Gut microbiota promotes host resistance to low-temperature stress by stimulating its arginine and proline metabolism pathway in adult Bactrocera dorsalis

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 a...

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Bibliographic Details
Published in:PLoS pathogens 2020-04, Vol.16 (4), p.e1008441-e1008441
Main Authors: Raza, Muhammad Fahim, Wang, Yichen, Cai, Zhaohui, Bai, Shuai, Yao, Zhichao, Awan, Umar Anwar, Zhang, Zhenyu, Zheng, Weiwei, Zhang, Hongyu
Format: Article
Language:English
Subjects:
Amino acids
Analysis
Animal reproduction
Antibiotics
Arginine
Bacteria
Bactrocera dorsalis
Biochemistry
Biology and Life Sciences
Cristae
Destruction
Electron microscopy
Entomology
Exposure
Fruit flies
Fruit flies (Tephritidae)
Fruits
Genes
Hemolymph
Horticulture
Insecticides
Intestinal microflora
Klebsiella
L-Proline
Laboratories
Levels
Life span
Low temperature
Low temperature resistance
Medicine and Health Sciences
Metabolism
Metabolites
Microbiota
Microbiota (Symbiotic organisms)
Microinjection
Microorganisms
Microscopy
Mitochondria
Physical Sciences
Physiological aspects
Plant biology
Plant sciences
Proline
Recolonization
RNA interference
RNA-mediated interference
Stress
Survival
Time
Transmission electron microscopy
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Summary: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
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1008441