BMC Microbiology

official impact factor 2.96

This article is part of the supplement: Arthropod symbioses: from fundamental studies to pest and disease management

Open Access Research

Metabolic stasis in an ancient symbiosis: genome-scale metabolic networks from two Blattabacterium cuenoti strains, primary endosymbionts of cockroaches

Carmen M González-Domenech1,2, Eugeni Belda1, Rafael Patiño-Navarrete1, Andrés Moya1,3,5, Juli Peretó1,4* and Amparo Latorre1,3,5*

Author Affiliations

1 Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, P.O. Box 22085, E-46071, València, Spain

2 Faculty of Pharmacy, University of Granada. Campus of Cartuja, E-18071. Granada, Spain

3 Departament de Genètica, Universitat de València, Spain

4 Departament de Bioquímica i Biologia Molecular, Universitat de València, Spain

5 Centre for Public Health Research (CSISP), E-46020. València, Spain

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BMC Microbiology 2012, 12(Suppl 1):S5 doi:10.1186/1471-2180-12-S1-S5

Published: 18 January 2012

Abstract

Background

Cockroaches are terrestrial insects that strikingly eliminate waste nitrogen as ammonia instead of uric acid. Blattabacterium cuenoti (Mercier 1906) strains Bge and Pam are the obligate primary endosymbionts of the cockroaches Blattella germanica and Periplaneta americana, respectively. The genomes of both bacterial endosymbionts have recently been sequenced, making possible a genome-scale constraint-based reconstruction of their metabolic networks. The mathematical expression of a metabolic network and the subsequent quantitative studies of phenotypic features by Flux Balance Analysis (FBA) represent an efficient functional approach to these uncultivable bacteria.

Results

We report the metabolic models of Blattabacterium strains Bge (iCG238) and Pam (iCG230), comprising 296 and 289 biochemical reactions, associated with 238 and 230 genes, and 364 and 358 metabolites, respectively. Both models reflect both the striking similarities and the singularities of these microorganisms. FBA was used to analyze the properties, potential and limits of the models, assuming some environmental constraints such as aerobic conditions and the net production of ammonia from these bacterial systems, as has been experimentally observed. In addition, in silico simulations with the iCG238 model have enabled a set of carbon and nitrogen sources to be defined, which would also support a viable phenotype in terms of biomass production in the strain Pam, which lacks the first three steps of the tricarboxylic acid cycle. FBA reveals a metabolic condition that renders these enzymatic steps dispensable, thus offering a possible evolutionary explanation for their elimination. We also confirm, by computational simulations, the fragility of the metabolic networks and their host dependence.

Conclusions

The minimized Blattabacterium metabolic networks are surprisingly similar in strains Bge and Pam, after 140 million years of evolution of these endosymbionts in separate cockroach lineages. FBA performed on the reconstructed networks from the two bacteria helps to refine the functional analysis of the genomes enabling us to postulate how slightly different host metabolic contexts drove their parallel evolution.