Abstract
Gut symbiotic bacteria have a substantial impact on host physiology and ecology. However, the contribution of gut microbes to host fitness during long-term low-temperature stress is still unclear. This study examined the role of gut microbiota in host low-temperature stress resistance at molecular and biochemical levels in the oriental fruit fly Bactrocera dorsalis. The results showed that after the gut bacteria of flies were removed via antibiotic treatment, the median survival time was significantly decreased to approximately 68% of that in conventional flies following exposure to a temperature stress of 10°C. Furthermore, we found that Klebsiella michiganensis BD177 is a key symbiotic bacterium, whose recolonization in antibiotic treated (ABX) flies significantly extended the median survival time to 160% of that in the ABX control, and restored their lifespan to the level of conventional flies. Notably, the relative levels of proline and arginine metabolites were significantly downregulated by 34- and 10-fold, respectively, in ABX flies compared with those in the hemolymph of conventional flies after exposure to a temperature stress of 10°C whereas recolonization of ABX flies by K. michiganensis BD177 significantly upregulated the levels of proline and arginine by 13- and 10- fold, respectively, compared with those found in the hemolymph of ABX flies. qPCR analysis also confirmed that K. michiganensis-recolonized flies significantly stimulated the expression of transcripts from the arginine and proline metabolism pathway compared with the ABX controls, and RNAi mediated silencing of two key genes Pro-C and ASS significantly reduced the survival time of conventional flies, postexposure low-temperature stress. We show that microinjection of L-arginine and L-proline into ABX flies significantly increased their survival time following exposure to temperature stress of 10°C. Transmission electron microscopy (TEM) analysis further revealed that low-temperature stress caused severe destruction in cristae structures and thus resulted in abnormal circular shapes of mitochondria in ABX flies gut, while the recolonization of live K. michiganensis helped the ABX flies to maintain mitochondrial functionality to a normal status, which is important for the arginine and proline induction. Our results suggest that gut microbiota plays a vital role in promoting the host resistance to low-temperature stress in B. dorsalis by stimulating its arginine and proline metabolism pathway.
Highlights
Animals are inevitably challenged by adverse environmental conditions, such as extreme temperature, toxic substances or pathogen infections, ultraviolet (UV) radiation, insecticide exposure and oxidative stress [1, 2]
By combining transcriptomic and metabolomic approaches, we found that the presence of gut symbionts, especially K. michiganensis BD177, helps the host B. dorsalis to elevate the levels of particular cryoprotectant transcripts and metabolites, which suggests that the gut symbiont K. michiganensis BD177 stimulates the host arginine and proline metabolism pathway to promote its resistance to long-term low-temperature stress via influencing the mitochondrial functionality
To investigate a possible role of gut microbiota in host resistance to temperature stress, ABX and conventional flies were subjected to different longterm low- to mild-temperatures stresses of 5 ̊C (S1B Fig), 7.5 ̊C (S1C Fig), 10 ̊C (Fig 1D) and 15 ̊C (S1D Fig); 10 ̊C was chosen for the subsequent studies because this was the lowest temperature at which we found a significant difference in the median survival time between conventional and ABX flies (Fig 1D)
Summary
Animals are inevitably challenged by adverse environmental conditions, such as extreme temperature, toxic substances or pathogen infections, ultraviolet (UV) radiation, insecticide exposure and oxidative stress [1, 2]. Environmental stress has a direct effect on metabolism and cellular processes that affect individual survival [3,4,5]. Some invasive insect pests of fruit crops exhibit a unique form of phenotypic response [10, 11] to mild or even extreme temperature conditions [12, 13] or a rapid adaptation of thermal traits [14, 15] that may facilitate the survival of those introduced or alien species in novel environments. Unpredictable climatic conditions, sudden cold spells or milder winters are among the explanatory factors involved in the reduced mortality [16], distribution and dynamics of many insect pest species [17]. The mechanisms underlying cold acclimation responses are the main focus of much research in insect species [18, 19]
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