A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola

Thomas, Gavin H.; Zucker, Jeremy; MacDonald, Sandy; Sorokin, Anatoly; Goryanin, Igor; Douglas, Angela E.

doi:10.1186/1752-0509-3-24

Cited by 95 publications

(126 citation statements)

References 24 publications

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“…For instance, nitrogen fixation in Rhizobium etli bacteroids at the root nodules of the bean plant has recently been modeled [48]. Moreover, Buchnera aphidicola, intracellular endosymbiont of pea aphids, and Sodalis glossinidius, endosymbiont of tsetse flies, have been recently reconstructed [49,50].…”

Section: Resultsmentioning

confidence: 99%

A systems biology approach to studying the role of microbes in human health

Thiele¹,

Heinken²,

Fleming³

2013

Current Opinion in Biotechnology

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Section: Resultsmentioning

confidence: 99%

A systems biology approach to studying the role of microbes in human health

Thiele¹,

Heinken²,

Fleming³

2013

Current Opinion in Biotechnology

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“…The metabolic network of B. aphidicola has been reconstructed and the metabolic flux through the network, as investigated by flux balance analysis, results in the net production of both succinate and acetate, i.e., these compounds are "overflow metabolites". 55 Succinate is a product of succinyl-diaminopimelate desuccinylase (DapE), a reaction in the lysine biosynthetic pathway; and B. aphidicola lacks the genetic capacity to utilize succinate. The increased succinate content of aphids on diet-L may, therefore, relate to an increased production of the essential amino acid lysine by B. aphidicola in these aphids.…”

Section: Discussionmentioning

confidence: 99%

Integrated Metabonomic−Proteomic Analysis of an Insect−Bacterial Symbiotic System

et al. 2010

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The health of animals, including humans, is dependent on their resident microbiota, but the complexity of the microbial communities makes these associations difficult to study in most animals. Exceptionally, the microbiology of the pea aphid Acyrthosiphon pisum is dominated by a single bacterium Buchnera aphidicola (B. aphidicola). A 1 H NMR-based metabonomic strategy was applied to investigate metabolic profiles of aphids fed on a low essential amino acid diet and treated by antibiotic to eliminate B. aphidicola. In addition, differential gel electrophoresis (DIGE) with mass spectrometry was utilized to determine the alterations of proteins induced by these treatments. We found that these perturbations resulted in significant changes to the abundance of 15 metabolites and 238 proteins. Ten (67%) of the metabolites with altered abundance were amino acids, with nonessential amino acids increased and essential amino acids decreased by both perturbations. Over-represented proteins in the perturbed treatments included catabolic enzymes with roles in amino acid degradation and glycolysis, various cuticular proteins, and a C-type lectin and regucalcin with candidate defensive roles. This analysis demonstrates the central role of essential amino acid production in the relationship and identifies candidate proteins and processes underpinning the function and persistence of the association.

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“…(b) Budget analysis EAA production by Buchnera was estimated by budget analysis, as used previously [3,6,16]. Protein growth of aphids on diets individually lacking each EAA was calculated over 2-7 days of larval development from the weight and protein density (mg protein g 21 weight) of the aphids and the increase in each EAA determined from the %EAA content of aphid protein (electronic supplementary material, Methods, tables S1 and S2).…”

Section: Materials and Methods (A) Experimental Materialsmentioning

confidence: 99%

Matching the supply of bacterial nutrients to the nutritional demand of the animal host

et al. 2014

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Various animals derive nutrients from symbiotic microorganisms with muchreduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium Buchnera aphidicola in the pea aphid Acyrthosiphon pisum is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that Buchnera scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing Buchnera) revealed that these metabolic changes are not accompanied by significant change in Buchnera or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated Buchnera increased with increasing cystathionine concentration. We propose that Buchnera metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.

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A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola

Cited by 95 publications

References 24 publications

A systems biology approach to studying the role of microbes in human health

A systems biology approach to studying the role of microbes in human health

Integrated Metabonomic−Proteomic Analysis of an Insect−Bacterial Symbiotic System

Matching the supply of bacterial nutrients to the nutritional demand of the animal host

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