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

Monnin, David; Jackson, Raphaella; Kiers, E. Toby; Bunker, Marie; Ellers, Jacintha; Henry, Lee M.

doi:10.1016/j.cub.2020.03.011

Cited by 67 publications

(112 citation statements)

References 71 publications

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“…Because of its strict vertical transmission, Buchnera has undergone long-term coevolution with its aphid hosts [5]. However, due to the metabolic losses caused by rapid genome deterioration in Buchnera [6], some aphid species of the subfamilies Lachninae, Chaitophorinae, and Aphidinae have established co-obligate associations with other symbiotic partners [7,8].…”

Section: Introductionmentioning

confidence: 99%

Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

Jiang

Qiao

et al. 2020

Microb Ecol

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Aphids are known to be associated with a variety of symbiotic bacteria. To improve our knowledge of the bacterial diversity of polyphagous aphids, in the present study, we investigated the microbiota of the cosmopolitan agricultural pest Myzus persicae (Sulzer). Ninety-two aphid samples collected from different host plants in various regions of China were examined using high-throughput amplicon sequencing. We comprehensively characterized the symbiont diversity of M. persicae and assessed the variations in aphid-associated symbiont communities. We detected a higher diversity of symbionts than has been previously observed. M. persicae hosted the primary endosymbiont Buchnera aphidicola and seven secondary symbionts, among which Wolbachia was the most prevalent and Rickettsia, Arsenophonus, and Spiroplasma were reported for the first time. Ordination analyses and statistical tests revealed that the symbiont flora associated with M. persicae did not change with respect to host plant or geography, which may be due to frequent migrations between different aphid populations. These findings will advance our knowledge of the microbiota of polyphagous insects and will enrich our understanding of assembly of host-microbiome systems.

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Section: Introductionmentioning

confidence: 99%

Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

Jiang

Qiao

et al. 2020

Microb Ecol

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“…Growing evidence suggested that Serratia has evolved into a co-obligate symbiont with Buchnera. As an integrated unit, they function collectively in many aphid species, such as the Periphyllus genus, to synthesize and express essential nutrients-provisioning genes that are lost in Buchnera [ 45 ]. Co-obligate symbionts are located within the same bacteriome, and removal of Serratia had the most dramatic effect on aphid survival and reproduction.…”

Section: Discussionmentioning

confidence: 99%

Serratia symbiotica Enhances Fatty Acid Metabolism of Pea Aphid to Promote Host Development

Zhou

Ling

Guo

et al. 2021

IJMS

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Bacterial symbionts associated with insects are often involved in host development and ecological adaptation. Serratia symbiotica, a common facultative endosymbiont harbored in pea aphids, improves host fitness and heat tolerance, but studies concerning the nutritional metabolism and impact on the aphid host associated with carrying Serratia are limited. In the current study, we showed that Serratia-infected aphids had a shorter nymphal developmental time and higher body weight than Serratia-free aphids when fed on detached leaves. Genes connecting to fatty acid biosynthesis and elongation were up-regulated in Serratia-infected aphids. Specifically, elevated expression of fatty acid synthase 1 (FASN1) and diacylglycerol-o-acyltransferase 2 (DGAT2) could result in accumulation of myristic acid, palmitic acid, linoleic acid, and arachidic acid in fat bodies. Impairing fatty acid synthesis in Serratia-infected pea aphids either by a pharmacological inhibitor or through silencing FASN1 and DGAT2 expression prolonged the nymphal growth period and decreased the aphid body weight. Conversely, supplementation of myristic acid (C14:0) to these aphids restored their normal development and weight gain. Our results indicated that Serratia promoted development and growth of its aphid host through enhancing fatty acid biosynthesis. Our discovery has shed more light on nutritional effects underlying the symbiosis between aphids and facultative endosymbionts.

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“…It is now established that intracellular host-dependent symbionts of insects can evolve from originally free-living bacterial lineages (Husník et al 2011;Clayton et al 2012;Manzano-Marıń et al 2020). Genetic analyses indicate that these intimate relationships between insects and bacteria can evolve in a very dynamic fashion involving the recruitment of new bacterial partners and the repeated replacement of pre-existing intracellular symbionts (Koga and Moran 2014;Husnik and McCutcheon 2016;Meseguer et al 2017;Monnin et al 2020;Mao and Bennett 2020). Symbiont switching is an important evolutionary mechanism, which is not limited to insects (e.g., in reef organisms such as corals and sponges) (Webster and Reusch 2017), and by which maladaptive symbionts are replaced by new functional ones (Sudakaran et al 2017).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to this, a growing number of studies have recently shown that symbiotic associations between insects and bacteria evolve in a very dynamic fashion, involving the acquisition of new symbionts, and/or the loss and replacement of established bacterial partners, even in the context of obligate associations established sometimes for millions of years (Koga and Moran 2014;Hosokawa et al 2016;Husnik and McCutcheon 2016;Manzano-Marín et al 2017;Sudakaran et al 2017;Chong and Moran 2018;Matsuura et al 2018;Mao and Bennett 2020). For example, genomic analyses in aphids indicate that the dependence of some species on co-obligate symbiotic bacteria has arisen independently many times during their evolutionary history , 2017Meseguer et al 2017;Manzano-Marıń et al 2020;Monnin et al 2020). The repeated replacement of pre-existing symbionts by other microbial partners is now considered a redundant evolutionary process that occurs in many insect species, suggesting 1) the continuous formation of new mutualistic associations in nature, and 2) the existence of a pool of environmental symbionts from which new intimate, facultative, or obligate associations are formed in nature.…”

Section: Introductionmentioning

confidence: 99%

Ubiquity of the SymbiontSerratia symbioticain the Aphid Natural Environment: Distribution, Diversity and Evolution at a Multitrophic Level

Pons

Scieur

Dhondt

et al. 2021

Preprint

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Bacterial symbioses are significant drivers of insect evolutionary ecology. However, despite recent findings that these associations can emerge from environmentally derived bacterial precursors, there is still little information on how these potential progenitors of insect symbionts circulates in the trophic systems. The aphid symbiont Serratia symbiotica represents a valuable model for deciphering evolutionary scenarios of bacterial acquisition by insects, as its diversity includes intracellular host-dependent strains as well as gut-associated strains that have retained some ability to live independently of their hosts and circulate in plant phloem sap. These strains represent a potential reservoir for the emergence of new and more intimate symbioses. Here, we conducted a field study to examine the distribution and diversity of S. symbiotica found in aphid populations, as well as in different compartments of their surrounding environment. A total of 250 aphid colonies, 203 associated insects, and 161 plant samples associated with aphid colonies were screened for S. symbiotica. Twenty percent of aphids were infected with S. symbiotica, and the symbiont includes a wide diversity of strains with varied tissue tropism corresponding to different lifestyle. We also showed that the prevalence of S. symbiotica is influenced by seasonal temperatures. For the first time, we found that S. symbiotica was present in non aphid species and in host plants, and that the prevalence of the bacterium in these samples was higher when associated aphid colonies were infected. Furthermore, phylogenetic analyses suggest the existence of horizontal transfers between the different trophic levels examined. These results provide a completely new picture of the ubiquity of an insect symbiont in nature. They suggest that ecological interactions promote the dissemination of strains that are still free-living and poorly specialized, and for which plants are a proabable reservoir for the acquisition of new bacterial partners in insects.

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

Cited by 67 publications

References 71 publications

Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

Diversity of bacterial symbionts associated with Myzus persicae (Sulzer) (Hemiptera: Aphididae: Aphidinae) revealed by 16S rRNA Illumina sequencing

Serratia symbiotica Enhances Fatty Acid Metabolism of Pea Aphid to Promote Host Development

Ubiquity of the SymbiontSerratia symbioticain the Aphid Natural Environment: Distribution, Diversity and Evolution at a Multitrophic Level

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