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Antibacterial effect of Blumea balsamifera DC. essential oil against Haemophilus parasuis

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Abstract

Haemophilus parasuis (H. parasuis), the cause of the Glasser’s disease, is a potentially pathogenic gram-negative organism that colonizes the upper respiratory tract of pigs. The extraction of Blumea balsamifera DC., as a traditional Chinese herb, has shown great bacteriostatic effect against several common bacteria. To study the antibacterial effect on H. parasuis in vitro, this study evaluated the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of Blumea balsamifera DC. essential oil (BBO) as well as morphological changes in H. parasuis treated with it. Furthermore, changes in expression of total protein and key virulence factors were also assessed. Results showed that the MIC and MBC were 0.625 and 1.25 μg/mL, respectively. As the concentration of BBO increased, the growth curve inhibition became stronger. H. parasuis cells were damaged severely after treatment with BBO for 4 h, demonstrating plasmolysis and enlarged vacuoles, along with broken cell walls and membranes. Total protein and virulence factor expression in H. parasuis was significantly downregulated by BBO. Taken together, these results indicated a substantial antibacterial effect of BBO on H. parasuis.

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Abbreviations

H. parasuis :

Haemophilus parasuis

BBO:

Blumea balsamifera DC. essential oil

S. aureus :

Staphylococcus aureus

E. coli :

Escherichia coli

B. cereus :

Bacillus cereus

MIC:

Minimum inhibitory concentration

MBC:

Minimum bactericidal concentration

TSB:

Tryptic Soy Broth

TSA:

Tryptic Soy Agar

OsO4:

Osmium tetroxide

CBB:

Coomassie Brilliant Blue

SDS-PAGE:

SDS polyacrylamide gel electrophoresis

VtaA:

Virulence-associated trimeric autotransporters

OmpP:

Outer-membrane protein

nanH:

Neuraminidase

ppiB:

Peptidylprolyl isomerase B

TEM:

Transmission electron microscope

AT-2:

Trimeric autotransporters

References

  • Bin Z, Cheng T, Falong Y et al (2009) Molecular cloning, sequencing and expression of the outer membrane protein A gene from Haemophilus parasuis. Vet Microbiol 136(3–4):408–410

    Google Scholar 

  • Bin Z, Chenggang X, Suming Z et al (2012) Comparative proteomic analysis of a Haemophilus parasuis SC096 mutant deficient in the outer membrane protein P5. Microb Pathog 52(2):117–124

    Google Scholar 

  • Bregón-Villahoz M, Cb Gutiérrez-Martín, Álvarez-Estrada Á et al (2017) Molecular study of an outer fragment of Haemophilus parasuis neuraminidase and utility with diagnostic and immunogen purposes. Res Vet Sci 115:463

    PubMed  Google Scholar 

  • Chun Y, Rui-Zhi L, Lei X et al (2019) Effects of Baicalin on piglet monocytes involving PKC-MAPK signaling pathways induced by Haemophilus parasuis. BMC Vet Res 15(1):98

    Google Scholar 

  • Dahham S, Tabana Y, Iqbal M et al (2015) The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna. Molecules 20(7):11808–11829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dayao D, Js Gibson, Pj Blackall et al (2016) Antimicrobial resistance genes in Actinobacillus pleuropneumoniae, Haemophilus parasuis and Pasteurella multocida isolated from Australian pigs. Aust Vet J 94(7):227–231

    CAS  PubMed  Google Scholar 

  • El Garch F, de Jong A, Simjee S et al (2016) Monitoring of antimicrobial susceptibility of respiratory tract pathogens isolated from diseased cattle and pigs across Europe, 2009–2012: VetPath results. Vet Microbiol 194:11–22

    PubMed  Google Scholar 

  • Genevieve L, Katy V, Philippe B et al (2019) Antibacterial activity against porcine respiratory bacterial pathogens and in vitro biocompatibility of essential oils. Arch Microbiol 201:833–840

    Google Scholar 

  • Guofeng L, Hongjuan Z, Jie H (2017) Antifungal graphene oxide-borneol composite. Colloids Surf B Biointerfaces 160:220–227

    Google Scholar 

  • Huang J, Qian C, Xu H et al (2018) Antibacterial activity of Artemisia asiatica essential oil against some common respiratory infection causing bacterial strains and its mechanism of action in Haemophilus influenzae. Microb Pathog 114:470–475

    CAS  PubMed  Google Scholar 

  • Hui-Sheng L, Qiao X, Qiao-Ying Z et al (2016) Haemophilus parasuis vaccines. Vet Immunol Immunopathol 180:53–58

    Google Scholar 

  • Ji-Feng Y, Wen-Gui W, Yong W et al (2015) Study on biological characteristics and drug sensitivity of Haemophilus parasuis isolated in Sichuan Province. China Anim Husb Vet Med 6:1566–1570

    Google Scholar 

  • Li L (2017) Study on the antibacterial mechanism of emodin in vitro against Haemophilus parasuis using iTRAQ-based proteomic analysis. Dissertation, Sichuan Agricultural University

  • Li L, Xu S, Zhongqiong Y et al (2016) The antibacterial activity and action mechanism of emodin from Polygonum cuspidatum against Haemophilus parasuis in vitro. Microbiol Res 186:139–145

    PubMed  Google Scholar 

  • Li L, Tian Y, Yu J (2017) iTRAQ-based quantitative proteomic analysis reveals multiple effects of Emodin to Haemophilus parasuis. J Proteomics 166:39–47

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Macedo N, Rovira A, Torremorell M (2015) Haemophilus parasuis: infection, immunity and enrofloxacin. Vet Res 46(1):128

    PubMed  PubMed Central  Google Scholar 

  • Mar Ch, Maria B, Gm Nuria et al (2012) VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages. Vet Res 43(1):57

    Google Scholar 

  • Martinez-Martinez S, Frandoloso R, Ef Ferri et al (2013) Immunoproteomic analysis of the protective response obtained with subunit and commercial vaccines against Glasser’s disease in pigs. Vet Immunol Immunopathol 151(3–4):235–247

    CAS  PubMed  Google Scholar 

  • Mccaig Wd, Cl Loving, Hr Hughes et al (2016) Characterization and vaccine potential of outer membrane vesicles produced by Haemophilus parasuis. PLoS ONE 11(3):e149132

    Google Scholar 

  • Moghimi R, Ghaderi L, Rafati H et al (2016) Superior antibacterial activity of nanoemulsion of Thymus daenensis essential oil against E. coli. Food Chem 194:410–415

    CAS  PubMed  Google Scholar 

  • Oliveira S, Pj Blackall, Pijoan C (2003) Characterization of the diversity of Haemophilus parasuis field isolates by use of serotyping and genotyping. Am J Vet Res 64(4):435–442

    PubMed  Google Scholar 

  • Olvera A, Pina S, Macedo N et al (2012) Identification of potentially virulent strains of Haemophilus parasuis using a multiplex PCR for virulence-associated autotransporters (vtaA). Br Vet J 191(2):213–218

    CAS  Google Scholar 

  • Pina S, Olvera A, Barcelo A et al (2009) Trimeric autotransporters of Haemophilus parasuis: generation of an extensive passenger domain repertoire specific for pathogenic strains. J Bacteriol 191(2):576–587

    CAS  PubMed  Google Scholar 

  • Ping DU, Xian-Jun Z, Xiao-Dong S (2009) Chemical constituents of volatile oil from Blumea balsamifera (Linn.) DC. in Yunnan. Chem Ind For Prod 2:115–118

    Google Scholar 

  • Qing W, Yuxin P, Xuan H et al (2015) Study on antibacterial activity of extracts from residues of Blumea balsamifera (L.) DC. in vitro. J Guangdong Pharm Univ 6(31):713–716

  • Sakee U, Maneerat S, Cushnie TPT et al (2011) Antimicrobial activity of Blumea balsamifera, (Lin.) DC. extracts and essential oil. Nat Prod Res 25(19):1849–1856

    CAS  PubMed  Google Scholar 

  • Suming Z, Xianhui H, Chenggang X et al (2014) The outer membrane protein P2 (OmpP2) of Haemophilus parasuis induces proinflammatory cytokine mRNA expression in porcine alveolar macrophages. Br Vet J 199(3):461–464

    Google Scholar 

  • Veronica M, Pedro S, Javier M et al (2012) Distribution of genes involved in sialic acid utilization in strains of Haemophilus parasuis. Microbiology 158(8):2117–2124

    Google Scholar 

  • Wang Q, Li J, Zhao Y (2018) Epidemiology of Haemophilus parasuis isolates from pigs in China using serotyping, antimicrobial susceptibility, biofilm formation and ERIC-PCR genotyping. PeerJ 6(5):e5040

    PubMed  PubMed Central  Google Scholar 

  • Wu K, Lin Y, Chai X et al (2019) Mechanisms of vapor-phase antibacterial action of essential oil from Cinnamomum camphora var. linaloofera Fujita against Escherichia coli. Food Sci Nutr 7(8):2546–2555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yong-Da Z, Li-Li G, Jie L et al (2018) Characterization of antimicrobial resistance genes in Haemophilus parasuis isolated from pigs in China. PeerJ 6(1):e4613

    Google Scholar 

  • Yuan Y, Mei H, Yu-Xin P et al (2016) Variations in essential oil yield, composition, and antioxidant activity of different plant organs from Blumea balsamifera (L.) DC. at different growth times. Molecules 8(21):1024

    Google Scholar 

  • Yuan-Hui W, Hong-Yun T, Si-Jia HE et al (2012) Analysis of volatile components from Blumea balsamifera (L.) DC. leaf with different extraction methods by gas chromatography-mass spectrometry. Sci Technol Food Ind 12(33):96–97

    Google Scholar 

  • Yu-Xin P, Dan W, Zuo-Wang F et al (2014) Blumea balsamifera—a phytochemical and pharmacological review. Molecules 19(7):9453–9477

    Google Scholar 

  • Ze-Hua L, Ming C, Yuan-Shuai L et al (2019) Antibacterial activity and mechanisms of essential oil from Citrus medica L. var. sarcodactylis. Molecules 24(8):1577

    Google Scholar 

  • Zhi-Long J, Yan Z, Wei-Chen G et al (2014) Phytochemical compositions of volatile oil from Blumea balsamifera and their biological activities. Pharmacogn Mag 10(39):346–352

    Google Scholar 

  • Zuo-Wang F, Yu-Xin P, Kai W et al (2015) Blumea balsamifera oil for the acceleration of healing of burn injuries. Molecules 20(9):17166–17179

    Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (no. 31872510). We thank Gillian Campbell, PhD, from Liwen Bianji, Edanz Group China (http://www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Funding

This work was supported by National Natural Science Foundation of China under Grant (no. 31872510).

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Author notes

  1. Changliang He and Peiyi Yang contributed equally to this work.

Authors and Affiliations

  1. Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural University, Huimin Road No. 211, Wenjiang District, Chengdu, Sichuan, People’s Republic of China

    Changliang He, Peiyi Yang, Xiaolin Jiang, Wei Zhang, Xiaoxia Liang, Lizi Yin, Zhongqiong Yin, Xu Song, Yuanfeng Zou, Lixia Li & Cheng Lv

  2. Natural Medicine Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, People’s Republic of China

    Changliang He, Peiyi Yang, Xiaolin Jiang, Wei Zhang, Xiaoxia Liang, Lizi Yin, Zhongqiong Yin, Xu Song, Yuanfeng Zou, Lixia Li & Cheng Lv

  3. Engineering Research Center of the Utilization for Characteristic Bio-Pharmaceutical Resources in Southwest, Ministry of Education, Guizhou University, Guiyang, 550025, Guizhou, People’s Republic of China

    Lu Wang

  4. Department of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, People’s Republic of China

    Yi Geng

  5. Sichuan Province Key Laboratory of Animal Disease and Human Health, Key Laboratory of Environmental Hazard and Human Health of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, People’s Republic of China

    Zhijun Zhong

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  1. Changliang He
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Correspondence to Changliang He.

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Communicated by Erko Stackebrandt.

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He, C., Yang, P., Wang, L. et al. Antibacterial effect of Blumea balsamifera DC. essential oil against Haemophilus parasuis. Arch Microbiol 202, 2499–2508 (2020). https://doi.org/10.1007/s00203-020-01946-4

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