Nitrogen recycling and nutritional provisioning byBlattabacterium, the cockroach endosymbiont

Abstract

Nitrogen acquisition and assimilation is a primary concern of insects feeding on diets largely composed of plant material. Reclaiming nitrogen from waste products provides a rich reserve for this limited resource, provided that recycling mechanisms are in place. Cockroaches, unlike most terrestrial insects, excrete waste nitrogen within their fat bodies as uric acids, postulated to be a supplement when dietary nitrogen is limited. The fat bodies of most cockroaches are inhabited by Blattabacterium, which are vertically transmitted, Gram-negative bacteria that have been hypothesized to participate in uric acid degradation, nitrogen assimilation, and nutrient provisioning. We have sequenced completely the Blattabacterium genome from Periplaneta americana. Genomic analysis confirms that Blattabacterium is a member of the Flavobacteriales (Bacteroidetes), with its closest known relative being the endosymbiont Sulcia muelleri, which is found in many sap-feeding insects. Metabolic reconstruction indicates that it lacks recognizable uricolytic enzymes, but it can recycle nitrogen from urea and ammonia, which are uric acid degradation products, into glutamate, using urease and glutamate dehydrogenase. Subsequently, Blattabacterium can produce all of the essential amino acids, various vitamins, and other required compounds from a limited palette of metabolic substrates. The ancient association with Blattabacterium has allowed cockroaches to subsist successfully on nitrogen-poor diets and to exploit nitrogenous wastes, capabilities that are critical to the ecological range and global distribution of cockroach species.