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Bacterial reprogramming of tick metabolism impacts vector fitness and susceptibility to infection
Sourabh Samaddar1, Agustin Rolandelli1, Anya J O'Neal1,2
1Department of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, MD, USA.
Abstract:
Arthropod-borne pathogens are responsible for hundreds of millions of infections in humans each year. The blacklegged tick, Ixodes scapularis, is the predominant arthropod vector in the United States and is responsible for transmitting several human pathogens, including the Lyme disease spirochete Borrelia burgdorferi and the obligate intracellular rickettsial bacterium Anaplasma phagocytophilum, which causes human granulocytic anaplasmosis. However, tick metabolic response to microbes and whether metabolite allocation occurs upon infection remain unknown. Here we investigated metabolic reprogramming in the tick ectoparasite I. scapularis and determined that the rickettsial bacterium A. phagocytophilum and the spirochete B. burgdorferi induced glycolysis in tick cells. Surprisingly, the endosymbiont Rickettsia buchneri had a minimal effect on bioenergetics. An unbiased metabolomics approach following A. phagocytophilum infection of tick cells showed alterations in carbohydrate, lipid, nucleotide and protein metabolism, including elevated levels of the pleiotropic metabolite β-aminoisobutyric acid. We manipulated the expression of genes associated with β-aminoisobutyric acid metabolism in I. scapularis, resulting in feeding impairment, diminished survival and reduced bacterial acquisition post haematophagy. Collectively, we discovered that metabolic reprogramming affects interspecies relationships and fitness in the clinically relevant tick I. scapularis.
Insights
Tick infection with pathogens like Anaplasma phagocytophilum triggers metabolic changes, impacting tick survival and disease transmission. Understanding these metabolic shifts is key to controlling tick-borne diseases.
Area of Science:
- Vector-borne disease research
- Tick biology and metabolism
- Infectious disease pathogenesis
Background:
- Arthropod-borne pathogens cause millions of human infections annually.
- Ixodes scapularis ticks transmit pathogens like Borrelia burgdorferi and Anaplasma phagocytophilum.
- Tick metabolic responses to microbial infections are largely unknown.
Purpose of the Study:
- To investigate metabolic reprogramming in Ixodes scapularis ticks upon infection.
- To determine if metabolite allocation occurs in ticks post-infection.
- To understand the role of tick metabolism in host-pathogen interactions and tick fitness.
Main Methods:
- Infection of tick cells with Anaplasma phagocytophilum and Borrelia burgdorferi.
- Metabolomic analysis to identify changes in tick metabolites.
- Gene expression manipulation related to β-aminoisobutyric acid metabolism in ticks.
Main Results:
- Anaplasma phagocytophilum and Borrelia burgdorferi induced glycolysis in tick cells.
- Endosymbiont Rickettsia buchneri had minimal impact on tick bioenergetics.
- A. phagocytophilum infection altered carbohydrate, lipid, nucleotide, and protein metabolism, increasing β-aminoisobutyric acid levels.
- Manipulation of β-aminoisobutyric acid metabolism genes impaired tick feeding, survival, and bacterial acquisition.
Conclusions:
- Tick metabolic reprogramming is a significant response to microbial infection.
- Metabolite alterations, such as elevated β-aminoisobutyric acid, affect tick fitness and pathogen acquisition.
- Understanding tick metabolism offers insights into controlling the transmission of tick-borne diseases.
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