Boric acid enhances Metarhizium anisopliae virulence in Blattella germanica (L.) by disrupting the gut and altering its microbial community

Abstract

Extensive use of insecticides has caused widespread resistance in German cockroach (Blattella germanica) populations on a global scale. Biological control has potential to mitigate insecticide resistance, and Metarhizium anisopliae, an entomopathogenic fungus, has shown good efficacy against cockroaches alone and in combination with various insecticides, including boric acid. To investigate the mechanism(s) that underlie synergism between M. anisopliae and boric acid, we conducted dose-response assays with combinations of fungus and boric acid fed to cockroaches and histological observations of the midgut and we characterized the gut microbiome of treated cockroaches. The combination treatments were synergistic with co-toxicity factors >20 at 4 out of 12 treatments and LT50 values of 5 days at the highest concentration of boric acid. M. anisopliae reached the hemocoel faster when it was ingested with boric acid, likely because boric acid disrupted the epithelial cells of the midgut. The gut microbiome was also altered by these treatments. The abundance of Parabacteroides and Enterococcus, with known anti-inflammatory and antifungal activity, declined in boric acid and combination treatments, whereas Weissella, an opportunistic pathogen, significantly increased in these treatments. We conclude that two major mechanisms underlie this synergism: (1) boric acid facilitates the penetration of M. anisopliae by physically and chemically disrupting the midgut, and (2) by altering the gut microbiome, boric acid promotes survival and virulence of M. anisopliae in the harsh gut environment.