Identification of Aeromonas hydrophila Genes Preferentially Expressed after Phagocytosis by Tetrahymena and Involvement of Methionine Sulfoxide Reductases

Pang, Maoda; Lin, Xiaoqin; Jin, Lan; Guo, Changming; Gao, Shanshan; Du, Hechao; Chen, Lu; Liu, Yongjie

doi:10.3389/fcimb.2016.00199

Cited by 9 publications

(5 citation statements)

References 51 publications

(65 reference statements)

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“…The methionine sulfoxide reductase can repair ROS-damaged proteins and are important for many bacterial pathogens ( Sasindran et al, 2007 ). Mutation of methionine sulfoxide reductases in Aeromonas hydrophila reduces resistance to predation by T. thermophila and infection of zebrafish ( Pang et al, 2016 ). Hemagglutinin protease which destroys host cell receptors for several different V. cholerae adhesins, is also involved in the degradation of chironomid egg masses ( Halpern et al, 2003 ).…”

Section: Coincidental Evolution Hypothesismentioning

confidence: 99%

Dual Role of Mechanisms Involved in Resistance to Predation by Protozoa and Virulence to Humans

2018

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Most opportunistic pathogens transit in the environment between hosts and the environment plays a significant role in the evolution of protective traits. The coincidental evolution hypothesis suggests that virulence factors arose as a response to other selective pressures rather for virulence per se. This idea is strongly supported by the elucidation of bacterial-protozoal interactions. In response to protozoan predation, bacteria have evolved various defensive mechanisms which may also function as virulence factors. In this review, we summarize the dual role of factors involved in both grazing resistance and human pathogenesis, and compare the traits using model intracellular and extracellular pathogens. Intracellular pathogens rely on active invasion, blocking of the phagosome and lysosome fusion and resistance to phagocytic digestion to successfully invade host cells. In contrast, extracellular pathogens utilize toxin secretion and biofilm formation to avoid internalization by phagocytes. The complexity and diversity of bacterial virulence factors whose evolution is driven by protozoan predation, highlights the importance of protozoa in evolution of opportunistic pathogens.

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Section: Coincidental Evolution Hypothesismentioning

confidence: 99%

Dual Role of Mechanisms Involved in Resistance to Predation by Protozoa and Virulence to Humans

2018

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“…The anti-predation ability of A. hydrophila was expressed as the relative survival of bacteria after co-cultured with T. thermophila [15]. Briefly, A. hydrophila (1 × 10 9 CFU/mL) and T. thermophila SB210 (2 × 10 5 cells/mL) in TBSS (2 mM KCl, 1 mM CaCl 2 , 0.5 mM MgCl 2 , and 1 mM Tris [pH 6.8–7.2]) were well mixed in equal volume.…”

Section: Methodsmentioning

confidence: 99%

“…In our previous study, the norV gene of A. hydrophila was screened and identified to be about 15-fold upregulated under predation pressure of Tetrahymena thermophila [15]. The norV encodes a flavorubredoxin, a nitric oxide reductase, which is supposed to be inactivated by oxygen and provides physiological protection against nitric oxide (NO) only at low or zero oxygen concentrations [16].…”

Section: Introductionmentioning

confidence: 99%

Diverse effects of nitric oxide reductase NorV on Aeromonas hydrophila virulence-associated traits under aerobic and anaerobic conditions

Jin

Dong

Wang

et al. 2019

Vet Res

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NorV has been known to be an anaerobic nitric oxide reductase associated with nitric oxide (NO) detoxification. Recently, we showed that the norV gene of Aeromonas hydrophila was highly upregulated after co-culturing with Tetrahymena thermophila. Here, we demonstrated that the transcription and expression levels of norV were upregulated in a dose-dependent manner after exposure to NO under aerobic and anaerobic conditions. To investigate the roles of norV in resisting predatory protists and virulence of A. hydrophila, we constructed the norV gene-deletion mutant (ΔnorV). Compared to the wild type, the ΔnorV mutant showed no significant difference in growth at various NO concentrations under aerobic conditions but significantly stronger NO-mediated growth inhibition under anaerobic conditions. The deletion of norV exhibited markedly decreased cytotoxicity, hemolytic and protease activities under aerobic and anaerobic conditions. Also, the hemolysin co-regulated protein (Hcp) in the ΔnorV mutant showed increased secretion under aerobic conditions but decreased secretion under anaerobic conditions as compared to the wild-type. Moreover, the inactivation of norV led to reduced resistance to predation by T. thermophila, decreased survival within macrophages and highly attenuated virulence in zebrafish. Our data indicate a diverse role for norV in the expression of A. hydrophila virulence-associated traits that is not completely dependent on its function as a nitric oxide reductase. This study provides insights into an unexplored area of NorV, which will contribute to our understanding of bacterial pathogenesis and the development of new control strategies for A. hydrophila infection.

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“…In addition, the pMMB207 empty plasmid was also transformed into A. hydrophila to serve as controls. For the other three genes shown to be upregulated, the gene-deletion mutants were respectively constructed in A. hydrophila via homologous recombination using the suicide plasmid pYAK1 as previously described (Pang et al, 2016 ). Briefly, two flanking regions of the target gene were amplified and ligated by PCR.…”

Section: Methodsmentioning

confidence: 99%

“…Biofilm formation, cellular adhesion ability, antioxidant stress and virulence were evaluated as described above. Bacterial resistance to predation was assessed by measuring the relative survival of bacteria after co-culture with T. thermophila (Pang et al, 2016 ). A. hydrophila (1 × 10 9 CFU/ml) and T. thermophila SB210 (2 × 10 5 cells/ml) were mixed at a volume ratio of 1:1 in TBSS.…”

Section: Methodsmentioning

confidence: 99%

Tetrahymena thermophila Predation Enhances Environmental Adaptation of the Carp Pathogenic Strain Aeromonas hydrophila NJ-35

Jin

Dong

Wang

et al. 2018

Front. Cell. Infect. Microbiol.

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Persistence of Aeromonas hydrophila in aquatic environments is the principle cause of fish hemorrhagic septicemia. Protistan predation has been considered to be a strong driving force for the evolution of bacterial defense strategies. In this study, we investigated the adaptive traits of A. hydrophila NJ-35, a carp pathogenic strain, in response to Tetrahymena thermophila predation. After subculturing with Tetrahymena, over 70% of A. hydrophila colonies were small colony variants (SCVs). The SCVs displayed enhanced biofilm formation, adhesion, fitness, and resistance to bacteriophage infection and oxidative stress as compared to the non-Tetrahymena-exposed strains. In contrast, the SCVs exhibited decreased intracellular bacterial number in RAW264.7 macrophages and were highly attenuated for virulence in zebrafish. Considering the outer membrane proteins (OMPs) are directly involved in bacterial interaction with the external surroundings, we investigated the roles of OMPs in the antipredator fitness behaviors of A. hydrophila. A total of 38 differentially expressed proteins were identified in the SCVs by quantitative proteomics. Among them, three lipoproteins including SurA, Slp, and LpoB, and a serine/threonine protein kinase (Stpk) were evidenced to be associated with environmental adaptation of the SCVs. Also, the three lipoproteins were involved in attenuated virulence of SCVs through the proinflammatory immune response mediated by TLR2. This study provides an important contribution to the understanding of the defensive traits of A. hydrophila against protistan predators.

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Identification of Aeromonas hydrophila Genes Preferentially Expressed after Phagocytosis by Tetrahymena and Involvement of Methionine Sulfoxide Reductases

Cited by 9 publications

References 51 publications

Dual Role of Mechanisms Involved in Resistance to Predation by Protozoa and Virulence to Humans

Dual Role of Mechanisms Involved in Resistance to Predation by Protozoa and Virulence to Humans

Diverse effects of nitric oxide reductase NorV on Aeromonas hydrophila virulence-associated traits under aerobic and anaerobic conditions

Tetrahymena thermophila Predation Enhances Environmental Adaptation of the Carp Pathogenic Strain Aeromonas hydrophila NJ-35

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