Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

PEDRINI NICOLAS; ORTIZ-URQUIZA ALMUDENA; HUARTE BONNET CARLA; FAN YANHUA; M PATRICIA JUÁREZ; KEYHANI NEMAT O

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

NATL ACAD SCIENCES

Lugar: Washington DC, USA; Año: 2015 vol. 112 p. 3651 - 3660

0027-8424

PNAS 2015 112 (28) E3651-E3660. Entomopathogenic fungi and their insect hosts represent a model system for examining invertebrate-pathogen co-evolutionary selection processes. Here we report the characterization of competing components of an arms race consisting of insect protective antimicrobial compounds and evolving fungal-pathogen mechanisms of detoxification. The insect pathogenic fungus, Beauveria bassiana has a remarkably wide host range;however, some insects show a high degree of resistance to fungal infection. Amongst resistant insects is the tenebrionid beetle Tribolium castaneum that produces benzoquinone-containing defensive secretions. Reduced fungal germination and growth was seen in media containing T. castaneum dichloromethane-extracts or synthetic benzoquinone. In response to benzoquinone exposure, the fungus expresses a 1,4-benzoquinone oxidoreductase,BbbqrA,induced >40-fold. Gene knockout mutants(ΔBbbqrA) showed increased growth inhibition, whereas B. bassiana overexpressing BbbqrA (Bb::BbbqrAO), displayed increased resistance to benzoquinone compared to wild-type. Increased benzoquinone reductase activity was detected in both wild-type cells exposed to benzoquinone and in the over-expression strain. Heterologous expression and purification of BbbqrA in E. coli confirmed NAD(P)H-dependent benzoquinone reductase activity.The ΔBbbqrA strain showed decreased virulence towards T. castaneum, whereas overexpression of BbbqrA increased mortality versus T. castaneum. No change in virulence was seen for the ΔBbbqrA or Bb::BbbqrAOstrains when tested against the greater waxmoth, Galleria mellonella or the weevil, Sitophilus oryzae, neither of which produce significant amounts of cuticular quinones. The observation that artificial over-expression of BbbqrA results in increased virulence only towards quinone-secreting insects implies the lack of strong selection or failure of B. bassiana to counter adapt to this particular host defense throughout evolution.