Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica

Abstract

Bacterial endosymbionts of insects play a central role in upgrading the diet of their hosts. In certain cases, such as aphids and tsetse flies, endosymbionts complement the metabolic capacity of hosts living on nutrient-deficient diets, while the bacteria harbored by omnivorous carpenter ants are involved in nitrogen recycling. In this study, we describe the genome sequence and inferred metabolism of Blattabacterium strain Bge, the primary Flavobacteria endosymbiont of the omnivorous German cockroach Blattella germanica. Through comparative genomics with other insect endosymbionts and free-living Flavobacteria we reveal that Blattabacterium strain Bge shares the same distribution of functional gene categories only with Blochmannia strains, the primary Gamma-Proteobacteria endosymbiont of carpenter ants. This is a remarkable example of evolutionary convergence during the symbiotic process, involving very distant phylogenetic bacterial taxa within hosts feeding on similar diets. Despite this similarity, different nitrogen economy strategies have emerged in each case. Both bacterial endosymbionts code for urease but display different metabolic functions: Blochmannia strains produce ammonia from dietary urea and then use it as a source of nitrogen, whereas Blattabacterium strain Bge codes for the complete urea cycle that, in combination with urease, produces ammonia as an end product. Not only does the cockroach endosymbiont play an essential role in nutrient supply to the host, but also in the catabolic use of amino acids and nitrogen excretion, as strongly suggested by the stoichiometric analysis of the inferred metabolic network. Here, we explain the metabolic reasons underlying the enigmatic return of cockroaches to the ancestral ammonotelic state.

Identification and functional characterization of an ovarian aquaporin from the cockroachBlattella germanicaL. (Dictyoptera, Blattellidae)

“…Nevertheless, the permeability of BgAQP to urea may be physiologically relevant because a metabolic complementation for nitrogen metabolism appears to exist between B. germanica and their endosymbiont B. cuenoti through the combination of a urea cycle (host) and urease activity (endosymbiont) (Lopez-Sanchez et al, 2009).…”

“…They were obtained from a colony reared in the dark at 30±1°C and 60-70% relative humidity in a non-aseptic environment. Under these conditions, the cockroach fat body and ovary harbour the endosymbiont bacteroid Blattabacterium cuenoti (Giorgi and Nordin, 1994;Lopez-Sanchez et al, 2009). Sixth instar nymphs or freshly ecdysed adult females were selected from the colony and used at appropriate ages.…”

“…BLAST analyses against the genome of B. cuenoti (Lopez-Sanchez et al, 2009) revealed that the bacteroid does not have any gene sequence matching the nucleotide sequence of BgAQP, which indicates that the cloned cDNA must have come from B. germanica. Next, in order to place BgAQP in an evolutionary context within insects, we carried out a phylogenetic analysis of representative insect AQPs available in public databases.…”

Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion

“…; Bandi et al 1994). These bacteria apparently recycle uric acid reserves, providing the insect with usable nitrogenous compounds during times of nitrogen famine (Dasch et al 1984;Ishikawa 1989;Lopez-Sanchez et al 2009). Thus, when feeding on complex diets, symbiotic bacteria may act as a buffering agent-filling up the nutrient voids in the varied landscape of their host's diet and consequently optimizing fitness.…”

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts

“…Microorganisms can form different kinds of associations with eukaryotic hosts ranging from a facultative epiphytic life on green algae (8) to obligate intracellular symbiosis in insects (9). Symbionts can be acquired horizontally by the host, for example from the seawater for green algae (8) or from food in the human gut (10), and this mode of acquisition will lead to recruitment and selection based on symbiont function.…”