Neonicotinoids stimulate H2-limited methane emission in Periplaneta americana through the regulation of gut bacterium community

Methane emitted by insects is considered to be an important source of atmospheric methane. Here we report the stimulation of methane emission in Periplaneta americana, an insect species with abundant methanogens, by neonicotinoids, insecticides widely used to control insect pests. The application of cycloxaprid (CYC) and imidacloprid (IMI) caused foregut expansion in P. americana, and increased the methane production and emission. Antibiotics could mostly eliminate the stimulatory effects. In P. americana gut, hydrogen levels increased and pH values decreased, which could be significantly explained by the gut bacterium community change. The proportion of several bacterium genera increased in guts following CYC treatment, and four genera from five with increased proportions could generate hydrogen at anaerobic conditions. Hydrogen is a central intermediate in methanogenesis. Gut methanogens could use the increased hydrogen to produce more methane, especially at acidic conditions. Following neonicotinoid applications, all increased methanogens in both foregut and hindgut used hydrogen as electron donor to produce methane. Besides, the up-regulation of mcrA, encoding the enzyme that catalyzes the final step of methanogenesis, suggested an enhanced methane production ability in present methanogens. In the termite Coptotermes chaohuensis, another methanogen-abundant insect species, hydrogen levels in gut and methane emission significantly increased after neonicotinoid treatment, which was similar to the results in P. americana. In summary, neonicotinoids changed bacterium community in P. americana gut to generate more hydrogen, which then stimulate gut methanogens to produce and emit more methane. The finding raised a new concern over neonicotinoid applications, and might be a potential environmental risk associated with global warming.