaYA and SHJ2104 induced similar immune responses, and mice immunized with HTSaYA or SHJ2104 via an i.p. route were protected against wild-type Salmonella infection even at 100-fold of the LD50 (5×106 CFU). Taken together, these data indicate that HTSaYA and SHJ2104 could be developed as live attenuated Salmonella vaccine candidates.

Adaptation and Cross-Adaptation of Listeria monocytogenes and Salmonella enterica to Poultry Decontaminants: Alicia Alonso-Hernando , Rosa Capita , Miguel Prieto , Carlos Alonso-Calleja; J. Microbiol. 2009;47(2):142-146. Published online May 2, 2009; DOI: https://doi.org/10.1007/s12275-008-0237-5

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Abstract: Information on the potential for acquired reduced susceptibility of bacteria to poultry decontaminants occurring is lacking. Minimal Inhibitory Concentrations (MICs) were established for assessing the initial susceptibility and the adaptative and cross-adaptative responses of four bacterial strains (Listeria monocytogenes serovar 1/2a, L. monocytogenes serovar 4b, Salmonella enterica serotype Typhimurium, and S. enterica serotype Enteritidis) to four poultry decontaminants (trisodium phosphate, acidified sodium chlorite -ASC-, citric acid, and peroxyacetic acid). The initial susceptibility was observed to differ among species (all decontaminants) and between Salmonella strains (ASC). These inter- and intra-specific variations highlight (1) the need for strict monitoring of decontaminant concentrations to inactivate all target pathogens of concern, and (2) the importance of selecting adequate test strains in decontamination studies. MICs of ASC (0.17±0.02 to 0.21±0.02 mg/ml) were higher than the U.S. authorized concentration when applied as a pre-chiller or chiller solution (0.05 to 0.15 mg/ml). Progressively increasing decontaminant concentrations resulted in reduced susceptibility of strains. The highest increase in MIC was 1.88 to 2.71-fold (ASC). All decontaminants were shown to cause cross-adaptation of strains between both related and unrelated compounds, the highest increase in MIC being 1.82-fold (ASC). Our results suggest that the in-use concentrations of ASC could, in certain conditions, be ineffective against Listeria and Salmonella strains. The adaptative and cross-adaptative responses of strains tested to poultry decontaminants are of minor concern. However, the observations being presented here are based on in vitro studies, and further research into practical applications are needed in order to confirm these findings.

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