Large-Scale Label-Free Quantitative Proteomics of the Pea aphid-Buchnera Symbiosis

Poliakov, Anton; Russell, Calum W.; Ponnala, Lalit; Hoops, Harold J.; Sun, Qi; Douglas, Angela E.; Wijk, Klaas J. van

doi:10.1074/mcp.m110.007039

Cited by 131 publications

(181 citation statements)

References 79 publications

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“…In aphids, cells that are specified to become bacteriocytes show distinctive gene expression in early developmental stages, and their cellular fate is determined before Buchnera colonization (31,32). Bacteriocyte expression of genes underlying amino acid metabolism complements Buchnera pathways for amino acid biosynthesis, reflecting extensive host-symbiont collaboration in this central nutritional function (33)(34)(35). Certain aphid genes seem to function solely in controlling or supporting Buchnera.…”

Section: Evolutionary Hazards Of Symbiosismentioning

confidence: 99%

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

429

515

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Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sapfeeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphidBuchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.Buchnera | aphid | Muller's ratchet | selection levels | coevolution

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Section: Evolutionary Hazards Of Symbiosismentioning

confidence: 99%

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

429

515

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“…However, our finding that methionine levels are elevated in bacteriocytes from aphids reared on methionine-free diet (figure 3b) is not readily compatible with host-mediated alleviation of feedback inhibition. A further indication that metabolic removal of EAAs in aphid bacteriocytes is not central to the regulation of EAA production comes from the evidence that the protein synthesis machinery is not enriched in bacteriocytes [13,18,31], although certain aphid amino acid transporters in bacteriocytes may mediate efficient EAA export from the bacteriocyte [32].…”

Section: Discussionmentioning

confidence: 99%

“…This clone bore B. aphidicola and no secondary symbionts, as determined by diagnostic PCR assays and microscopy [12,13]. Routine cultures were maintained on pre-flowering Vicia faba cv.…”

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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“…Metabolic models based on the presence and absence of amino acid biosynthesis genes in A. pisum and Buchnera, as well as amino acid uptake and labeling experiments, show that precursors for the biosynthesis of essential amino acids are transported from the aphid host to the bacterial endosymbionts (Brinza et al, 2010;Hansen and Moran, 2011;Poliakov et al, 2011;Russell et al, 2014;Sasaki and Ishikawa, 1995;Shigenobu et al, 2000;Wilson et al, 2010). Four amino acids, aspartic acid, asparagine, glutamic acid and glutamine, not only provide the majority of the nitrogen flow into the Buchnera endosymbionts for the synthesis of essential amino acids but also constitute the majority of the phloem amino acids in most plant species, including in V. faba, a natural host for A. pisum (Gündüz and Douglas, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Sequencing of the pea aphid (Acyrthosiphon pisum) and Buchnera genomes, gene expression profiling, and proteomic studies have provided new insight into the predicted pathways of amino acid biosynthesis in the A. pisum-Buchnera symbiosis (Brinza et al, 2010;Hansen and Moran, 2011;Poliakov et al, 2011;Richards et al, 2010;Shigenobu et al, 2000). Notably, there are several examples of shared biosynthesis pathways for essential amino acids that are partly encoded by the endosymbiont bacteria and partly by the aphid host (Russell et al, 2013;Wilson et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Stable isotope studies reveal pathways for the incorporation of non-essential amino acids in Acyrthosiphon pisum (pea aphids)

Haribal

Jander

2015

Journal of Experimental Biology

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Plant roots incorporate inorganic nitrogen into the amino acids glutamine, glutamic acid, asparagine and aspartic acid, which together serve as the primary metabolites of nitrogen transport to other tissues. Given the preponderance of these four amino acids, phloem sap is a nutritionally unbalanced diet for phloem-feeding insects. Therefore, aphids and other phloem feeders typically rely on microbial symbionts for the synthesis of essential amino acids. To investigate the metabolism of the four main transport amino acids by the pea aphid (Acyrthosiphon pisum), and its Buchnera aphidicola endosymbionts, aphids were fed defined diets with stable isotope-labeled glutamine, glutamic acid, asparagine or aspartic acid (U-13C, U-15N; U-15N; α-15N; or γ-15N). The metabolic fate of the dietary 15N and 13C was traced using gas chromatography–mass spectrometry (GC-MS). Nitrogen was the major contributor to the observed amino acid isotopomers with one additional unit mass (M+1). However, there was differential incorporation, with the amine nitrogen of asparagine being incorporated into other amino acids more efficiently than the amide nitrogen. Higher isotopomers (M+2, M+3 and M+4) indicated the incorporation of varying numbers of 13C atoms into essential amino acids. GC-MS assays also showed that, even with an excess of dietary labeled glutamine, glutamic acid, asparagine or aspartic acid, the overall content of these amino acids in aphid bodies was mostly the product of catabolism of dietary amino acids and subsequent re-synthesis within the aphids. Thus, these predominant dietary amino acids are not passed directly to Buchnera endosymbionts for synthesis of essential amino acids, but are rather are produced de novo, most likely by endogenous aphid enzymes.

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Large-Scale Label-Free Quantitative Proteomics of the Pea aphid-Buchnera Symbiosis

Cited by 131 publications

References 79 publications

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

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

Stable isotope studies reveal pathways for the incorporation of non-essential amino acids in Acyrthosiphon pisum (pea aphids)

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