Sulphate utilization in an aphid symbiosis

doi:10.1016/0020-1790(88)90012-1

Insect Biochemistry

Volume 18, Issue 6, 1988, Pages 599-605

https://doi.org/10.1016/0020-1790(88)90012-1 Get rights and content

Abstract

When two clones of Myzus persicae were maintained on a defined diet with inorganic sulphate as sole sulphur source, their growth and survival were inferior to that on diets containing the sulphur amino acid, methionine. This discrepancy is due, at least in part, to the phagostimulatory properties of methionine, which stimulated aphid feeding rate by 50–150%. Myzus persicae incorporated radioactivity from dietary [³⁵S]sulphate into protein and low molecular weight compounds, including cysteine and methionine. Two lines of evidence indicate that the mycetocyte-symbionts are responsible for the reductive assimilation of sulphate. (1) [³⁵S]sulphate incorporation is abolished by treatment of the aphids with the antibiotic chlortetracycline, which disrupts the symbionts; and (2) [³⁵S]sulphate is utilized by isolated embryos (which contain mycetocyte-symbionts but no gut flora) but not by isolated guts. Tracer studies suggest that 20% of dietary radiosulphur is translocated to the aphid tissues, and it is hypothesized that methionine may be the principal product released by the symbionts.

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Cited by (68)

Parallel Evolution in the Integration of a Co-obligate Aphid Symbiosis
2020, Current Biology
Citation Excerpt :
Our analysis centered on the pathways and genes involved in essential nutrient provisioning to the host (Data S1D). Specifically, we focused on pathways that have experimental evidence for being essential for the aphid: riboflavin [14] and essential amino acids [15–21]. Of particular interest was the riboflavin pathway in Buchnera, as the loss of this pathway has been hypothesized to trigger the dependence on Serratia in the Lachninae aphids [10].
Insects evolve dependence—often extreme—on microbes for nutrition. This includes cases in which insects harbor multiple endosymbionts that function collectively as a metabolic unit [1, 2, 3, 4, 5]. How do these dependences originate [6], and is there a predictable sequence of events leading to the integration of new symbionts? While co-obligate symbioses, in which hosts rely on multiple nutrient-provisioning symbionts, have evolved numerous times across sap-feeding insects, there is only one known case in aphids, involving Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily [7, 8, 9]. Here, we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. Comparing recent and ancient associations allow us to investigate intermediate stages of metabolic and anatomical integration of Serratia. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner—through parallel evolutionary processes. Specifically, we show how the repeated losses of the riboflavin and peptidoglycan pathways in Buchnera lead to dependence on Serratia. We then provide evidence of a stepwise process of symbiont integration, whereby dependence evolves first. Then, essential amino acid pathways are lost (at ∼30–60 mya), which coincides with the increased anatomical integration of the companion symbiont. Finally, we demonstrate that dependence can evolve ahead of specialized structures (e.g., bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesizing nutrients may provide a unified explanation for the sequence of gene losses that occur during the evolution of co-obligate symbiosis.
Insect gut microbiome and its applications
2020, Recent Advancements in Microbial Diversity
Microbes through its symbiotic relationship between the host and their invaded organisms, owes a major part in nature as well as the evolutionary processes. Insects are the most diversified fauna with stable surveillance in innumerable ecological niches. Many among those act as secondary symbionts as well. These symbiotic connotations originated more recently and can be ephemeral. In some cases, the direct contact with the host also is not needed in a population for these organisms to survive. Because when the primary symbionts transfer the genes directly from mother to progeny, the secondary symbionts do it through several means. This chapter reviews the association between insect gut microbiomes and their interactions with the environment. Recent insights and potential applications of the insect gut microbiome will provide a metagenomic thorough knowledge of the microbial census in the insect gut.
Aphids as major potato pests
2013, Insect Pests of Potato
Aphids as Major Potato Pests
2012, Insect Pests of Potato: Global Perspectives on Biology and Management
Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum
2009, Comptes Rendus - Biologies
Citation Excerpt :
Experimental studies using a combination of controlled artificial diets and antibiotic-treated aphids (aposymbiotic aphids), as well as genomic information, have focused on nitrogenous compounds that are not present in the phloem sap, and especially on essential amino acids. Douglas et al. have provided evidence for the synthesis of methionine by Buchnera in the aphid Myzus persicae [31], and that of tryptophan in BAp [32]. The involvement of Buchnera in the transfer of nitrogen from glutamine or glutamate has been demonstrated by Sasaki and Ishikawa [33].
Buchnera aphidicola is the primary obligate intracellular symbiont of most aphid species. B. aphidicola and aphids have been evolving in parallel since their association started, about 150 Myr ago. Both partners have lost their autonomy, and aphid diversification has been confined to smaller ecological niches by this co-evolution. B. aphidicola has undergone major genomic and biochemical changes as a result of adapting to intracellular life. Several genomes of B. aphidicola from different aphid species have been sequenced in the last decade, making it possible to carry out analyses and comparative studies using system-level in silico methods. This review attempts to provide a systemic description of the symbiotic function of aphid endosymbionts, particularly of B. aphidicola from the pea aphid Acyrthosiphon pisum, by analyzing their structural genomic properties, as well as their genetic and metabolic networks. To cite this article: L. Brinza et al., C. R. Biologies 332 (2009).
Buchnera aphidicola est la bactérie symbiotique intracellulaire obligatoire de la plupart des espèces de pucerons. Depuis leur association, il y a environ 150 Ma, B. aphidicola et le puceron ont évolué en parallèle. Les deux partenaires ont ainsi perdu leur autonomie et cette co-évolution a confiné les possibilités de diversification du puceron à des niches écologiques plus restreintes. Suite à son adaptation au mode de vie intracellulaire, B. aphidicola a connu d'importantes modifications génomiques et physiologiques. Plusieurs génomes de B. aphidicola provenant de différentes espèces de pucerons ont été publiés ces dix dernières années, permettant ainsi des analyses comparatives grâce à des approches systémiques in silico. Cet article propose une description systémique de la fonction symbiotique des endocytobiotes des pucerons, en se focalisant sur B. aphidicola issue du puceron du pois Acyrthosiphon pisum, et en analysant leurs propriétés génomiques ainsi que leurs réseaux génétique et métabolique. Pour citer cet article : L. Brinza et al., C. R. Biologies 332 (2009).
Host’s demand for essential amino acids is compensated by an extracellular bacterial symbiont in a hemipteran insect model
2022, Frontiers in Physiology

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^∗: Present address: Department of Zoology, University of Oxford, South Parks Road, Oxford, England.

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Insect Biochemistry

Abstract

References (33)

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye study

Analyt. Biochem.

Dietary amino acid requirements of the aphid Myzus persicae

J. Insect Physiol.

On the source of sterols for the green peach aphid, Myzus persicae, on holidic diets

J. Insect Physiol.

Host-symbiont interactions in the protein synthesis in the pea aphid Acyrthosiphon pisum

Insect Biochem.

DNA, RNA and protein synthesis in the isolated symbionts from the pea aphid, Acyrthosiphon pisum

Insect Biochem.

Effect of dietary amino acids on size and alary polymorphism of Aphis fabae

J. Insect Physiol.

Dietary amino acid requirements of the cotton aphid, Aphis gossypii: the sulphur-containing amino acids

J. Insect Physiol.

Phloem transport of sulfur in Ricinus

Planta

Endosymbiosis of Animals with Plant Microorganisms

Nutrition: organisms

Staining by neutral red and trypan blue in sequence for assaying vital and non-vital cultured cells

Stain Technol.

Aphids and translocation

Einfluss von Ernahrungsfaktoren auf die Entwicklung von Safte saugenden Insekten unter besonderer Beruchsichtung von Symbionten

Z. Parasitenkd.

Sulphur dioxide metabolism in soy-bean Glycine max var. Biloxi. II. Biochemical distribution of ³⁵SO₂ products

New Phytol.

Establishment of four strains of cells from insect tissues grown in vitro

Nature

Juvenile hormone stimulation of oocyte development and embryogenesis in the parthenogenetic ovaries of an aphid, Aphis fabae

Int. J. Invert. Reprod. Dev.

Cited by (68)

Parallel Evolution in the Integration of a Co-obligate Aphid Symbiosis

Insect gut microbiome and its applications

Aphids as major potato pests

Aphids as Major Potato Pests

Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum

Host’s demand for essential amino acids is compensated by an extracellular bacterial symbiont in a hemipteran insect model

Sulphate utilization in an aphid symbiosis

Abstract

Analyt. Biochem.

J. Insect Physiol.

J. Insect Physiol.

Insect Biochem.

Insect Biochem.

J. Insect Physiol.

J. Insect Physiol.

Phloem transport of sulfur in Ricinus

Planta

Endosymbiosis of Animals with Plant Microorganisms

Nutrition: organisms

Staining by neutral red and trypan blue in sequence for assaying vital and non-vital cultured cells

Stain Technol.

Aphids and translocation

Einfluss von Ernahrungsfaktoren auf die Entwicklung von Safte saugenden Insekten unter besonderer Beruchsichtung von Symbionten

Z. Parasitenkd.

Sulphur dioxide metabolism in soy-bean Glycine max var. Biloxi. II. Biochemical distribution of 35SO2 products

New Phytol.

Establishment of four strains of cells from insect tissues grown in vitro

Nature

Juvenile hormone stimulation of oocyte development and embryogenesis in the parthenogenetic ovaries of an aphid, Aphis fabae

Int. J. Invert. Reprod. Dev.

Sulphur dioxide metabolism in soy-bean Glycine max var. Biloxi. II. Biochemical distribution of ³⁵SO₂ products