Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold
Girish Neelakanta, … , John F. Anderson, Erol Fikrig
Girish Neelakanta, … , John F. Anderson, Erol Fikrig
Published August 25, 2010
Citation Information: J Clin Invest. 2010;120(9):3179-3190. https://doi.org/10.1172/JCI42868.
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Research Article

Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold

Abstract

In the United States, Ixodes scapularis ticks overwinter in the Northeast and Upper Midwest and transmit the agent of human granulocytic anaplasmosis, Anaplasma phagocytophilum, among other pathogens. We now show that the presence of A. phagocytophilum in I. scapularis ticks increases their ability to survive in the cold. We identified an I. scapularis antifreeze glycoprotein, designated IAFGP, and demonstrated via RNAi knockdown studies the importance of IAFGP for the survival of I. scapularis ticks in a cold environment. Transfection studies also show that IAFGP increased the viability of yeast cells subjected to cold temperature. Remarkably, A. phagocytophilum induced the expression of iafgp, thereby increasing the cold tolerance and survival of I. scapularis. These data define a molecular basis for symbiosis between a human pathogenic bacterium and its arthropod vector and delineate what we believe to be a new pathway that may be targeted to alter the life cycle of this microbe and its invertebrate host.

Authors

Girish Neelakanta, Hameeda Sultana, Durland Fish, John F. Anderson, Erol Fikrig

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Figure 1

A. phagocytophilum–infected nymphs survive better at cold temperatures.

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A. phagocytophilum–infected nymphs survive better at cold temperatures....
(A) Survival of uninfected and A. phagocytophilum–infected (A. phag–infected) unfed nymphs at –20°C for 0, 10, 15, 20, 25, 30, 45, or 90 minutes. Data from 2 independent experiments with 10 ticks/group/time point/experiment are shown. The dashed box indicates the LT50 time point for ticks at –20°C. Mean ± SD error bars from 2 independent experiments are shown for comparison. (B) Survival of uninfected and A. phagocytophilum–infected unfed nymphs at the LT50 (–20°C, 25 minutes) from 18 independent experiments. Each circle represents 1 independent experiment (10 ticks/group/experiment). The difference in the survival between A. phagocytophilum–infected and uninfected nymphs is significant (P < 0.001). (C) Mobility (in cm) by uninfected or A. phagocytophilum–infected unfed nymphs after cold shock at LT50. Each circle represents 1 individual tick. Survival (D and F) and mobility (E and G) measurements of uninfected and A. phagocytophilum–infected unfed nymphs at LT50 in a sequential (D and E) and scrambled (F and G) cold tolerance assay. Each circle in D and F represents 1 independent experiment (10 ticks/group/experiment) and in E and G represents 1 individual tick. In all panels, white circles represent uninfected ticks and black circles represent A. phagocytophilum–infected ticks. For all panels, statistical significance was calculated using Mann-Whitney U nonparametric test. n = 70 (C); n = 60 (E); n = 30 (G) for both uninfected and A. phagocytophilum–infected ticks. Horizontal lines in B–G indicate the median of the readings from independent experiment/ticks.