ScienceDaily (Nov. 16, 2009) — A study by scientists from the University of Valencia sheds new light on how the cockroach organism works. A research team from the Cavanilles Institute for Biodiversity and Evolutionary Biology, led by professors Amparo Latorre and Andrés Moya, has shown why the German cockroach (Blatella germanica) eliminates excess nitrogen by excreting ammonia, in contrast to most terrestrial insects that commonly produce uric acid as a waste compound. The research is published November 13 in the open-access journal PLoS Genetics.
Cockroach. A study by scientists from the University of Valencia sheds new light on how the cockroach organism works. (Credit: iStockphoto)
The biochemical explanation of nitrogen secretion as ammonia in cockroaches, something that has puzzled insect physiologists for years, was determined from the whole genome sequence of the German cockroach's bacterial endosymbiont -- Blattabacterium strain Bge, a bacterium living within cockroach cells -- and the inference of its metabolic network. In order to produce ammonia "the bacterial metabolism employs an apparently inefficient mechanism: bacterial enzymes simultaneously synthesize, by an energetically expensive pathway, and destroy the same molecule, urea," explains Amparo Latorre of the University of Valencia. The authors point out that this surprising mechanism makes sense when considering the metabolic interaction between endosymbiont bacteria and their host and the whole physiology of the cockroach.
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Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica
Maria J. López-Sánchez1, Alexander Neef1,2, Juli Peretó1,2,3, Rafael Patiño-Navarrete1, Miguel Pignatelli1,2,4, Amparo Latorre1,2,4,5, Andrés Moya1,2,4,5*
1 Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, València, Spain, 2 CIBER en Epidemiología y Salud Pública (CIBEResp), Barcelona, Spain, 3 Departament de Bioquímica i Biologia Molecular, Universitat de València, València, Spain, 4 Centro Superior de Investigación en Salud Pública (CSISP), València, Spain, 5 Departament de Genètica, Universitat de València, València, Spain
Abstract Top
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.
Author Summary Top
Bacterial endosymbionts from insects are subjected to a process of genome reduction from the moment they interact with their host, especially when the symbiosis is strict (the partners live together permanently) and the endosymbiont is maternally inherited. The type of genes that are retained correlates with specific metabolic host requirements. Here, we report the genome sequence of Blattabacterium strain Bge, the primary endosymbiont of the German cockroach B. germanica. Cockroaches are omnivorous insects and Blattabacterium cooperates with their metabolism, not only with essential nutrient metabolism but also through an efficient use of amino acids and the nitrogen excretion by the combination of a urea cycle and urease activity. The repertoires of functions that are maintained in Blattabacterium are similar to those already observed in Blochmannia spp., the primary endosymbiont of carpenter ants, also an omnivorous insect. This constitutes a nice example of evolutionary convergence of two endosymbionts belonging to very different bacterial phyla that have evolved a similar repertoire of functions according to the host. However, the current set of genes and, more importantly, those that were lost in the process of genome reduction in both endosymbiont lineages have also contributed to a different involvement of Blattabacterium and Blochmannia in nitrogen metabolism.
Citation: López-Sánchez MJ, Neef A, Peretó J, Patiño-Navarrete R, Pignatelli M, et al. (2009) Evolutionary Convergence and Nitrogen Metabolism in Blattabacterium strain Bge, Primary Endosymbiont of the Cockroach Blattella germanica. PLoS Genet 5(11): e1000721. doi:10.1371/journal.pgen.1000721
Editor: Seth R. Bordenstein, Vanderbilt University, United States of America
Received: July 31, 2009; Accepted: October 15, 2009; Published: November 13, 2009
Copyright: © 2009 López-Sánchez et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Financial support was provided by grants BFU2006/06003/BMC and BFU2009-12895-C02-01/BMC (Ministerio de Ciencia e Innovación Spain) to A. Latorre and European Community's Seventh Framework Programme (FP7/2007–2013) under grant agreement number 212894 and Prometeo/2009/092 (Conselleria D'Educació, Generalitat Valenciana, Spain) to A. Moya. M. J. López-Sánchez and R. Patiño-Navarrete were recipients of a fellowship from Ministerio de Educación y Ciencia, Spain. A. Neef is supported by an Intra-European Marie Curie fellowship (LSHM-CT-2005_019023) from the European Union. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: andres.moya@uv.es
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