Friday, November 22, 2024

Bacterial reprogramming of tick metabolism impacts vector fitness and susceptibility to infection – Nature Microbiology

Must read

  • Vector-borne Diseases (WHO, 2020); https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases

  • Kurokawa, C. et al. Interactions between Borrelia burgdorferi and ticks. Nat. Rev. Microbiol. 18, 587–600 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lochhead, R. B., Strle, K., Arvikar, S. L., Weis, J. J. & Steere, A. C. Lyme arthritis: linking infection, inflammation and autoimmunity. Nat. Rev. Rheumatol. 17, 449–461 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • O’Neal, A. J., Singh, N., Mendes, M. T. & Pedra, J. H. F. The genus Anaplasma: drawing back the curtain on tick–pathogen interactions. Pathog. Dis. 79, ftab022 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Smith, R. P. Tick-borne diseases of humans. Emerg. Infect. Dis. 11, 1808–1809 (2005).

    Article 
    PubMed Central 

    Google Scholar
     

  • Verhoeve, V. I., Fauntleroy, T. D., Risteen, R. G., Driscoll, T. P. & Gillespie, J. J. Cryptic genes for interbacterial antagonism distinguish Rickettsia species infecting blacklegged ticks from other Rickettsia pathogens. Front. Cell Infect. Microbiol. 12, 880813 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hagen, R., Verhoeve, V. I., Gillespie, J. J. & Driscoll, T. P. Conjugative transposons and their cargo genes vary across natural populations of Rickettsia buchneri infecting the tick Ixodes scapularis. Genome Biol. Evol. 10, 3218–3229 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kurtti, T. J. et al. Rickettsia buchneri sp. nov., a rickettsial endosymbiont of the blacklegged tick Ixodes scapularis. Int. J. Syst. Evol. Microbiol. 65, 965–970 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cabezas-Cruz, A., Espinosa, P., Alberdi, P. & de la Fuente, J. Tick–pathogen interactions: the metabolic perspective. Trends Parasitol. 35, 316–328 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Samaddar, S., Marnin, L., Butler, L. R. & Pedra, J. H. F. Immunometabolism in arthropod vectors: redefining interspecies relationships. Trends Parasitol. 36, 807–815 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shaw, D. K. et al. Vector immunity and evolutionary ecology: the harmonious dissonance. Trends Immunol. 39, 862–873 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boggs, C. Resource allocation: exploring connections between foraging and life history. Funct. Ecol. 6, 508–518 (1992).

    Article 

    Google Scholar
     

  • Roff, D. Evolution of Life Histories: Theory and Analysis (Springer Science & Business Media, 1993).

  • Stearns, S. C., Rose, M. R. & Mueller, L. D. The evolution of life histories. J. Evol. Biol. 6, 304–306 (1992).


    Google Scholar
     

  • Burger, J. R., Hou, C. & Brown, J. H. Toward a metabolic theory of life history. Proc. Natl Acad. Sci. USA 116, 26653–26661 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, A., Luan, H. H. & Medzhitov, R. An evolutionary perspective on immunometabolism. Science 363, eaar3932 (2019).

  • Russell, D. G., Huang, L. & VanderVen, B. C. Immunometabolism at the interface between macrophages and pathogens. Nat. Rev. Immunol. 19, 291–304 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Warburg, O., Posener, K. & Negelein, E. Über den stoffwechsel der carcinomzelle. Naturwissenschaften 12, 1131–1137 (1924).

    Article 
    CAS 

    Google Scholar
     

  • Ward, P. S. & Thompson, C. B. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 21, 297–308 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G. & Thompson, C. B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7, 11–20 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hall, S. R., Simonis, J. L., Nisbet, R. M., Tessier, A. J. & Cáceres, C. E. Resource ecology of virulence in a planktonic host–parasite system: an explanation using dynamic energy budgets. Am. Nat. 174, 149–162 (2009).

    Article 
    PubMed 

    Google Scholar
     

  • Peyraud, R., Cottret, L., Marmiesse, L., Gouzy, J. & Genin, S. A resource allocation trade-off between virulence and proliferation drives metabolic versatility in the plant pathogen Ralstonia solanacearum. PLoS Pathog. 12, e1005939 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hite, J. L., Pfenning, A. C. & Cressler, C. E. Starving the enemy? Feeding behavior shapes host–parasite interactions. Trends Ecol. Evol. 35, 68–80 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Cressler, C. E., Nelson, W. A., Day, T. & McCauley, E. Disentangling the interaction among host resources, the immune system and pathogens. Ecol. Lett. 17, 284–293 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Voss, K. et al. A guide to interrogating immunometabolism. Nat. Rev. Immunol. 21, 637–652 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Song, X., Zhong, Z., Gao, L., Weiss, B. L. & Wang, J. Metabolic interactions between disease-transmitting vectors and their microbiota. Trends Parasitol. 38, 697–708 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hoxmeier, J. C. et al. Metabolomics of the tick–Borrelia interaction during the nymphal tick blood meal. Sci. Rep. 7, 1–11 (2017).

    Article 

    Google Scholar
     

  • Cabezas-Cruz, A., Alberdi, P., Valdes, J. J., Villar, M. & de la Fuente, J. Anaplasma phagocytophilum infection subverts carbohydrate metabolic pathways in the tick vector, Ixodes scapularis. Front. Cell Infect. Microbiol. 7, 23 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Alberdi, P. et al. The redox metabolic pathways function to limit Anaplasma phagocytophilum infection and multiplication while preserving fitness in tick vector cells. Sci. Rep. 9, 13236 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dahmani, M., Anderson, J. F., Sultana, H. & Neelakanta, G. Rickettsial pathogen uses arthropod tryptophan pathway metabolites to evade reactive oxygen species in tick cells. Cell. Microbiol. 22, e13237 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Namjoshi, P., Dahmani, M., Sultana, H. & Neelakanta, G. Rickettsial pathogen inhibits tick cell death through tryptophan metabolite mediated activation of p38 MAP kinase. iScience 26, 105730 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Villar, M. et al. Integrated metabolomics, transcriptomics and proteomics identifies metabolic pathways affected by Anaplasma phagocytophilum infection in tick cells. Mol. Cell. Proteomics 14, 3154–3172 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mookerjee, S. A., Gerencser, A. A., Nicholls, D. G. & Brand, M. D. Quantifying intracellular rates of glycolytic and oxidative ATP production and consumption using extracellular flux measurements. J. Biol. Chem. 292, 7189–7207 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nicholls, D. G. et al. Bioenergetic profile experiment using C2C12 myoblast cells. J. Vis. Exp. 46, e2511 (2010).

  • Munderloh, U. G., Liu, Y., Wang, M., Chen, C. & Kurtti, T. J. Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. J. Parasitol. 80, 533–543 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Troughton, D. R. & Levin, M. L. Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J. Med. Entomol. 44, 732–740 (2007).

    Article 
    PubMed 

    Google Scholar
     

  • Kocan, K. M., de la Fuente, J. & Coburn, L. A. Insights into the development of Ixodes scapularis: a resource for research on a medically important tick species. Parasit. Vectors 8, 592 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Troha, K. & Ayres, J. S. Metabolic adaptations to infections at the organismal level. Trends Immunol. 41, 113–125 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rosenberg, G., Riquelme, S., Prince, A. & Avraham, R. Immunometabolic crosstalk during bacterial infection. Nat. Microbiol. 7, 497–507 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Thapa, S., Zhang, Y. & Allen, M. S. Bacterial microbiomes of Ixodes scapularis ticks collected from Massachusetts and Texas, USA. BMC Microbiol. 19, 138 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Van Treuren, W. et al. Variation in the microbiota of Ixodes ticks with regard to geography, species, and sex. Appl. Environ. Microbiol. 81, 6200–6209 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roberts, L. D. et al. β-aminoisobutyric acid induces browning of white fat and hepatic β-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab. 19, 96–108 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tanianskii, D. A., Jarzebska, N., Birkenfeld, A. L., O’Sullivan, J. F. & Rodionov, R. N. β-aminoisobutyric acid as a novel regulator of carbohydrate and lipid metabolism. Nutrients 11, 524 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sharma, A. et al. Cas9-mediated gene editing in the black-legged tick, Ixodes scapularis, by embryo injection and ReMOT Control. iScience 25, 103781 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sawada, M., Yamamoto, H., Ogasahara, A., Tanaka, Y. & Kihara, S. β-aminoisobutyric acid protects against vascular inflammation through PGC-1β-induced antioxidative properties. Biochem. Biophys. Res. Commun. 516, 963–968 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kitase, Y. et al. β-aminoisobutyric acid, BAIBA, is a muscle-derived osteocyte survival factor. Cell Rep. 22, 1531–1544 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhu, X. W., Ding, K., Dai, X. Y. & Ling, W. Q. β-aminoisobutyric acid accelerates the proliferation and differentiation of MC3T3-E1 cells via moderate activation of ROS signaling. J. Chin. Med. Assoc. 81, 611–618 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Alasmari, S. & Wall, R. Determining the total energy budget of the tick Ixodes ricinus. Exp. Appl. Acarol. 80, 531–541 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Corona, A. & Schwartz, I. Borrelia burgdorferi: carbon metabolism and the tick-mammal enzootic cycle. Microbiol. Spectr. 3, 10 (2015).

    Article 

    Google Scholar
     

  • Rikihisa, Y. Mechanisms of obligatory intracellular infection with Anaplasma phagocytophilum. Clin. Microbiol. Rev. 24, 469–489 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Driscoll, T. P. et al. Wholly Rickettsia! reconstructed metabolic profile of the quintessential bacterial parasite of eukaryotic cells. MBio 8, e00859–17 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dumler, J. S. et al. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 51, 2145–2165 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Narasimhan, S. et al. Grappling with the tick microbiome. Trends Parasitol. 37, 722–733 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gillespie, J. J. et al. A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. J. Bacteriol. 194, 376–394 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xiong, Q., Lin, M., Huang, W. & Rikihisa, Y. Infection by Anaplasma phagocytophilum requires recruitment of low-density lipoprotein cholesterol by flotillins. MBio 10, e02783–18 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Villar, M. et al. Identification and characterization of Anaplasma phagocytophilum proteins involved in infection of the tick vector, Ixodes scapularis. PLoS ONE 10, e0137237 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Villar, M. et al. The intracellular bacterium Anaplasma phagocytophilum selectively manipulates the levels of vertebrate host proteins in the tick vector Ixodes scapularis. Parasit. Vectors 9, 467 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Truchan, H. K. et al. Anaplasma phagocytophilum Rab10-dependent parasitism of the trans-Golgi network is critical for completion of the infection cycle. Cell. Microbiol. 18, 260–281 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shi, C. X. et al. β-aminoisobutyric acid attenuates hepatic endoplasmic reticulum stress and glucose/lipid metabolic disturbance in mice with type 2 diabetes. Sci. Rep. 6, 21924 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Audzeyenka, I. et al. β-aminoisobutyric acid (L-BAIBA) is a novel regulator of mitochondrial biogenesis and respiratory function in human podocytes. Sci. Rep. 13, 766 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Oliva Chávez, A. S. et al. Tick extracellular vesicles enable arthropod feeding and promote distinct outcomes of bacterial infection. Nat. Commun. 12, 3696 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yoshiie, K., Kim, H. Y., Mott, J. & Rikihisa, Y. Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect. Immun. 68, 1125–1133 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Labandeira-Rey, M. & Skare, J. T. Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect. Immun. 69, 446–455 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shaw, D. K. et al. Infection-derived lipids elicit an immune deficiency circuit in arthropods. Nat. Commun. 8, 14401 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Collet, T.-H. et al. A metabolomic signature of acute caloric restriction. J. Clin. Endocrinol. Metab. 102, 4486–4495 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Evans, A. et al. High resolution mass spectrometry improves data quantity and quality as compared to unit mass resolution mass spectrometry in high-throughput profiling metabolomics. Metabolomics 4, 1 (2014).


    Google Scholar
     

  • DeHaven, C. D., Evans, A. M., Dai, H. & Lawton, K. A. Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J. Cheminform. 2, 9 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sidak-Loftis, L. C. et al. The unfolded-protein response triggers the arthropod immune deficiency pathway. MBio 13, e00703–e00722 (2022).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Latest article