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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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AbstractAbstract
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.

Citations

Citations to this article as recorded by  
  • Thioredoxin C of Streptococcus suis serotype 2 contributes to virulence by inducing antioxidative stress and inhibiting autophagy via the MSR1/PI3K-Akt-mTOR pathway in macrophages
    Chunxiao Ji, Yanying Pan, Bocheng Liu, Jianying Liu, Chijun Zhao, Zhuyuan Nie, Simeng Liao, Guangwei Kuang, Xin Wu, Quan Liu, Jie Ning, Yulong Tang, Lihua Fang
    Veterinary Microbiology.2024; 298: 110263.     CrossRef
  • A Comprehensive Review on the Roles of Metals Mediating Insect–Microbial Pathogen Interactions
    Subhanullah Khan, Minglin Lang
    Metabolites.2023; 13(7): 839.     CrossRef
Characterization of a novel dsRNA mycovirus of Trichoderma atroviride NFCF377 reveals a member of “Fusagraviridae” with changes in antifungal activity of the host fungus
Jeesun Chun , Byeonghak Na , Dae-Hyuk Kim
J. Microbiol. 2020;58(12):1046-1053.   Published online October 23, 2020
DOI: https://doi.org/10.1007/s12275-020-0380-1
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  • 9 Web of Science
  • 8 Crossref
AbstractAbstract
Trichoderma atroviride is a common fungus found in various ecosystems that shows mycoparasitic ability on other fungi. A novel dsRNA virus was isolated from T. atroviride NFCF377 strain and its molecular features were analyzed. The viral genome consists of a single segmented double-stranded RNA and is 9,584 bp in length, with two discontinuous open reading frames (ORF1 and ORF2). A mycoviral structural protein and an RNA-dependent RNA polymerase (RdRp) are encoded by ORF1 and ORF2, respectively, between which is found a canonical shifty heptameric signal motif (AAAAAAC) followed by an RNA pseudoknot. Analysis of sequence similarity and phylogeny showed that it is closely related to members of the proposed family “Fusagraviridae”, with a highest similarity to the Trichoderma atroviride mycovirus 1 (TaMV1). Although the sequence similarity of deduced amino acid to TaMV1 was evident, sequence deviations were distinctive at untranslated regions (UTRs) due to the extended size. Thus, we inferred this dsRNA to be a different strain of Trichoderma atroviride mycovirus 1 (TaMV1-NFCF377). Electron microscopy image exhibited an icosahedral viral particle of 40 nm diameter. Virus-cured isogenic isolates were generated and no differences in growth rate, colony morphology, or conidia production were observed between virus-infected and virus-cured strains. However, culture filtrates of TaMV1- NFCF377-infected strain showed enhanced antifungal activity against the plant pathogen Rhizoctonia solani but not to edible mushroom Pleurotus ostreatus. These results suggested that TaMV1-NFCF377 affected the metabolism of the fungal host to potentiate antifungal compounds against a plant pathogen, but this enhanced antifungal activity appeared to be species-specific.

Citations

Citations to this article as recorded by  
  • Co-infection with two novel mycoviruses affects the biocontrol activity of Trichoderma polysporum
    Jeesun Chun, Hae-Ryeong Yoon, Sei-Jin Lee, Dae-Hyuk Kim
    Biological Control.2024; 188: 105440.     CrossRef
  • An Outstandingly Rare Occurrence of Mycoviruses in Soil Strains of the Plant-Beneficial Fungi from the Genus Trichoderma and a Novel Polymycoviridae Isolate
    Chenchen Liu, Xiliang Jiang, Zhaoyan Tan, Rongqun Wang, Qiaoxia Shang, Hongrui Li, Shujin Xu, Miguel A. Aranda, Beilei Wu, Lea Atanasova
    Microbiology Spectrum.2023;[Epub]     CrossRef
  • Sixteen Novel Mycoviruses Containing Positive Single-Stranded RNA, Double-Stranded RNA, and Negative Single-Stranded RNA Genomes Co-Infect a Single Strain of Rhizoctonia zeae
    Siwei Li, Zhihao Ma, Xinyi Zhang, Yibo Cai, Chenggui Han, Xuehong Wu
    Journal of Fungi.2023; 10(1): 30.     CrossRef
  • Trichoderma – genomes and genomics as treasure troves for research towards biology, biotechnology and agriculture
    Miriam Schalamun, Monika Schmoll
    Frontiers in Fungal Biology.2022;[Epub]     CrossRef
  • A Transfectable Fusagravirus from a Japanese Strain of Cryphonectria carpinicola with Spherical Particles
    Subha Das, Sakae Hisano, Ana Eusebio-Cope, Hideki Kondo, Nobuhiro Suzuki
    Viruses.2022; 14(8): 1722.     CrossRef
  • Molecular characteristics of a novel hypovirus from Trichoderma harzianum
    Jeesun Chun, Kum-Kang So, Yo-Han Ko, Dae-Hyuk Kim
    Archives of Virology.2022; 167(1): 233.     CrossRef
  • Sustainable Management of Medicago sativa for Future Climates: Insect Pests, Endophytes and Multitrophic Interactions in a Complex Environment
    Mark R. McNeill, Xiongbing Tu, Eric Altermann, Wu Beilei, Shengjing Shi
    Frontiers in Agronomy.2022;[Epub]     CrossRef
  • A New Double-Stranded RNA Mycovirus in Cryphonectria naterciae Is Able to Cross the Species Barrier and Is Deleterious to a New Host
    Carolina Cornejo, Sakae Hisano, Helena Bragança, Nobuhiro Suzuki, Daniel Rigling
    Journal of Fungi.2021; 7(10): 861.     CrossRef

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