Cross-epithelial hydrogen transfer from the midgut compartment drives methanogenesis in the hindgut of cockroaches

In the intestinal tracts of animals, methanogenesis from CO2 and other C-1 compounds strictly depends on the supply of electron donors by fermenting b acteria, but sources and sinks of reducing equivalents may be spatially sep arated. Microsensor measurements in the intestinal tract of the omnivorous cockroach Blaberus sp. showed that molecular hydrogen strongly accumulated in the midgut (H-2 partial pressures of 3 to 26 kPa), whereas it was not de tectable (<0.1 kPa) in the posterior hindgut. Moreover, living cockroaches emitted large quantities of CH4 [105 +/- 49 nmol (g of cockroach)(-1) h(-1) ] but only traces of H-2. In vitro incubation of isolated gut compartments, however, revealed that the midguts produced considerable amounts of H-2, w hereas hindguts emitted only CH4 [106 +/- 58 and 71 +/- 50 nmol (g of cockr oach)(-1) h(-1), respectively]. When ligated midgut and hindgut segments we re incubated in the same vials, methane emission increased by 28% over that of isolated hindguts, whereas only traces of H-2 accumulated in the headsp ace. Radial hydrogen profiles obtained under air enriched with H-2 (20 kPa) identified the hindgut as an efficient sink for externally supplied H-2. A cross-epithelial transfer of hydrogen from the midgut to the hindgut compa rtment was clearly evidenced by the steep H-2 concentration gradients which developed when ligated fragments of midgut and hindgut were placed on top of each other-a configuration that simulates the situation in vivo. These f indings emphasize that it is essential to analyze the compartmentalization of the gut and the spatial organization of its microbiota in order to under stand the functional interactions among different microbial populations dur ing digestion.