RESVERATROL INHIBITS GROWTH, VIRULENCE AND BIOFILM FORMATION OF <i>AEROMONAS HYDROPHILA</i>

TAN Hong-Liang; CHEN Kai; XI Bing-Wen; QIN Ting; PAN Liang-Kun; XIE Jun

doi:10.7541/2019.102

Volume 43 Issue 4

Jul. 2019

Turn off MathJax

Article Contents

Abstract

References

ACTA HYDROBIOLOGICA SINICA > 2019 > 43(4): 861-868. > DOI: 10.7541/2019.102

TAN Hong-Liang, CHEN Kai, XI Bing-Wen, QIN Ting, PAN Liang-Kun, XIE Jun. RESVERATROL INHIBITS GROWTH, VIRULENCE AND BIOFILM FORMATION OF AEROMONAS HYDROPHILA[J]. ACTA HYDROBIOLOGICA SINICA, 2019, 43(4): 861-868. DOI: 10.7541/2019.102

Citation:

PDF (777 KB)

RESVERATROL INHIBITS GROWTH, VIRULENCE AND BIOFILM FORMATION OF AEROMONAS HYDROPHILA

1.
Wuxi Fisheries College, Nanjing Agricultural University, Wuxi 214081, China
2.
Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Science, Wuxi 214081, China

Funds: Supported by the Natural Science Foundation of China (31572662); Jiangsu Natural Science Foundation (BK20171152); Earmarked Fund for China Agriculture Research System (CARS-45-18)

Received Date: July 01, 2018
Rev Recd Date: January 03, 2019
Available Online: June 18, 2019
Published Date: June 30, 2019

Graphical Abstract

Abstract

Abstract

Resveratrol (Res) is an important active ingredient in Chinese herbal medicines such as rhubarb and polygonum cuspidatum with antibacterial, anti-inflammatory and antioxidant properties. To explore its application value in the prevention and treatment of bacterial diseases in aquatic animals, we explored the antibacterial activity of resveratrol against Aeromonas hydrophila, an important bacterial pathogen in freshwater aquaculture. The growth, biofilm formation, hemolysis inhibition, and virulence related gene expression of A. hydrophila under different resveratrol concentrations were detected. The in-vivo protection of resveratrol was confirmed by artificially infecting crucian carp with A. hydrophila. The results showed that the minimal inhibitory concentration (MIC) of resveratrol against A. hydrophila was above 1024 μg/mL, and the concentration less than 64 μg/mL did not affect the growth ratio of A. hydrophila. Resveratrol with more than 32 μg/mL significantly inhibited the biofilm formation and hemolytic activity of A. hydrophila (P<0.05) in a dose-dependent pattern. Resveratrol mediated heavy moisture of bacterium group sense of regulation and of QS system by inducing luxR and reucing luxS gene expression. The expression of omp was significantly down-regulated by resveratrol. Artificial infections showed that the mortality rate of allogynogenetic crucian carp infection in the 25—100 mg/kg resveratrol-treated group was significantly lower than that of the control group, and the expression of TNF-α and IFN-γ mRNA was significantly decreased. This study showed that resveratrol can effectively inhibit the viru-lence of A. hydrophila and reduce the inflammatory response at 2500 mg/kg on fish infected with A. hydrophila.
- Medical plant,
- Resveratrol,
- Aeromonas hydrophila,
- Virulence

FullText(HTML)

References (44)

References

[1]	Janda J M, Abbott S L. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions [J]. Clini-cal Infectious Diseases, 1998, 27(2): 332—344 doi: 10.1086/cid.1998.27.issue-2
[2]	梁利国, 谢骏. 青鱼病原嗜水气单胞菌分离鉴定、毒力因子检测及药敏试验. 生态学杂志, 2013, 32(12): 3236—3242 Liang L G, Xie J. Isolation and identification, virulence factor detection, and susceptibility test of pathogen Aeromonas hydrophila isolated from Mylopharyngodon piceus [J]. Chinese Journal of Ecology, 2013, 32(12): 3236—3242
[3]	邱军强, 杨先乐, 程训佳. 嗜水气单胞菌毒力因子特性及作用机理研究进展. 中国病原生物学杂志, 2009, 4(8): 616—619 Qiu J Q, Yang X L, Cheng X J. Advances in the characteristics and pathogenic mechanisms of virulence factors in Aeromonas hydrophila [J]. Journal of Pathogen Biology, 2009, 4(8): 616—619
[4]	Chakraborty T, Schmid A, Notermans S, et al. Aerolysin of Aeromonas sobria: evidence for formation of ionpermeable channels and comparison with alpha-oxin of Staphylococcus aureus [J]. Infection & Immunity, 1990, 58(7): 2127—2132
[5]	朱大玲, 李爱华, 汪建国, 等. 嗜水气单胞菌毒力与毒力基因分布的相关性. 中山大学学报, 2006, 45(1): 82—85 doi: 10.3321/j.issn:0529-6579.2006.01.021 Zhu D L, Li A H, Wang J G, et al. The correlation between the distribution pattern of virulence genes and virulence of Aeromonas hydrophila strains [J]. Acta Scientiarum Naturalium Universitatis Sunyatseni, 2006, 45(1): 82—85 doi: 10.3321/j.issn:0529-6579.2006.01.021
[6]	Rasmussen-Ivey C R, Figueras M J, McGarey D, et al. Virulence factors of Aeromonas hydrophila: in the wake of reclassification [J]. Frontiers in Microbiology, 2016, 7: 1337
[7]	张旭杰, 杨五名, 李彤彤, 等. 湖北地区暴发病池塘中嗜水气单胞菌的遗传多样性和毒力特征研究. 水生生物学报, 2013, 37(3): 458—466 Zhang X J, Yang W M, Li T T, et al. The genetic diversity and virulence characteristics of Aeromonas hydrophila isolated from fishponds with disease outbreaks in Hubei province [J]. Acta Hydrobiologica Sinica, 2013, 37(3): 458—466
[8]	Williams P. Quorum sensing, communication and cross-kingdom signaling in the bacterial world [J]. Microbiology, 2007, 153(12): 3923—3938 doi: 10.1099/mic.0.2007/012856-0
[9]	Bassler B L, Losick R. Bacterially speaking [J]. Cell, 2006, 125(2): 237—246 doi: 10.1016/j.cell.2006.04.001
[10]	Frémont L. Biological effects of resveratrol [J]. Life Sciences, 2000, 66(8): 663—673 doi: 10.1016/S0024-3205(99)00410-5
[11]	闫亚楠, 夏斯蕾, 田红艳, 等. 白藜芦醇对高脂胁迫团头鲂抗氧化能力、非特异免疫机能和抗病力的影响. 水生生物学报, 2017, 41(1): 155—164 Yan Y N, Xia S L, Tian H Y, et al. Effects of resveratrol supplementation on growth performance, immunity, antioxidant capability and disease resistance of blunt snout bream fed high-fat diet [J]. Acta Hydrobiologica Sinica, 2017, 41(1): 155—164
[12]	Waffoteguo P, Lee D, Cuendet M, et al. Two new stilbene dimer glucosides from grape (Vitis vinifera) cell cultures [J]. Journal of Natural Products, 2001, 64(1): 136—138 doi: 10.1021/np000426r
[13]	Wang W B, Lai H C, Hsueh P R, et al. Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol [J]. Journal of Medical Microbiology, 2006, 55(10): 1313—1321 doi: 10.1099/jmm.0.46661-0
[14]	Zhou J W, Chen T T, Tan X J, et al. Can resveratrol, a quorum sensing inhibitor, function as an aminoglycoside antibiotic-accelerant against Pseudomonas aeruginosa [J]? International Journal of Antimicrobial Agents, 2018, 52(1): 35—41 doi: 10.1016/j.ijantimicag.2018.03.002
[15]	Augustine N, Goel A K, Sivakumar K C, et al. Resveratrol - A potential inhibitor of biofilm formation in Vibrio cholera [J]. Phytomedicine, 2014, 21(3): 286—289 doi: 10.1016/j.phymed.2013.09.010
[16]	高路, 袁育康, 吕卓人, 等. 白藜芦醇的免疫调节作用. 西安交通大学学报(医学版), 2003, 24(2): 121—123 doi: 10.3969/j.issn.1671-8259.2003.02.008 Gao L, Yuan Y K, Lü Z R, et al. The immunomodulatory function of resveratrol [J]. Journal of Xi’an Jiaotong University ( Medical Sciences ) , 2003, 24(2): 121—123 doi: 10.3969/j.issn.1671-8259.2003.02.008
[17]	卢静, 王振宁, 陈锐, 等. 几种中药单体和抗生素对嗜水气单胞菌及温和气单胞菌的体外抑菌活性研究. 水生生物学报, 2013, 37(6): 1128—1132 Lu J, Wang Z N, Chen R, et al. In vitro antibacterial activity of several Chinese medicine monomers and antibiotics on Aeromonsa hydrophila and Aeromonas sobria [J]. Acta Hydrobiologica Sinica, 2013, 37(6): 1128—1132
[18]	Vasudevan P, Nair M K, Annamalai T, et al. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation [J]. Veterinary Microbiology, 2003, 92(1-2): 179—185 doi: 10.1016/S0378-1135(02)00360-7
[19]	Mao Y, Niu S, Xu X, et al. The effect of an adding histi-dine on biological activity and stability of pc-pis from Pseudosciaena crocea [J]. PLoS One, 2013, 8(12): e83268 doi: 10.1371/journal.pone.0083268
[20]	Bostanghadiri N, Pormohammad A, Chirani A S, et al. Comprehensive review on the antimicrobial potency of the plant polyphenol resveratrol [J]. Biomedicine & Pharmacotherapy, 2017, 95: 1588—1595
[21]	He Z, Huang Z, Zhou W, et al. Anti-biofilm activities from resveratrol against fusobacterium nucleatum [J]. Frontiers in Microbiology, 2016, 7: 1065
[22]	Jung C M, Heinze T M, Schnackenberg L K, et al. Inte-raction of dietary resveratrol with nimal-associated bacteria [J]. FEMS Microbiology Letters, 2009, 297: 266—273 doi: 10.1111/fml.2009.297.issue-2
[23]	赵晶, 张福蓉, 崔一, 等. 嗜水气单胞菌群体感应信号分子AI-2的细胞外生物合成及活性检测. 微生物学通报, 2015, 42(10): 1858—1865 Zhao J, Zhang F R, Chui Y, et al. In vitro biosynthesis and activity detection of quorum sensing signal molecule AI-2 of Aeromonas hydrophila [J]. Microbiology China, 2015, 42(10): 1858—1865
[24]	Han X, Bai H, Liu L, et al. The luxS gene functions in the pathogenesis of avian pathogenic Escherichia coli [J]. Microbial Pathogenesis, 2013, 55(2): 21—27
[25]	王娜. 嗜水气单胞菌浮游态和生物被膜状态比较蛋白质组学及相关蛋白特性分析. 博士学位论文, 南京农业大学, 南京. 2012 Wang N. Comparative proteomic analysis between biofilm and planktonic cells of Aeromonas hydrophila and characteristics of related oriteins [D]. Thesis for Doctor of science. Nanjing Agricultural University, Nanjing. 2012
[26]	Kovacikova G, Lin W, Skorupski K. The LysR-type viru-lence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobio-sis [J]. Journal of Bacteriology, 2010, 192(16): 4181—4191 doi: 10.1128/JB.00193-10
[27]	崔一, 赵晶, 张福蓉, 等. 嗜水气单胞菌ATCC7966 luxS基因缺失株构建及特性研究. 中国人兽共患病学报, 2016, 32(5): 462—468 doi: 10.3969/j.issn.1002-2694.2016.05.009 Chui Y, Zhao J, Zhang F R, et al. Construction of luxS gene deletion mutant strain in Aeromonas hydrophila ATCC7966 [J]. Chinese Journal of Zoonoses, 2016, 32(5): 462—468 doi: 10.3969/j.issn.1002-2694.2016.05.009
[28]	Smith D, Wang J H, Swatton J E, et al. Variations on a theme: diverse N-acyl homoserine lactone-mediated quo-rum sensing mechanisms in gram-negative bacteria [J]. Science Progress, 2006, 89(3-4): 167—211 doi: 10.3184/003685006783238335
[29]	Swift S, Karlyshev AV, Durant EL, et al. Quorum sensing in Aeromonas hydrophila and Aeromonas salmoni-cida: identification of the LuxRI homologues AhyRI and AsaRI and their congnate signal molecules [J]. Journal of Bacteriology, 1997, 179(17): 5272—5281
[30]	张小军. 嗜水气单胞菌J-1株luxS基因缺失株的构建及特性分析. 硕士学位论文, 南京农业大学, 南京. 2009 Zhang X J. Construction and characterization of LuxS deleted mutant strain in Aeromonas hydrophila J-1 [D]. Nanjing Agricultural University, Nanjing. 2009
[31]	Howard S P, Garland W J, Green M J, et al. Nucleotide sequence of the gene for the hole-forming toxin aerolysin of Aeromonas hydrophila [J]. Journal of Bacteriology, 1987, 169(6): 2869—2871 doi: 10.1128/jb.169.6.2869-2871.1987
[32]	Wong C Y, Heuzenroeder M W, Flower R L. Inactivation of two haemolytic toxin genes in Aeromonas hydrophila attenuates virulence in a suckling mouse model [J]. Microbiology, 1998, 144(2): 291—298 doi: 10.1099/00221287-144-2-291
[33]	Hazes B, Boodhoo A, Cockle S A, et al. Crystal structure of the pertussis toxin-ATP complex: a molecular sensor [J]. Journal of Molecular Biology, 1996, 258(4): 661—671 doi: 10.1006/jmbi.1996.0277
[34]	Miles G, Jayasinghe L, Bayley H. Assembly of the Bi-component leukocidin pore examined by truncation mutagenesis [J]. Journal of Biological Chemistry, 2006, 281(4): 2205—2214 doi: 10.1074/jbc.M510842200
[35]	邓国成, 江小燕, 叶星, 等. 草鱼出血病混合感染的嗜水气单胞菌的分离、鉴定与理化特性. 微生物学通报, 2009, 36(8): 1170—1177 Deng G C, Jiang X Y, Ye X, et al. Isolation, identification and characterization of Aeromonas hydrophila from hemorrhagic grass carp [J]. Microbiology China, 2009, 36(8): 1170—1177
[36]	Song T, Toma C, Nakasone N, et al. Aerolysin is activa-ted by metalloprotease in Aeromonas veronii biovar sobria [J]. Journal of Medical Microbiologxy, 2004, 53(6): 477—482 doi: 10.1099/jmm.0.05405-0
[37]	Gryllos I, Shaw J G, Gavín R, et al. Role of flm locus in mesophilic Aeromonas species adherence [J]. Infection & Immunity, 2001, 69(1): 65—74
[38]	Rahman M H, Kawai K. Outer membrane proteins of Aeromonas hydrophila induce protective immunity in goldfish [J]. Fish & Shellfish Immunology, 2000, 10(4): 379—382
[39]	刘俊瑶. 白藜芦醇腹腔注射后在大鼠体内的组织分布及其溶剂相关性. 大连医科大学. 2016 Liu J Y. Solvent-related biodistribution of intraperitoneal administered Resveratrol in rats [D]. Dalian Medical University. 2016
[40]	Yu S, Ao J, Chen X. Molecular characterization and expression analysis of MHC class II α and β genes in large yellow croaker (Pseudosciaena crocea) [J]. Molecular Biology Reports, 2010, 37(3): 1295 doi: 10.1007/s11033-009-9504-8
[41]	Wang H, Shen X, Xu D, et al. Lipopolysaccharide-induced TNF-α factor in grass carp (Ctenopharyngodon idella): evidence for its involvement in antiviral innate immunity [J]. Fish & Shellfish Immunology, 2013, 34(2): 538—545
[42]	杨智景, 李长红, 张浩, 等. 香鱼(Plecoglossus altivelis)肿瘤坏死因子-α (TNF-α)基因的分子克隆、鉴定及免疫相关性表达. 海洋与湖沼, 2015, 46(6): 1380—1389 Yang Z J, Li C H, Zhang H, et al. Molecular coloning, characterisation and immune-related expression of tumor necrosis factor α (TNF-α) gene in Plecoglossus altivelis [J]. Oceanologia et Limnologia Sinica, 2015, 46(6): 1380—1389
[43]	Zhang X, Wang Y, Xiao C, et al. Resveratrol inhibits LPS-induced mice mastitis through attenuating the MAPK and NF-κB signaling pathway [J]. Microbial Pathogenesis, 2017, 107: 462—467 doi: 10.1016/j.micpath.2017.04.002
[44]	Zheng Y, Zhao Z, Wu W, et al. Effects of dietary resveratrol supplementation on hepatic and serum pro-/anti-inflammatory activity in juvenile GIFT tilapia, Oreochromis niloticus [J]. Developmental & Comparative Immunology, 2017, 73: 220—228

Cited By

Get Citation

PDF

XML

Article views (1714) PDF downloads (55)

RESVERATROL INHIBITS GROWTH, VIRULENCE AND BIOFILM FORMATION OF AEROMONAS HYDROPHILA

Abstract

References

Catalog

Related

RESVERATROL INHIBITS GROWTH, VIRULENCE AND BIOFILM FORMATION OF AEROMONAS HYDROPHILA

Abstract

References

Catalog

Related

Export File

Citation

Format

Content