Journal of Microbiology

Volume 61(4); April 2023

Review

Bacterial Sialic Acid Catabolism at the Host–Microbe Interface: Jaeeun Kim , Byoung Sik Kim; J. Microbiol. 2023;61(4):369-377. Published online March 27, 2023; DOI: https://doi.org/10.1007/s12275-023-00035-7

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Abstract: Sialic acids consist of nine-carbon keto sugars that are commonly found at the terminal end of mucins. This positional feature of sialic acids contributes to host cell interactions but is also exploited by some pathogenic bacteria in evasion of host immune system. Moreover, many commensals and pathogens use sialic acids as an alternative energy source to survive within the mucus-covered host environments, such as the intestine, vagina, and oral cavity. Among the various biological events mediated by sialic acids, this review will focus on the processes necessary for the catabolic utilization of sialic acid in bacteria. First of all, transportation of sialic acid should be preceded before its catabolism. There are four types of transporters that are used for sialic acid uptake; the major facilitator superfamily (MFS), the tripartite ATP-independent periplasmic C4-dicarboxilate (TRAP) multicomponent transport system, the ATP binding cassette (ABC) transporter, and the sodium solute symporter (SSS). After being moved by these transporters, sialic acid is degraded into an intermediate of glycolysis through the well-conserved catabolic pathway. The genes encoding the catabolic enzymes and transporters are clustered into an operon(s), and their expression is tightly controlled by specific transcriptional regulators. In addition to these mechanisms, we will cover some researches about sialic acid utilization by oral pathogens.

Journal Articles

Descr!ption of Ornithinimicrobium cryptoxanthini sp. nov., a Novel Actinomycete Producing β‑cryptoxanthin Isolated from the Tongtian River Sediments: Yuyuan Huang , Yifan Jiao , Sihui Zhang , Yuanmeihui Tao , Suping Zhang , Dong Jin , Ji Pu , Liyun Liu , Jing Yang , Shan Lu; J. Microbiol. 2023;61(4):379-388. Published online March 16, 2023; DOI: https://doi.org/10.1007/s12275-023-00029-5

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Abstract: Two novel Gram-stain-positive, aerobic, non-motile, and yellow-pigmented, irregular rod-shaped bacteria (JY.X269 and JY.X270T) were isolated from the near-surface sediments of river in Qinghai Province, P. R. China (32°37′13″N, 96°05′37″E) in July 2019. Both strains were shown to grow at 15–35 °C and pH 7.0–10.0, and in the presence of 0–6.0% (w/v) NaCl. The 16S rRNA gene sequence analysis showed that the isolates were closely related to Ornithinimicrobium cavernae CFH 30183 T (98.6–98.8% 16S rRNA gene sequence similarity), O. ciconiae H23M54T (98.5–98.6%) and O. murale 01-Gi-040T (98.3–98.5%). The phylogenetic and phylogenomic trees based on the 16S rRNA gene and 537 core gene sequences, respectively, revealed that the two strains formed a distinct cluster with the above three species. The digital DNA-DNA hybridization (dDDH) and average nucleotide identity (ANI) values between our two isolates (JY.X269 and JY.X270T) and other Ornithinimicrobium species were within the ranges of 19.0–23.9% and 70.8–80.4%, respectively, all below the respective recommended 70.0% and 95–96% cutoff point. Furthermore, the major cellular fatty acids (> 10.0%) of strains JY.X269 and JY.X270T were iso-C15:0, iso-C16:0, and summed feature 9. Strain JY.X270T contained MK-8(H4) and ornithine as the predominant menaquinone and diagnostic diamino acid component within the cell wall teichoic acids. β-cryptoxanthin ( C40H56O) can be extracted from strain JY.X270T, and its content is 6.3 μg/ml. Based on results from the phylogenetic, chemotaxonomic, and phenotypic analyses, the two strains could be classified as a novel species of the genus Ornithinimicrobium, for which the name Ornithinimicrobium cryptoxanthini sp. nov. is proposed (type strain JY.X270T = CGMCC 1.19147T = JCM 34882T).

Rhizosphere Microbial Community and Metabolites of Susceptible and Resistant Tobacco Cultivars to Bacterial Wilt: Wan Zhao , Yanyan Li , Chunlei Yang , Yong Yang , Yun Hu; J. Microbiol. 2023;61(4):389-402. Published online March 7, 2023; DOI: https://doi.org/10.1007/s12275-023-00012-0

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Abstract: Soil-borne diseases are closely related to rhizosphere microecosystem. While, plant species and genotypes are important factors affected rhizosphere microecosystem. In this study, the rhizosphere soil microbial community and metabolites of susceptible and resistant tobacco cultivars were investigated. The results showed that there were significant differences in the rhizosphere microbial community and metabolites between susceptible cultivar Yunyan87 and resistant cultivar Fandi3. Furthermore, the rhizosphere soil of Fandi3 showed a higher microbial diversity than that of Yunyan87. The abundance of R. solanacearum was much higher in the rhizosphere soil of Yunyan87 than in the rhizosphere soil of Fandi3, resulting in a higher disease incidence and index. While the abundance of beneficial bacteria in the rhizosphere soil of Fandi3 were higher than that of Yunyan87. Additionally, there were significant differences in metabolites between Yunyan87 and Fandi3 cultivars, and 4-hydroxybenzaldehyde, 3-hydroxy-4-methoxybenzoic acid, vamillic aldehyde, benzoic acid, 4-hydroxybenzyl alcohol, p-hydroxybenzoic acid and phthalic acid were notably high in Yunyan87. Redundancy analysis (RDA) indicated that the rhizosphere microbial community of Fandi3 and Yunyan87 were highly correlated with various environmental factors and metabolites. Overall, susceptible and resistant tobacco cultivars had different impact on rhizosphere microbial community and metabolites. The results expand our understanding of the roles of tobacco cultivars in plant-micro-ecosystem interactions, and provide a basis for the control of tobacco bacterial wilt.

Review

Apoptotic Factors, CaNma111 and CaYbh3, Function in Candida albicans Filamentation by Regulating the Hyphal Suppressors, Nrg1 and Tup1: Suyoung Kim , Se Hyeon Kim , Eunjoong Kweon , Jinmi Kim; J. Microbiol. 2023;61(4):403-409. Published online March 27, 2023; DOI: https://doi.org/10.1007/s12275-023-00034-8

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Abstract: The morphological switch from the yeast to hyphal form is a key virulence attribute of the opportunistic fungal pathogen, Candida albicans. Our recent report showed that deletion of the newly identified apoptotic factor, CaNma111 or CaYbh3, leads to hyperfilamentation and increased virulence in a mouse infection model. CaNma111 and CaYbh3 are homologs of the pro-apoptotic protease, HtrA2/Omi, and BH3-only protein, respectively. In this study, we examined the effects of CaNMA111 and CaYBH3 deletion mutations on the expression levels of the hypha-specific transcr!ption factors, Cph1 (a hyphal activator), Nrg1 (a hyphal repressor), and Tup1 (a hyphal repressor). The protein levels of Nrg1 were decreased in Caybh3/Caybh3 cells while those of Tup1 were decreased in both Canma111/Canma111 and Caybh3/Caybh3 cells. These effects on Nrg1 and Tup1 proteins were retained during serum-induced filamentation and appear to explain the hyperfilamentation phenotypes of the CaNMA111 and CaYBH3 deletion mutants. Treatment with the apoptosis-inducing dose of farnesol decreased the Nrg1 protein levels in the wild-type strain and more evidently in Canma111/Canma111 and Caybh3/Caybh3 mutant strains. Together, our results suggest that CaNma111 and CaYbh3 are key regulators of Nrg1 and Tup1 protein levels in C. albicans.

Journal Articles

Identification and Characterization of HEPN‑MNT Type II TA System from Methanothermobacter thermautotrophicus ΔH: Wonho Choi , Anoth Maharjan , Hae Gang Im , Ji-Young Park , Jong-Tae Park , Jung-Ho Park; J. Microbiol. 2023;61(4):411-421. Published online April 18, 2023; DOI: https://doi.org/10.1007/s12275-023-00041-9

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Abstract: Toxin-antitoxin (TA) systems are widespread in bacteria and archaea plasmids and genomes to regulate DNA replication, gene transcr!ption, or protein translation. Higher eukaryotic and prokaryotic nucleotide-binding (HEPN) and minimal nucleotidyltransferase (MNT) domains are prevalent in prokaryotic genomes and constitute TA pairs. However, three gene pairs (MTH304/305, 408/409, and 463/464) of Methanothermobacter thermautotropicus ΔH HEPN-MNT family have not been studied as TA systems. Among these candidates, our study characterizes the MTH463/MTH464 TA system. MTH463 expression inhibited Escherichia coli growth, whereas MTH464 did not and blocked MTH463 instead. Using site-directed MTH463 mutagenesis, we determined that amino acids R99G, H104A, and Y106A from the R[ɸX]4-6H motif are involved with MTH463 cell toxicity. Furthermore, we established that purified MTH463 could degrade MS2 phage RNA, whereas purified MTH464 neutralized MTH463 activity in vitro. Our results indicate that the endonuclease toxin MTH463 (encoding a HEPN domain) and its cognate antitoxin MTH464 (encoding the MNT domain) may act as a type II TA system in M. thermautotropicus ΔH. This study provides initial and essential information studying TA system functions, primarily archaea HEPN-MNT family.

Vaginal Microbiome Dysbiosis is Associated with the Different Cervical Disease Status: Yingying Ma , Yanpeng Li , Yanmei Liu , Le Cao , Xiao Han , Shujun Gao , Chiyu Zhang; J. Microbiol. 2023;61(4):423-432. Published online April 3, 2023; DOI: https://doi.org/10.1007/s12275-023-00039-3

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Abstract: Vaginal microbiome composition was demonstrated to be associated with cervical disease. The colonization characteristics of vaginal microbes and their association with the different cervical disease status, especially cervical cancer (CC), are rarely investigated. In this cross-sectional study, we characterized the vaginal microbiome of women with different status of cervical diseases, including 22 NV + (normal tissue with HPV infection), low-grade squamous intraepithelial lesion (LSIL, n = 45), high-grade squamous intraepithelial lesion (HSIL, n = 36) and CC (n = 27) using bacterial 16S DNA sequencing. Thirty HPV-negative women with normal tissue were used as the control group. We found that higher diversity of microbiome with gradual depletion of Lactobacillus, especially L. crispatus, was associated with the severity of cervical disease. High-risk HPV16 infection was associated with higher microbiome diversity and depletion of Lactobacillus in high-grade cervical diseases (i.e. HSIL and CC). The CC group was characterized by higher levels of Fannyhessea vaginae, Prevotella, Bacteroides, Finegoldia, Vibrio, Veillonella, Peptostreptococcus, and Dialister. Co-occurrence network analyses showed that negative correlations were exclusively observed between Lactobacillus and other bacteria, and almost all non-Lactobacillus bacteria were positively correlated with each other. In particular, the most diverse and complex co-occurrence network of vaginal bacteria, as well as a complete loss of L. crispatus, was observed in women with CC. Logistic regression model identified HPV16 and Lactobacillus as significant risk and protective factors for CC, respectively. These results suggest that specific Lactobacillus species (e.g. L. crispatus and L. iners) can be used as important markers to target prevention measures prioritizing HPV16-infected women and other hrHPV-infected women for test, vaccination and treat initiatives.

Thioredoxin A of Streptococcus suis Serotype 2 Contributes to Virulence by Inhibiting the Expression of Pentraxin 3 to Promote Survival Within Macrophages: Chijun Zhao , Xinglin Jia , Yanying Pan , Simeng Liao , Shuo Zhang , Chunxiao Ji , Guangwei Kuang , Xin Wu , Quan Liu , Yulong Tang , Lihua Fang; J. Microbiol. 2023;61(4):433-448. Published online April 3, 2023; DOI: https://doi.org/10.1007/s12275-023-00038-4

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Abstract: Streptococcus suis serotype 2 (SS2) is an important zoonotic pathogen that can infect humans in contact with infected pigs or their byproducts. It can employ different types of genes to defend against oxidative stress and ensure its survival. The thioredoxin (Trx) system is a key antioxidant system that contributes adversity adaptation and pathogenicity. SS2 has been shown to encode putative thioredoxin genes, but the biological roles, coding sequence, and underlying mechanisms remains uncharacterized. Here, we demonstrated that SSU05_0237-ORF, from a clinical SS2 strain, ZJ081101, encodes a protein of 104 amino acids with a canonical CGPC active motif and an identity 70–85% similar to the thioredoxin A (TrxA) in other microorganisms. Recombinant TrxA efficiently catalyzed the thiol-disulfide oxidoreduction of insulin. The deletion of TrxA led to a significantly slow growth and markedly compromised tolerance of the pathogen to temperature stress, as well as impaired adhesion ability to pig intestinal epithelial cells (IPEC-J2). However, it was not involved in H2O2 and paraquat-induced oxidative stress. Compared with the wild-type strain, the ΔTrxA strain was more susceptible to killing by macrophages through increasing NO production. Treatment with TrxA mutant strain also significantly attenuated cytotoxic effects on RAW 264.7 cells by inhibiting inflammatory response and apoptosis. Knockdown of pentraxin 3 in RAW 264.7 cells was more vulnerable to phagocytic activity, and TrxA promoted SS2 survival in phagocytic cells depending on pentraxin 3 activity compared with the wild-type strain. Moreover, a co-inoculation experiment in mice revealed that TrxA mutant strain is far more easily cleared from the body than the wild type strain in the period from 8–24 h, and exhibits significantly attenuated oxidative stress and liver injury. In summary, we reveal the important role of TrxA in the pathogenesis of SS2.

Comparison of Ganoderma boninense Isolate’s Aggressiveness Using Infected Oil Palm Seedlings: Mei Lieng Lo , Tu Anh Vu Thanh , Frazer Midot , Sharon Yu Ling Lau , Wei Chee Wong , Hun Jiat Tung , Mui Sie Jee , Mei-Yee Chin , Lulie Melling; J. Microbiol. 2023;61(4):449-459. Published online April 25, 2023; DOI: https://doi.org/10.1007/s12275-023-00040-w

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Abstract: Basal stem rot incidence caused by a white-rot fungus, Ganoderma boninense, is the major disease of oil palm in Southeast Asia. The rate of disease transmission and host damage are affected by variations in pathogen aggressiveness. Several other studies have used the disease severity index (DSI) to determine G. boninense aggressiveness levels while verifying disease using a culture-based method, which might not provide accurate results or be feasible in all cases. To differentiate G. boninense aggressiveness, we employed the DSI and vegetative growth measurement of infected oil palm seedlings. Disease confirmation was performed through scanning electron microscopy and molecular identification of fungal DNA from both infected tissue and fungi isolated from Ganoderma selective medium. Two-month-old oil palm seedlings were artificially inoculated with G. boninense isolates (2, 4A, 5A, 5B, and 7A) sampled from Miri (Lambir) and Mukah (Sungai Meris and Sungai Liuk), Sarawak. The isolates were categorized into three groups: highly aggressive (4A and 5B), moderately aggressive (5A and 7A), and less aggressive (2). Isolate 5B was identified as the most aggressive, and it was the only one to result in seedling mortality. Out of the five vegetative growth parameters measured, only the bole size between treatments was not affected. The integration of both conventional and molecular approaches in disease confirmation allows for precise detection.

CXCL12/CXCR4 Axis is Involved in the Recruitment of NK Cells by HMGB1 Contributing to Persistent Airway Inflammation and AHR During the Late Stage of RSV Infection: Sisi Chen , Wei Tang , Guangyuan Yu , Zhengzhen Tang , Enmei Liu; J. Microbiol. 2023;61(4):461-469. Published online February 13, 2023; DOI: https://doi.org/10.1007/s12275-023-00018-8

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Abstract: We previously showed that both high-mobility group box-1 (HMGB1) and natural killer (NK) cells contribute to respiratory syncytial virus (RSV)-induced persistent airway inflammation and airway hyperresponsiveness (AHR). Meanwhile, Chemokine (C-X-C motif) ligand 12 (CXCL12) and its specific receptor (chemokine receptor 4, CXCR4) play important roles in recruitment of immune cells. CXCL12 has been reported to form a complex with HMGB1 that binds to CXCR4 and increases inflammatory cell migration. The relationship between HMGB1, NK cells and chemokines in RSV-infected model remains unclear. An anti-HMGB1 neutralizing antibody and inhibitor of CXCR4 (AMD3100) was administered to observe changes of NK cells and airway disorders in nude mice and BALB/c mice. Results showed that the mRNA expression and protein levels of HMGB1 were elevated in late stage of RSV infection and persistent airway inflammation and AHR were diminished after administration of anti-HMGB1 antibodies, with an associated significant decrease in CXCR4+ NK cells. In addition, CXCL12 and CXCR4 were reduced after HMGB1 blockade. Treatment with AMD3100 significantly suppressed the recruitment of NK cells and alleviated the airway disorders. Thus, CXCL12/CXCR4 axis is involved in the recruitment of NK cells by HMGB1, contributing to persistent airway inflammation and AHR during the late stage of RSV infection.

Epidemiological Characteristics of Norovirus Outbreaks in Shenyang from 2017 to 2021: Ying Qi , Xinxin Dong , Xiaowei Cheng , Han Xu , Jin Wang , Bing Wang , Ye Chen , Baijun Sun , Linlin Zhang , Yan Yao; J. Microbiol. 2023;61(4):471-478. Published online March 27, 2023; DOI: https://doi.org/10.1007/s12275-023-00033-9

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Abstract: Norovirus is one of the leading causes of acute gastroenteritis outbreaks worldwide. This study aimed to identify the epidemiological characteristics of norovirus outbreaks and to provide evidence for public health entities. Specimens and epidemiological survey data were collected to determine if there were differences in the attack rate of norovirus in terms of the year, season, transmission route, exposure setting, and region and to determine whether there were relationships between the reporting interval, the number of illnesses in a single outbreak and the duration of the outbreak. Norovirus outbreaks were reported throughout the year, with seasonal characteristics (i.e., high rates in spring and winter). Among all regions in Shenyang with the exception of Huanggu and Liaozhong, norovirus outbreaks had been reported, and the primary genotype was GII.2[P16]. Vomiting was the most common symptom. The main places of occurrence were childcare institutions and schools. The person-to-person route was the main transmission route. The median duration of norovirus was 3 days (IQR [interquartile range]: 2–6 days), the median reporting interval was 2 days (IQR: 1–4 days), the median number of illnesses in a single outbreak was 16 (IQR: 10–25); there was a positive correlation between these parameters. Norovirus surveillance and genotyping studies still need to be further strengthened to increase knowledge regarding the pathogens and their variant characteristics, to better characterize the patterns of norovirus outbreaks and to provide information for outbreak prevention. Norovirus outbreaks should be detected, reported and handled early. Public health entities and the government should develop corresponding measures for different seasons, transmission routes, exposure settings, and regions.

Published Erratum

Erratum: Secretions from Serratia marcescens Inhibit the Growth and Biofilm Formation of Candida spp. and Cryptococcus neoformans: Caiyan Xin , Fen Wang , Jinping Zhang , Quan Zhou , Fangyan Liu , Chunling Zhao , Zhangyong Song; J. Microbiol. 2023;61(4):479-479.; DOI: https://doi.org/10.1007/s12275-023-00037-5

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Abstract: Erratum: Journal of Microbiology (2023) 61:221–232 https://doi.org/10.1007/s12275-022-00007-3 In this article the acknowledgment has been given erroneously. It should be read as follows: This research was supported financially by the Sichuan Science and Technology Program (2023NSFSC1698, 2023NSFSC0529, 2022NSFSC1539, and 2022YFS0629) and Luzhou (2021-JYJ-73 and 2022-JYJ-159), the Technology Strategic Cooperation Project of Luzhou Municipal People’s Government Southwest Medical University (2020LZXNYDJ38 and 2020LZXNYDJ23), and the Foundation of Southwest Medical University (2021ZKMS008, 2022QN042, 2022QN085, 2022QN102, and 2022QN118). The original article has been corrected.

Retraction of Publication

Retraction Note to: Cryptic prophages in a blaNDM‑1‑bearing plasmid increase bacterial survival against high NaCl concentration, high and low temperatures, and oxidative and immunological stressors: So Yeon Kim , Kwan Soo Ko; J. Microbiol. 2023;61(4):481-481.; DOI: https://doi.org/10.1007/s12275-023-00049-1

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Abstract: Retraction Note to: Journal of Microbiology (2020) Vol. 58, No. 6, pp. 483–488 https://doi.org/10.1007/s12275-020-9605-6 The Editor-in-Chief has retracted this article at the request of the authors. After publication concerns were raised that prophage sequences do not exist in the genome of the plasmid pNDM-A1 used in this study. The authors have not been able to confirm the existence of prophage sequences in the plasmid. As a result, the Editor-in-Chief no longer has confidence in the results and conclusions presented in this article. Kwan Soo Ko agrees with this retraction. So Yeon Kim has not responded to correspondence from the Editor-in-Chief about this retraction.

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