Involvement of the flagellar assembly pathway in Vibrio alginolyticus adhesion under environmental stresses

Wang, Lu; Huang, Lixing; Su, Yongquan; Qin, Yingxue; Kong, Wendi; Ma, Ying; Xu, Xiaojin; Lin, Mao; Zheng, Jiang; Yan, Qingpi

doi:10.3389/fcimb.2015.00059

Cited by 41 publications

(45 citation statements)

References 31 publications

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“…In the 13 C NMR spectrum, signals of 10 carbonyl groups (␦ 173.36 to 169.98) were detected in compound 1, 9 of which were attributed to amino acids. The resonances at ␦ 50.11 and 51.10 in the 13 C NMR spectrum also demonstrated the methoxy group attached on the Glu and Asp residues, respectively. In addition, a signal at ␦ 72.18 (corresponding to ␦ H 5.02) was characteristic for ␤-hydroxy fatty acids (30).…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, 1 H nuclear magnetic resonance (NMR) and 13 C NMR spectroscopy analyses were performed to clarify the exact structure of these active compounds. In the 1 H NMR spectrum, a long alkyl chain (␦ 1.4-1.1) and a peptide backbone (7 amine protons, ␦ 8.22 to 7.76 and 7 ␣-amino acid protons, ␦ 4.6 to 4.1) were observed in compound 1.…”

Section: Resultsmentioning

confidence: 99%

“…Polar flagella are constitutively expressed, while lateral flagellar expression is induced when polar flagellar function has been disabled (9)(10)(11). Furthermore, the flagellar assembly pathway of V. alginolyticus has been implicated in cell adhesion processes (12,13).…”

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confidence: 99%

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Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

Xiu

Zhang

et al. 2017

Appl Environ Microbiol

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Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (Vibrio alginolyticus strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that V. alginolyticus 178 motility was significantly suppressed by another marine bacterium, Bacillus sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from Bacillus sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of V. alginolyticus 178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of V. alginolyticus 178 to glass substrates. Notably, upon CLP treatment, the expression levels of two V. alginolyticus flagellar assembly genes (flgA and flgP) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from Bacillus sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.IMPORTANCE Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium Bacillus sp. strain 176 dramatically suppress the motility of the pathogenic bacterium Vibrio alginolyticus strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance.KEYWORDS lipopeptide, pumilacidin, Vibrio alginolyticus, motility, antibiotic, antimicrobial, antibiofilm B acterial motility is one of several crucial factors during the initial infection and colonization processes of pathogens. In particular, it helps pathogens overcome the repulsive forces between the bacterial cell wall and the host tissues and facilitates host attachment (1-3). The flagellum is one of the main locomotive organelles respon-

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

Xiu

Zhang

et al. 2017

Appl Environ Microbiol

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“…S5 in the supplemental material). For these biological processes, some representative genes, such as those encoding the small heat shock protein IbpA, heat shock protein 70 (chaperone protein DnaK), DnaK-related protein, the chaperone protein HtpG, the flagellar basal body rod protein FlgF, flagellin core protein A, and polar flagellin B, were involved in the heat stress response and the flagellar assembly process, indicating that these genes might be of benefit for protecting JZ6 from high temperatures and escape from adverse environments (37)(38)(39). These results could partly explain the adaptation of JZ6 to low temperatures and its survival in high-temperature environments.…”

Section: Discussionmentioning

confidence: 99%

Comparative Transcriptome Analysis of Vibrio splendidus JZ6 Reveals the Mechanism of Its Pathogenicity at Low Temperatures

Chen

Zhang

et al. 2016

Appl Environ Microbiol

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dYesso scallop-pathogenic Vibrio splendidus strain JZ6 was found to have the highest virulence at 10°C, while its pathogenicity was significantly reduced with increased temperature and completely incapacitated at 28°C. In the present study, comparative transcriptome analyses of JZ6 and another nonpathogenic V. splendidus strain, TZ19, were conducted at two crucial culture temperatures (10°C and 28°C) in order to determine the possible mechanism of temperature regulation of virulence. Comparisons among four libraries, constructed from JZ6 and TZ19 cultured at 10°C and 28°C (designated JZ6_10, JZ6_28, TZ19_10, and TZ19_28), revealed that 241 genes were possibly related to the increased virulence of JZ6 at 10°C. There were 10 genes, including 2 encoding Flp pilus assembly proteins (FlhG and VS_2437), 6 encoding proteins of the "Vibrio cholerae pathogenic cycle" (ToxS, CqsA, CqsS, RpoS, HapR, and Vsm), and 2 encoding proteins in the Sec-dependent pathway (SecE and FtsY), that were significantly upregulated in JZ6_10 (P < 0.05) compared to those in JZ6_28, TZ19_10, and TZ19_28, which were supposed to be responsible for adhesion, quorum sensing, virulence, and protein secretion of V. splendidus. When cultured at 10°C, JZ6 cells were larger and tended to aggregate more than those cultured at 28°C. The virulence factor (extracellular metalloprotease) was also found to be highly expressed in the extracellular product (ECP) of JZ6 at 10°C, and this ECP exhibited obvious cytotoxicity to oyster primary hemocytes, A549 cells, and L929 cells. These results indicated that low temperatures (10°C) could enhance adhesion, activate the quorum sensing systems, upregulate virulence factor synthesis and secretion, and, lastly, increase the pathogenicity of JZ6.T he Gram-negative pathogenic bacterium Vibrio splendidus is a ubiquitous and representative species of the Vibrio genus, a causal agent of vibriosis, which causes high rates of mortality in aquaculture animals, including turbot, scallop, clam, and oyster (1-5). Like most Vibrio strains, V. splendidus is an opportunistic pathogen that causes mortality of animals in an optimum environment, whereas it usually acts as a "normal bacterium" in the host or environment under adverse conditions (6-8). Therefore, environmental factors are important regulators of the pathogenicity of V. splendidus.In previous studies, most opportunistic pathogenic Vibrio bacteria, such as V. splendidus, V. cholerae, V. parahaemolyticus, V. alginolyticus, and V. harveyi, have been reported to cause high rates of mortality of cultured animals in the summer and enter a viable-but-nonculturable (VBNC) state when they are exposed to temperatures below 10°C (6, 8-11). Hence, temperature has been considered one of the crucial environmental factors that can regulate the metabolic process, growth, adhesion, and even pathogenicity of bacteria by influencing their gene expression (12-14). V. splendidus strain JZ6 was previously isolated and identified as a pathogenic agent for Yesso scallop (Patinopecten yessoensis...

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“…Adhesion to the host external surfaces and tissues by pathogenic bacteria represents the first crucial step in most infections, and it had been regarded as an important virulence factor in colonizing the host surface for proliferation and for the release of virulence factors of many pathogenic bacteria (Grześkowiak, Collado, Vesterlund, Mazurkiewicz, & Salminen, ; Huang et al., ; Wang et al., ).The ability of pathogens to attach to the host mucus, cells, and other tissues is mediated by adhesions that can cause many infectious diseases or other harm (Hori & Matsumoto, ). Therefore, the inhibition of bacterial adhesion to the host could be useful therapeutically (Acord, Maskell, & Sefton, ).…”

Section: Introductionmentioning

confidence: 99%

Ribose operon repressor (RbsR) contributes to the adhesion of Aeromonas hydrophila to Anguilla japonica mucus

Lin

Chen

et al. 2017

MicrobiologyOpen

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The characterization of adhesion between pathogenic bacteria and the host is critical. Pathogenic Aeromonas hydrophila was shown to adhere in vitro to the mucus of Anguilla japonica. To further investigate the adhesion mechanisms of A. hydrophila, a mini‐Tn10 transposon mutagenesis system was used to generate an insertion mutant library by cell conjugation. Seven mutants that were impaired in adhesion to mucus were selected out of 332 individual colonies, and mutant M196 was the most severely impaired strain. National Center for Biotechnology Information (NCBI) blast analysis showed that mutant M196 was inserted by mini‐Tn10 with an ORF of approximately 1,005 bp (GenBank accession numbers KP280172). This ORF is predicted to encode a protein consist of 334 amino acid, which displays the highest identity (98%) with the RbsR of A. hydrophila ATCC 7966. Random inactivation of rbsR gene affected the pleiotropic phenotypes of A. hydrophila. The adhesion ability and the survival level of the rbsR gene mutant (M196) were attenuated compared with the wild‐type and rbsR complementary type. The findings of this study indicated that RbsR plays roles in the bacterial adhesion and intracellular survival of A. hydrophila.

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Involvement of the flagellar assembly pathway in Vibrio alginolyticus adhesion under environmental stresses

Cited by 41 publications

References 31 publications

Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus

Comparative Transcriptome Analysis of Vibrio splendidus JZ6 Reveals the Mechanism of Its Pathogenicity at Low Temperatures

Ribose operon repressor (RbsR) contributes to the adhesion of Aeromonas hydrophila to Anguilla japonica mucus

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