Abstract
Temperature is one of the major factors that affect the outbreak of infectious disease. Lines of evidences have shown that virulence factors can be controlled by thermo-sensors in bacterial pathogens. However, how temperature influences host's responses to the pathogen is still largely unexplored, and the study of this might pave the way to develop strategies to manage pathogenic bacterial infection. In the present study, we show that finfish Carassius carassius, the crucian carp that is tolerant to a wide range of temperatures, is less susceptible to bacterial infection when grown in 20°C than in 30°C. The different responses of C. carassius to bacterial infection could be partially explained by the distinct metabolisms under the specific temperatures: C. carassius shows elevated tricarboxylic acid cycle (TCA cycle) but decreased taurine and hypotaurine metabolism as well as lower biosynthesis of unsaturated fatty acids at 30°C. The decreased abundance of palmitate, threonine, and taurine represents the most characteristic metabolic feature. Consistently, exogenous palmitate, threonine, or taurine enhances the survival of C. carassius to bacterial infection at 30°C in a dose-dependent manner. This effect could be attributed to the inhibition on the TCA cycle by the three metabolites. This notion is further supported by the fact that low concentration of malonate, a succinate dehydrogenase inhibitor, increases the survival of C. carassius at 30°C as well. On the other hand, addition of the three metabolites rescued the decreased expression of pro-inflammatory cytokines including TNF-α1, TNF-α2, IL-1β1, IL-1β2, and lysozyme at 30°C. Taken together, our results revealed an unexpected relationship between temperature and metabolism that orchestrates the immune regulation against infection by bacterial pathogens. Thus, this study shed light on the modulation of finfish physiology to fight against bacterial infection through metabolism.
Highlights
Climate is one of the most important environmental factors that influences the spread of communicable diseases prone to their epidemic [1]
These results indicate that C. carassius compromises taurine and hypotaurine metabolism and biosynthesis of unsaturated fatty acids but boosts the TCA cycle to cope with the temperature stress
L-Proline, a crucial biomarker identified from temperature shift, increased the survival of tilapias infected by Streptococcus agalactiae in high water temperature [39]
Summary
Climate is one of the most important environmental factors that influences the spread of communicable diseases prone to their epidemic [1]. The outbreak of bacterial infectious disease depends on the pathogenicity of the bacteria and many environmental factors, including the temperature changes. The outbreak of bacterial infectious diseases depends on at least two determining factors: [1] the multiple strategies of pathogens to sense the environmental perturbations and fluctuations as cues to adjust their growth, development and pathogenesis. It is well established that the elevated temperature promotes the expression of virulence genes like type III secretion system, temperature-sensitive hemagglutinin, adhesins, and other virulence regulators in the species of Edwardsiella, Vibrio, and Aeromonas [2,3,4,5,6]; [2] the fish’s immune responses to pathogens that affected by residential water temperature. It has long been shown that the elevated temperature negatively affected fish’s immune responses to vaccination and reduced the phagocytosis to bacterial pathogens [7]. The interplay between temperature and host immune response is still largely unexplored [8, 9]
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