Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera
01 Jan 1998-Annual Review of Entomology (Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303-0139, USA)-Vol. 43, Iss: 1, pp 17-37
TL;DR: It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
Abstract: Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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TL;DR: It is concluded that host plant quality affects the fecundity of herbivorous insects at both the individual and the population scale.
Abstract: Host plant quality is a key determinant of the fecundity of herbivorous insects. Components of host plant quality (such as carbon, nitrogen, and defensive metabolites) directly affect potential and achieved herbivore fecundity. The responses of insect herbivores to changes in host plant quality vary within and between feeding guilds. Host plant quality also affects insect reproductive strategies: Egg size and quality, the allocation of resources to eggs, and the choice of oviposition sites may all be influenced by plant quality, as may egg or embryo resorption on poor-quality hosts. Many insect herbivores change the quality of their host plants, affecting both inter- and intraspecific interactions. Higher-trophic level interactions, such as the performance of predators and parasitoids, may also be affected by host plant quality. We conclude that host plant quality affects the fecundity of herbivorous insects at both the individual and the population scale.
1,962 citations
TL;DR: Insect heritable symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
Abstract: Insect heritable symbionts have proven to be ubiquitous, based on molecular screening of various insect lineages. Recently, molecular and experimental approaches have yielded an immensely richer understanding of their diverse biological roles, resulting in a burgeoning research literature. Increasingly, commonalities and intermediates are being discovered between categories of symbionts once considered distinct: obligate mutualists that provision nutrients, facultative mutualists that provide protection against enemies or stress, and symbionts such as Wolbachia that manipulate reproductive systems. Among the most farreaching impacts of widespread heritable symbiosis is that it may promote speciation by increasing reproductive and ecological isolation of host populations, and it effectively provides a means for transfer of genetic information among host lineages. In addition, insect symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
1,438 citations
TL;DR: Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage.
Abstract: Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.
1,309 citations
TL;DR: The intestinal bacteria is discussed in the context of developing understanding of symbiotic relationships, of multitrophic interactions between insects and plant or animal host, and in developing new strategies for controlling insect pests.
Abstract: The diversity of the Insecta is reflected in the large and varied microbial communities inhabiting the gut Studies, particularly with termites and cockroaches, have focused on the nutritional contributions of gut bacteria in insects living on suboptimal diets The indigenous gut bacteria, however, also play a role in withstanding the colonization of the gut by non-indigenous species including pathogens Gut bacterial consortia adapt by the transfer of plasmids and transconjugation between bacterial strains, and some insect species provide ideal conditions for bacterial conjugation, which suggests that the gut is a "hot spot" for gene transfer Genomic analysis provides new avenues for the study of the gut microbial community and will reveal the molecular foundations of the relationships between the insect and its microbiome In this review the intestinal bacteria is discussed in the context of developing our understanding of symbiotic relationships, of multitrophic interactions between insects and plant or animal host, and in developing new strategies for controlling insect pests
1,283 citations
TL;DR: The results indicate that Buchnera is completely symbiotic and viable only in its limited niche, the bacteriocyte, and indicates complementarity and syntrophy between the host and the symbiont.
Abstract: Almost all aphid species (Homoptera, Insecta) have 60-80 huge cells called bacteriocytes, within which are round-shaped bacteria that are designated Buchnera. These bacteria are maternally transmitted to eggs and embryos through host generations, and the mutualism between the host and the bacteria is so obligate that neither can reproduce independently. Buchnera is a close relative of Escherichia coli, but it contains more than 100 genomic copies per cell, and its genome size is only a seventh of that of E. coli. Here we report the complete genome sequence of Buchnera sp. strain APS, which is composed of one 640,681-base-pair chromosome and two small plasmids. There are genes for the biosyntheses of amino acids essential for the hosts in the genome, but those for non-essential amino acids are missing, indicating complementarity and syntrophy between the host and the symbiont. In addition, Buchnera lacks genes for the biosynthesis of cell-surface components, including lipopolysaccharides and phospholipids, regulator genes and genes involved in defence of the cell. These results indicate that Buchnera is completely symbiotic and viable only in its limited niche, the bacteriocyte.
1,219 citations
References
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TL;DR: Rates calibrated using dates inferred from fossil aphids imply that Asian and American species of the aphid tribe Melaphidina diverged by the early Eocene; this result confirms an earlier hypothesis based on biogeographic evidence.
Abstract: The primary endosymbionts of aphids are maternally inherited bacteria that live only within specialized host cells. Phylogenetic analysis of the 16S ribosomal DNA sequences of aphid endosymbionts reveals that they are a monophyletic group with a phylogeny completely concordant with that of their hosts, implying long-term cospeciation. Here we show that rates of base substitution are similar in the 16.S ribosomal DNA of different endosymbiont lineages. In addition, we calibrate these rates by assigning age estimates for ancestral aphid hosts to the corresponding endosymbionts. The resulting rate estimates (1—2% per 50 Ma) are among the most reliable available for prokaryotes. They are very near values previously conjectured by using more tenuous assumptions for dating divergence events in eubacteria. Rates calibrated using dates inferred from fossil aphids imply that Asian and American species of the aphid tribe Melaphidina diverged by the early Eocene; this result confirms an earlier hypothesis based on biogeographic evidence. Based on these rate estimates, the minimum age of this endosymbiotic association and the age of aphids as a whole is estimated at 160-280 Ma.
553 citations
"Nutritional Interactions in Insect-..." refers background in this paper
...The ancestral Buchnerawas acquired once by aphids, subsequent to the divergence of the Phylloxeridae and Adelgidae, probably 160–280 million years ago (70)....
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TL;DR: An overview of the organization, regulation, and function of the nod genes and their participation in the determination of the host specificity is presented.
529 citations
TL;DR: Genetic and physiological studies indicate that Buchnera can synthesize methionine, cysteine, and tryptophan and supply these amino acids to the aphid host and involve plasmid-amplification of the gene coding for anthranilate synthase, the first enzyme of the tryptophile biosynthetic pathway.
Abstract: Evolutionary studies suggest that 200-250 million years ago an aphid ancestor was infected with a free-living eubacterium. The latter became established within aphid cells. Host and endosymbiont (genus Buchnera) became interdependent and unable to survive without each other. The growth of Buchnera became integrated with that of the aphids, which acquired the endosymbionts from their mothers before birth. Speciation of host lineages was paralleled by divergence of associated endosymbiont lineages, resulting in parallel evolution of Buchnera and aphids. Present day Buchnera retains many of the properties of its free-living ancestor, containing genes for proteins involved in DNA replication, transcription, and translation, as well as chaperonins and proteins involved in secretion, energy-yielding metabolism, and amino acid biosynthesis. Some of these processes are also observed in isolated endosymbiont cells. Genetic and physiological studies indicate that Buchnera can synthesize methionine, cysteine, and tryptophan and supply these amino acids to the aphid host. In the case of some fast-growing species of aphids, the overproduction of tryptophan by Buchnera involves plasmid-amplification of the gene coding for anthranilate synthase, the first enzyme of the tryptophan biosynthetic pathway. These recent studies provide a beginning in our understanding of Buchnera and its role in the endosymbiosis with aphids.
495 citations
"Nutritional Interactions in Insect-..." refers background in this paper
...the sequence responsible for allosteric inhibition of an enzyme) (10)....
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...67, 68, 94) and the molecular biology ofBuchnera(10)....
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TL;DR: Non‐pathogenic microorganisms, known as mycetocyte symbionts, are located in specialized ‘mycetocytes’ cells of many insects that feed on nutritionally unbalanced or poor diets.
Abstract: 1. Non-pathogenic microorganisms, known as mycetocyte symbionts, are located in specialized 'mycetocyte' cells of many insects that feed on nutritionally unbalanced or poor diets. The insects include cockroaches, Cimicidae and Lygaeidae (Heteroptera), the Homoptera, Anoplura, the Diptera Pupiparia, some formicine ants and many beetles. 2. Most mycetocyte symbionts are prokaryotes and a great diversity of forms has been described. None has been cultured in vitro and their taxonomic position is obscure. Yeasts have been reported in Cerambycidae and Anobiidae (Coleoptera) and a few planthoppers. They are culturable and those in anobiids have been assigned to the genus Torulopsis. 3. The mycetocyte cells may be associated with the gut, lie free in the abdominal haemocoel or be embedded in the fat body of the insect. The mycetocytes are large polyploid cells which rarely divide and the symbionts are restricted to their cytoplasm. 4. The mycetocyte symbionts are transmitted maternally from one insect generation to the next. In many beetles (Anobiidae, Cerambycidae, Chrysomelidae and cleonine Curculionidae), the microoganisms are smeared onto the eggs and consumed by the hatching larvae. In other insects, they are transferred from mycetocytes to oocytes in the ovary, a process known as transovarial transmission. The details of transmission in the different insect groups vary with the age of the mother (adult, larva or embryo) at which symbiont transfer to the ovary is initiated; whether isolated symbionts or intact mycetocytes are transferred; and the site of entry of symbionts to the egg (anterior, posterior or apolar). 5. Within an individual insect, the biomass of symbionts varies in a regular fashion with age, weight and sex of the insect. Suppression of symbiont growth rate and lysis of 'excess' microorganisms may contribute to the regulation of symbionts (including freshly-isolated preparations of unculturable forms) are used to investigate interactions between the partners. However, some methods to obtain aposymbiotic insects (e.g. antibiotics and lysozyme) deleteriously affect certain insects and aposymbionts may differ from the symbiont-containing stocks from which they were derived. 7. The mycetocyte symbionts have been proposed to synthesize various nutrients required by the insect. The symbionts of beetles and haematophagous insects may provide B vitamins and those in cockroaches and the Homoptera essential amino acids. The role of symbionts in the sterol nutrition of insects is equivocal. 8. Mycetocyte symbionts may have evolved from gut symbionts or guest microorganisms. The association is monophyletic in cockroaches but polyphyletic in many groups, including the sucking lice, beetles and scale insects.(ABSTRACT TRUNCATED AT 400 WORDS)
484 citations