Metabolic modulation of redox state confounds fish survival against <i>Vibrio alginolyticus</i> infection

Gong, Qiyang; Yang, Meisongzhu; Yang, Lei; Chen, Zhuang‐Gui; Jiang, Ming; Peng, Bo

doi:10.1111/1751-7915.13553

Cited by 42 publications

(34 citation statements)

References 54 publications

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“…Recent reports have indicated that bacterial sensitivity to antibiotics and host ability against bacteria are bacterial metabolic state‐ and host metabolic state‐dependent respectively (Zeng et al ., 2017; Cheng et al ., 2018; Yang et al ., 2018; Cheng et al ., 2019; Xu et al ., 2019; Jiang et al ., 2019b; Gong et al ., 2020). The present study explored the relationship between gentamicin resistance and ROS in V .…”

Section: Discussionmentioning

confidence: 99%

Reduced ROS‐mediated antibiotic resistance and its reverting by glucose in Vibrio alginolyticus

Zhang

Yang

Peng

et al. 2020

Environmental Microbiology

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Antibiotic-resistant Vibrio alginolyticus poses a big challenge to human health and food safety. It is urgently needed to understand the mechanisms underlying antibiotic resistance to develop effective approaches for the control. Here we explored the metabolic difference between gentamicin-resistant V. alginolyticus (VA-R GEN) and gentamicin-sensitive V. alginolyticus (VA-S), and found that the reactive oxygen species (ROS) generation was altered. Compared with VA-S, the ROS content in VA-R GEN was reduced due to the decreased generation and increased breakdown of ROS. The decreased production of ROS was attributed to the decreased central carbon metabolism, which is associated with the resistance to gentamicin. As such a mechanism, we exogenously administrated VA-R GEN with the glucose that activated the central carbon metabolism and promoted the generation of ROS, but decreased the breakdown of ROS in VA-R GEN. The gentamicin-mediated killing was increased with the elevation of the ROS level by a synergistic effect between gentamicin and exogenous glucose. The synergistic effect was inhibited by thiourea, a scavenger of ROS. These results reveal a reduced ROS-mediated antibiotic resistance mechanism and its reversal by exogenous glucose.

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Section: Discussionmentioning

confidence: 99%

Reduced ROS‐mediated antibiotic resistance and its reverting by glucose in Vibrio alginolyticus

Zhang

Yang

Peng

et al. 2020

Environmental Microbiology

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“…By comparing the metabolomes of dying fish and survival fish, we and other groups have shown that supplementation of zebrafish or tilapia with glucose, stearic acid, proline, serine, L-aspartic acid, or L-leucine could regulate the expression of immune-related genes and eventually increase fish's survival upon the infection by Vibrio alginolyticus, Streptococcus iniae, Streptococcus agalactiae, or Edwardsiella tarda (Peng et al, 2015b;Du et al, 2017;Cheng et al, 2019). It was also revealed that tryptophan increased zebrafish survival to V. alginolyticus infection by downregulating the production of ROS to avoid excessive immune response (Gong Q. Y. et al, 2020). In addition, metabolism-based approach also found that maltose, palmitic acid, threonine, and taurine enhanced zebrafish survival to Aeromonas sorbrial or E. tarda infection at higher temperature (Jiang et al, 2019a).…”

Section: Introductionmentioning

confidence: 93%

Succinate Promotes Phagocytosis of Monocytes/Macrophages in Teleost Fish

Yang

Cao

et al. 2021

Front. Mol. Biosci.

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Development of immunity-based strategy to manage bacterial infection is urgently needed in aquaculture due to the widespread of antibiotic-resistant bacteria. Phagocytosis serves as the first line defense in innate immunity that engulfs bacteria and restricts their proliferations and invasions. However, the mechanism underlying the regulation of phagocytosis is not fully elucidated and the way to boost phagocytosis is not yet explored. In this manuscript, we profiled the metabolomes of monocytes/macrophages isolated from Nile tilapia, prior and after phagocytosis on Vibrio alginolyticus. Monocytes/macrophages showed a metabolic shift following phagocytosis. Interestingly, succinate was accumulated after phagocytosis and was identified as a crucial biomarker to distinguish before and after phagocytosis. Exogenous succinate increased the phagocytotic rate of monocytes/macrophages in a dose-dependent manner. This effect was dependent on the TCA cycle as the inhibitor of malonate that targets succinate dehydrogenase abrogated the effect. Meanwhile, exogenous succinate regulated the expression of genes associated with innate immune and phagocytosis. In addition, succinate-potentiated phagocytosis was applicable to both gram-negative and -positive cells, including V. alginolyticus, Edwardsiella tarda, Streptococcus agalactiae, and Streptococcus iniae. Our study shed light on the understanding of how modulation on host’s metabolism regulates immune response, and this can be a potent therapeutic approach to control bacterial infections in aquaculture.

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“…Thus, a synergistic use of antibiotics with ROS generation promoter or/and ROS degradation inhibitor will elevate the antibiotic-mediated killing. In addition, metabolites promoting hosts to eliminate bacterial pathogens have been reported ( Jiang et al, 2019a , b , 2020b ; Gong et al, 2020a , b ; Yang et al, 2020 ), where ROS are involved ( Sarr et al, 2018 ; Gong et al, 2020b ). Thus, it is possible to select the promoters or/and inhibitors that simultaneously elevate the ROS level of both hosts and bacteria.…”

Section: Discussionmentioning

confidence: 99%

Reactive Oxygen Species-Related Ceftazidime Resistance Is Caused by the Pyruvate Cycle Perturbation and Reverted by Fe3 + in Edwardsiella tarda

Peng

et al. 2021

Front. Microbiol.

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Reactive oxygen species (ROS) are related to antibiotic resistance and have been reported in bacteria. However, whether ROS contribute to ceftazidime resistance and plays a role in ceftazidime-mediated killing is unknown. The present study showed lower ROS production in ceftazidime-resistant Edwardsiella tarda (LTB4-RCAZ) than that in LTB4-sensitive E. tarda (LTB4-S), two isogenic E. tarda LTB4 strains, which was related to bacterial viability in the presence of ceftazidime. Consistently, ROS promoter Fe3+ and inhibitor thiourea elevated and reduced the ceftazidime-mediated killing, respectively. Further investigation indicated that the reduction of ROS is related to inactivation of the pyruvate cycle, which provides sources for ROS biosynthesis, but not superoxide dismutase (SOD) and catalase (CAT), which degrade ROS. Interestingly, Fe3+ promoted the P cycle, increased ROS biosynthesis, and thereby promoted ceftazidime-mediated killing. The Fe3+-induced potentiation is generalizable to cephalosporins and clinically isolated multidrug-resistant pathogens. These results show that ROS play a role in bacterial resistance and sensitivity to ceftazidime. More importantly, the present study reveals a previously unknown mechanism that Fe3+ elevates ROS production via promoting the P cycle.

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Metabolic modulation of redox state confounds fish survival against Vibrio alginolyticus infection

Cited by 42 publications

References 54 publications

Reduced ROS‐mediated antibiotic resistance and its reverting by glucose in Vibrio alginolyticus

Reduced ROS‐mediated antibiotic resistance and its reverting by glucose in Vibrio alginolyticus

Succinate Promotes Phagocytosis of Monocytes/Macrophages in Teleost Fish

Reactive Oxygen Species-Related Ceftazidime Resistance Is Caused by the Pyruvate Cycle Perturbation and Reverted by Fe3 + in Edwardsiella tarda

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