Journal of Microbiology

Volume 58(8); August 2020

Review

Recent advances in the development of β-lactamase inhibitors: Shivakumar S. Jalde , Hyun Kyung Choi; J. Microbiol. 2020;58(8):633-647. Published online July 27, 2020; DOI: https://doi.org/10.1007/s12275-020-0285-z

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Abstract: β-Lactam antibiotics are the most commonly prescribed antibiotics worldwide; however, antimicrobial resistance (AMR) is a global challenge. The β-lactam resistance in Gram-negative bacteria is due to the production of β-lactamases, including extended-spectrum β-lactamases, metallo-β-lactamases, and carbapenem-hydrolyzing class D β-lactamases. To restore the efficacy of BLAs, the most successful strategy is to use them in combination with β-lactamase inhibitors (BLI). Here we review the medically relevant β-lactamase families and penicillins, diazabicyclooctanes, boronic acids, and novel chemical scaffold-based BLIs, in particular approved and under clinical development.

Journal Articles

Production and characterization of melanin pigments derived from Amorphotheca resinae: Jeong-Joo Oh , Jee Young Kim , Sun Lul Kwon , Dong-Hyeok Hwang , Yoon-E Choi , Gyu-Hyeok Kim; J. Microbiol. 2020;58(8):648-656. Published online May 18, 2020; DOI: https://doi.org/10.1007/s12275-020-0054-z

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Abstract: As melanin has emerged as functional pigment with cosmetic, health and food applications, the demand for the pigments is expected to increase. However, the conventional sources (e.g. mushroom, hair, and wool) of melanin production entail pigments inside the substrates which requires the costly extraction procedures, leading to inappropriate scalable production. In this study, we screened 102 of fungal isolates for their ability to produce melanin in the supernatant and selected the only Amorphotheca resinae as a promising candidate. In the peptone yeast extract glucose broth, A. resinae produced the melanin rapidly during the autolysis phase of growth, reaching up 4.5 g/L within 14 days. Structural characterization of the purified melanin from A. resinae was carried out by using elemental analysis, electron paramagnetic resonance, 13C solid-state nuclear magnetic resonance spectroscopy, and pyrolysis-gas chromatography-mass spectrometry in comparison with the standard melanins. The results indicate that the structural properties of A. resinae melanin is similar to the eumelanin which has a wide range of industrial uses. For example, the purified melanin from A. resinae has the potent antioxidant activities as a result of free radical scavenging assays. Consequently, A. resinae KUC3009 can be a promising candidate for scalable production of industrially applicable melanin.

Short-term effects of returning granulated straw on soil microbial community and organic carbon fractions in dryland farming: Wei Fan , Jinggui Wu; J. Microbiol. 2020;58(8):657-667. Published online June 25, 2020; DOI: https://doi.org/10.1007/s12275-020-9266-5

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Abstract: We conducted a 2-year field experiment which was comprised of five treatments, namely no straw returning (CK), straw mulching (SM), straw plowed into the soil (SP), and straw returned in granulated form (SG). The aim of this study was to investigate the effects of different straw returning modes on soil bacterial and fungal community structure and their relationships to soil organic carbon (SOC) fractions at three different soil depths (0–20, 20–40, and 40–60 cm) in a dryland under maize cultivation in Northeast (NE) China. SM, SP, and SG treatments significantly increased SOC content. Compared with SM and SP treatments, SG treatment significantly increased the content of SOC and easily oxidizable carbon (EOC) in the topsoil (0–20 cm depth), and increased dissolved organic carbon (DOC) and SOC content of the light fraction (LFOC) in the 20–40 cm layer. Meanwhile, SG treatment exhibited the highest microbial biomass C (MBC) content in all of the three soil depths. SG treatment also enhanced bacterial richness as well as fungal richness and diversity in the upper 40 cm of soil. In addition, SG treatment increased the relative abundance of Proteobacteria in all depths, and had the highest relative abundance of Basidiomycota in the first 20 cm of soil. SP treatment showed the lowest soil organic carbon content in all fractions and soil microbial community composition. SM treatment exhibited similar results to SG treatment in SOC, DOC, and LFOC contents, and bacterial diversity in the topsoil and subsoil. As a whole, treatment SG improved soil quality and maize yield, hence we recommend returning granulated straw as the most effective practice for enhancing labile SOC fractions as well as maintaining soil diversity and microbial richness of arid farmlands in NE China.

Simultaneous detection of Salmonella spp., Pseudomonas aeruginosa, Bacillus cereus, and Escherichia coli O157:H7 in environmental water using PMA combined with mPCR: Guoyang Xie , Shuang Yu , Wen Li , Dan Mu , Zoraida P. Aguilar , Hengyi Xu; J. Microbiol. 2020;58(8):668-674. Published online June 25, 2020; DOI: https://doi.org/10.1007/s12275-020-0084-6

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Abstract: A multiplex polymerase chain reaction (mPCR) with propidium monoazide (PMA) and internal amplification control (IAC) for the simultaneous detection of waterborne pathogens Salmonella spp., Pseudomonas aeruginosa, Bacillus cereus, and Escherichia coli O157:H7, was developed. This PMA-IAC-mPCR assay used four new specific primers based on the genes for invA, ecfX, cesB, and fliC, respectively. A 16S rRNA primer was chosen for IAC to eliminate false negative
results
. The photosensitive dye, propidium monoazide (PMA) was used to exclude signals from dead bacteria that could lead to false positive results. In pure culture, the limits of detection (LOD) were 101 CFU/ml for P. aeruginosa, 102 CFU/ml for both Salmonella spp. and E. coli O157:H7, and 103 CFU/ml for B. cereus, respectively. In addition, with a 6–8 h enrichment of all four bacteria that were combined in a mixture that was spiked in water sample matrix, the LOD was 3 CFU/ml for Salmonella spp., 7 CFU/ml for E. coli O157:H7, 10 CFU/ml for B. cereus and 2 CFU/ml for P. aeruginosa. This PMA-IAC-mPCR assay holds potential for application in the multiplex assay of waterborne pathogens.

In vitro disinfection efficacy and clinical protective effects of common disinfectants against acute hepatopancreatic necrosis disease (AHPND)-causing Vibrio isolates in Pacific white shrimp Penaeus vannamei: Peizhuo Zou , Qian Yang , Hailiang Wang , Guosi Xie , Zhi Cao , Xing Chen , Wen Gao , Jie Huang; J. Microbiol. 2020;58(8):675-686. Published online July 27, 2020; DOI: https://doi.org/10.1007/s12275-020-9537-1

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Abstract: Acute hepatopancreatic necrosis disease (AHPND) is one of the most significant bacterial diseases in global shrimp culture, causing severe economic losses. In the present study, we carried out in vitro antimicrobial tests to investigate the disinfection efficacy of 14 common disinfectants toward different AHPND-causing Vibrio spp., including eight isolates of V. parahaemolyticus, four isolates of V. campbellii, and one isolate of V. owensii. Polyhexamethylene biguanidine hydrochloride (PHMB) was revealed to possess the strongest inhibitory activity. Through analyzing and evaluating the results of antimicrobial tests and acute toxicity test, we selected PHMB and hydrogen peroxide (H2O2) for further clinical protection test. Clinical manifestations indicated that both PHMB (2 mg/L and 4 mg/L) and H2O2 (12 mg/L) could effectively protect juvenile Penaeus vannamei from the infection of V. parahaemolyticus isolate Vp362 at 106 CFU/ml, and the survival rate was over 80%. When the bacterial concentration was reduced to 105 CFU/ml, 104 CFU/ml, and 103 CFU/ml, the survival rate after treated by 1 mg/L PHMB was 64.44%, 93.33%, and 100%, respectively. According to the results, PHMB and H2O2 showed a lower toxicity while a better protection activity, particularly against a lower concentration of the pathogens. Therefore, these two disinfectants are proved to be promising disinfectants that can be applied to prevent and control AHPND in shrimp culture. Moreover, the methods of this study also provided valuable information for the prevention of other important bacterial diseases and suggested a reliable means for screening potential drugs in aquaculture.

The effects of deletion of cellobiohydrolase genes on carbon source-dependent growth and enzymatic lignocellulose hydrolysis in Trichoderma reesei: Meibin Ren , Yifan Wang , Guoxin Liu , Bin Zuo , Yuancheng Zhang , Yunhe Wang , Weifeng Liu , Xiangmei Liu , Yaohua Zhong; J. Microbiol. 2020;58(8):687-695. Published online June 10, 2020; DOI: https://doi.org/10.1007/s12275-020-9630-5

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Abstract: The saprophytic fungus Trichoderma reesei has long been used as a model to study microbial degradation of lignocellulosic biomass. The major cellulolytic enzymes of T. reesei are the cellobiohydrolases CBH1 and CBH2, which constitute more than 70% of total proteins secreted by the fungus. However, their physiological functions and effects on enzymatic hydrolysis of cellulose substrates are not sufficiently elucidated. Here, the cellobiohydrolase-encoding genes cbh1 and cbh2 were deleted, individually or combinatively, by using an auxotrophic marker-recycling technique in T. reesei. When cultured on media with different soluble carbon sources, all three deletion strains (Δcbh1, Δcbh2, and Δcbh1Δcbh2) exhibited no dramatic variation in morphological phenotypes, but their growth rates increased apparently when cultured on soluble cellulase-inducing carbon sources. In addition, Δcbh1 showed dramatically reduced growth and Δcbh1Δcbh2 could hardly grew on microcrystalline cellulose (MCC), whereas all strains grew equally on sodium carboxymethyl cellulose (CMC-Na), suggesting that the influence of the CBHs on growth was carbon source-dependent. Moreover, five representative cellulose substrates were used to analyse the influence of the absence of CBHs on saccharification efficiency. CBH1 deficiency significantly affected the enzymatic hydrolysis rates of various cellulose substrates, where acid pre-treated corn stover (PCS) was influenced the least. CBH2 deficiency reduced the hydrolysis of MCC, PCS, and acid pre-treated and delignified corncob but improved the hydrolysis ability of filter paper. These results demonstrate the specific contributions of CBHs to the hydrolysis of different types of biomass, which could facilitate the development of tailor-made strains with highly efficient hydrolysis enzymes for certain biomass types in the biofuel industry.

WasC, a WASP family protein, is involved in cell adhesion and migration through regulation of F-actin polymerization in Dictyostelium: Pyeonghwa Jeon , Taeck Joong Jeon; J. Microbiol. 2020;58(8):696-702. Published online June 10, 2020; DOI: https://doi.org/10.1007/s12275-020-0138-9

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Abstract: The actin cytoskeleton is involved in the regulation of cell morphology and migration. Wiskott-Aldrich Syndrome proteins (WASPs) play an important role in controlling actin polymerization by activating the Arp2/3 complex. The present study investigated the roles of WasC, one of the 3 WASPs in Dictyostelium, in cellular processes. Cells lacking WasC displayed strong cell adhesion and approximately 1.5-fold increase in F-actin levels as compared to the wild-type cells. Loss of wasC caused defects in phagocytosis and decreased the migration speed in chemoattractant-mediated cell migration but did not affect directionality. WasC was localized to the protruding region in migrating cells and, transiently and rapidly translocated to the cell cortex in response to chemoattractant stimulation, in an F-actin dependent manner. Our
results
suggest that WasC is involved in cell adhesion and migration by regulating F-actin polymerization at the leading edge of migrating cells, probably as a negative regulator. The increased strength of adhesion in wasC null cells is likely to decrease the migration speed but not the directionality.

Performance comparison of fecal preservative and stock solutions for gut microbiome storage at room temperature: Chanhyeok Park , Kyeong Eui Yun , Jeong Min Chu , Ji Yeon Lee , Chang Pyo Hong , Young Do Nam , Jinuk Jeong , Kyudong Han , Yong Ju Ahn; J. Microbiol. 2020;58(8):703-710. Published online June 25, 2020; DOI: https://doi.org/10.1007/s12275-020-0092-6

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Abstract: The gut microbiome, which is symbiotic within the human body, assists in human digestion. It plays significant roles in identifying intestinal disease as well as in maintaining a healthy body with functional immune and metabolic activities. To confirm the consistency of fecal intestinal microbial research, it is necessary to study the changes in intestinal microbial flora according to the fecal collection solution and storage period. We collected fecal samples from three healthy Korean adults. To examine the efficacy of fecal collection solution, we used NBgene-Gut, OMNIgene-Gut, 70% ethanol (Ethanol-70%), and RNAlater. The samples were stored for up to two months at room temperature using three different
methods
, and we observed changes in microbial communities over time. We analyzed clusters of changes in the microbial flora by observing fecal stock solutions and metagenome sequencing performed over time. In particular, we confirmed the profiling of alpha and beta diversity and microbial classification according to the differences in intestinal environment among individuals. We also confirmed that the microbial profile remained stable for two months and that the microbial profile did not change significantly over time. In addition, our results suggest the possibility of verifying microbial profiling even for long-term storage of a single sample. In conclusion, collecting fecal samples using a stock solution rather than freezing feces seems to be relatively reproducible and stable for GUT metagenome analysis. Therefore, stock solution tubes in intestinal microbial research can be used without problems.

Development of a real-time loop-mediated isothermal amplification method for the detection of severe fever with thrombocytopenia syndrome virus: Jae Woong Lee , Yu-Jung Won , Lae Hyung Kang , Sung-Geun Lee , Seung-Won Park , Soon-Young Paik; J. Microbiol. 2020;58(8):711-715. Published online May 18, 2020; DOI: https://doi.org/10.1007/s12275-020-0109-1

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Abstract: Severe fever with thrombocytopenia syndrome (SFTS) is being reported annually in South Korea since its first detection there in 2010. The causal agent is a negative-strand RNA virus 80–100 nm in diameter. It causes fever, thrombocytopenia, leukocytopenia, gastrointestinal symptoms, and neural symptoms. The mortality rate of SFTS was 32.6% among 172
case
s reported from 2012 to 2015 in South Korea. Thus, is necessary to develop an effective diagnostic method that selectively identifies the isolates circulating in South Korea. The real-time reverse transcription loop-mediated isothermal amplification (RT-LAMP) assay is a simple, rapid, and sensitive approach for molecular diagnosis. Here, we designed novel primers for this assay and found that the technique had very high specificity, sensitivity, and efficiency. This real-time RTLAMP approach using the novel primers developed herein can be applied for early diagnosis of SFTSV strains in South Korea to reduce the mortality rate of SFTS.

Inhibitory effects of piceatannol on human cytomegalovirus (hCMV) in vitro: San-Ying Wang , Jing Zhang , Xiao-Gang Xu , Hui-Li Su , Wen-Min Xing , Zhong-Shan Zhang , Wei-Hua Jin , Ji-Huan Dai , Ya-Zhen Wang , Xin-Yue He , Chuan Sun , Jing Yan , Gen-Xiang Mao; J. Microbiol. 2020;58(8):716-723. Published online June 10, 2020; DOI: https://doi.org/10.1007/s12275-020-9528-2

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Abstract: Human cytomegalovirus (hCMV) is a ubiquitous herpesvirus, which results in the establishment of a latent infection that persists throughout the life of the host and can be reactivated when the immunity is low. Currently, there is no vaccine for hCMV infection, and the licensed antiviral drugs mainly target the viral enzymes and have obvious adverse reactions. Thus, it is important to search for compounds with antihCMV properties. The present study aimed to investigate the suppressive effects of piceatannol on hCMV Towne strain infection and the putative underlying mechanisms using human diploid fibroblast WI-38 cells. Piceatannol supplementation prevented the lytic changes induced by hCMV infection in WI-38 cells. Furthermore, piceatannol suppressed the expression of hCMV immediate-early (IE) and early (E) proteins as well as the replication of hCMV DNA in a dose-dependent manner. Moreover, hCMV-induced cellular senescence was suppressed by piceatannol, as shown by a decline in the senescence-associated β-galactosidase (SA-β-Gal) activity and decreased production of intracellular reactive oxygen species (ROS). p16INK4a, a major senescence-associated molecule, was dramatically elevated by current hCMV infection that was attenuated by pre-incubation with piceatannol in a dose-dependent manner. These results demonstrated that piceatannol suppressed the hCMV infection via inhibition of the activation of p16INK4a and cellular senescence induced by hCMV. Together, these findings indicate piceatannol as a novel and potent anti-hCMV agent with the potential to be developed as an effective treatment for chronic hCMV infection.

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