Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis

Douglas, Angela E.; Prosser, W.A.

doi:10.1016/0022-1910(92)90107-o

Cited by 220 publications

(160 citation statements)

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“…Particularly frequent in species thriving on nutritionally unbalanced environments, such endosymbioses are believed to impact several aspects of host biology, including physiology, immunity and reproduction [2][3][4][5][6][7][8]. They ensure a nutritional complementation of the host diet by providing vitamins and essential amino acids [3,7,9,10], thus greatly improving host fitness [2,3,7,11,12]. Early on during insect embryogenesis, endosymbionts are housed within specific host cells, the bacteriocytes, which group together to form the bacteriome organ in some insect species.…”

Section: Introductionmentioning

confidence: 99%

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

Masson¹,

Zaidman-Rémy²,

Heddi³

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Many insects sustain long-term relationships with intracellular symbiotic bacteria that provide them with essential nutrients. Such endosymbiotic relationships likely emerged from ancestral infections of the host by free-living bacteria, the genomes of which experience drastic gene losses and rearrangements during the host-symbiont coevolution. While it is well documented that endosymbiont genome shrinkage results in the loss of bacterial virulence genes, whether and how the host immune system evolves towards the tolerance and control of bacterial partners remains elusive. Remarkably, many insects rely on a 'compartmentalization strategy' that consists in secluding endosymbionts within specialized host cells, the bacteriocytes, thus preventing direct symbiont contact with the host systemic immune system. In this review, we compile recent advances in the understanding of the bacteriocyte immune and cellular regulators involved in endosymbiont maintenance and control. We focus on the cereal weevils Sitophilus spp., in which bacteriocytes form bacteriome organs that strikingly evolve in structure and number according to insect development and physiological needs. We discuss how weevils track endosymbiont dynamics through at least two mechanisms: (i) a bacteriome local antimicrobial peptide synthesis that regulates endosymbiont cell cytokinesis and helps to maintain a homeostatic state within bacteriocytes and (ii) some cellular processes such as apoptosis and autophagy which adjust endosymbiont load to the host developmental requirements, hence ensuring a fine-tuned integration of symbiosis costs and benefits.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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Section: Introductionmentioning

confidence: 99%

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

Masson¹,

Zaidman-Rémy²,

Heddi³

2016

Phil. Trans. R. Soc. B

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“…Conversely, these symbionts lack nonessential amino acid biosynthetic pathways; thus, the host must provide these amino acids to the symbiont (6). The best-studied model of this phenomenon is the symbiosis of the pea aphid, Acyrthosiphon pisum, and its bacterial endosymbiont, Buchnera aphidicola (4,(6)(7)(8).…”

mentioning

confidence: 99%

“…Genomic and physiological research reveals that Buchnera synthesizes essential amino acids for its host (6,7,(9)(10)(11)(12)). Buchnera's genome includes genes for almost all enzymes in the essential amino acid pathways and for enzymes in pathways for the nonessential amino acids tyrosine, glycine, and cysteine (6).…”

mentioning

confidence: 99%

Aphid genome expression reveals host–symbiont cooperation in the production of amino acids

Hansen

Moran

2011

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

365

478

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The evolution of intimate symbiosis requires the coordination of gene expression and content between the distinct partner genomes; this coordination allows the fusion of capabilities of each organism into a single integrated metabolism. In aphids, the 10 essential amino acids are scarce in the phloem sap diet and are supplied by the obligate bacterial endosymbiont ( Buchnera ), which lives inside specialized cells called bacteriocytes. Although Buchnera ’s genome encodes most genes for essential amino acid biosynthesis, several genes in essential amino acid pathways are missing, as are most genes for production of nonessential amino acids. Additionally, it is unresolved whether the supply of nitrogen for amino acid biosynthesis is supplemented by recycling of waste ammonia. We compared pea aphid gene expression between bacteriocytes and other body tissues using RNA sequencing and pathway analysis and exploiting the genome sequences available for both partners. We found that 26 genes underlying amino acid biosynthesis were up-regulated in bacteriocytes. Seven of these up-regulated genes fill the gaps of Buchnera ’s essential amino acid pathways. In addition, genes underlying five nonessential amino acid pathways lost from Buchnera are up-regulated in bacteriocytes. Finally, our results reveal that two genes, glutamine synthetase and glutamate synthase, which potentially work together in the incorporation of ammonium nitrogen into glutamate (GOGAT) cycle to assimilate ammonia into glutamate, are up-regulated in bacteriocytes. Thus, host gene expression and symbiont capabilities are closely integrated within bacteriocytes, which function as specialized organs of amino acid production. Furthermore, the GOGAT cycle may be a key source of nitrogen fueling the integrated amino acid metabolism of the aphid– Buchnera partnership.

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“…Aphids are plant sap suckers consuming a diet rich in carbohydrates but low in amino acids, and it is thought that Buchnera provides the aphid with these essential amino acids (3)(4)(5). Evidence has been presented indicating that the endosymbionts are able to reduce sulfate to sulfide and synthesize methionine, cysteine, and tryptophan (10,(15)(16)(17). Tryptophan synthase, the last enzyme in the tryptophan biosynthetic pathway, has been detected in the endosymbionts (17).…”

mentioning

confidence: 99%