Evolutionary loss and replacement of <i>Buchnera</i>, the obligate endosymbiont of aphids

Chong, Rebecca A.; Moran, Nancy A.

doi:10.1038/s41396-017-0024-6

Cited by 77 publications

(72 citation statements)

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“…The history of the symbiosis between aphids and their primary symbiont B. aphidicola is well known, with a 160–280 million years old association [ 74 ]. Although B. aphidicola can be experimentally transferred between aphid matrilines and has been lost in a few aphid taxa [ 75 ], it is considered as a strictly maternally inherited symbiont, and no horizontal transfer has been observed so far at different phylogenetic scales [ 63 , 76 , 77 ]. For A. pisum , we observed in the present work a close congruence between mitochondrial and B. aphidicola phylogenies, indicating a persisting association between the host and its primary symbionts, and a codiversification of both partners in recent evolutionary time.…”

Section: Discussionmentioning

confidence: 99%

Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches

et al. 2018

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BackgroundMost metazoans are involved in durable relationships with microbes which can take several forms, from mutualism to parasitism. The advances of NGS technologies and bioinformatics tools have opened opportunities to shed light on the diversity of microbial communities and to give some insights into the functions they perform in a broad array of hosts. The pea aphid is a model system for the study of insect-bacteria symbiosis. It is organized in a complex of biotypes, each adapted to specific host plants. It harbors both an obligatory symbiont supplying key nutrients and several facultative symbionts bringing additional functions to the host, such as protection against biotic and abiotic stresses. However, little is known on how the symbiont genomic diversity is structured at different scales: across host biotypes, among individuals of the same biotype, or within individual aphids, which limits our understanding on how these multi-partner symbioses evolve and interact.ResultsWe present a framework well adapted to the study of genomic diversity and evolutionary dynamics of the pea aphid holobiont from metagenomic read sets, based on mapping to reference genomes and whole genome variant calling. Our results revealed that the pea aphid microbiota is dominated by a few heritable bacterial symbionts reported in earlier works, with no discovery of new microbial associates. However, we detected a large and heterogeneous genotypic diversity associated with the different symbionts of the pea aphid. Partitioning analysis showed that this fine resolution diversity is distributed across the three considered scales. Phylogenetic analyses highlighted frequent horizontal transfers of facultative symbionts between host lineages, indicative of flexible associations between the pea aphid and its microbiota. However, the evolutionary dynamics of symbiotic associations strongly varied depending on the symbiont, reflecting different histories and possible constraints. In addition, at the intra-host scale, we showed that different symbiont strains may coexist inside the same aphid host.ConclusionsWe present a methodological framework for the detailed analysis of NGS data from microbial communities of moderate complexity and gave major insights into the extent of diversity in pea aphid-symbiont associations and the range of evolutionary trajectories they could take.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0562-9) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches

et al. 2018

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“…When a symbiont replacement occurs, it is expected that the new symbiont will replace the symbiotic functions of the former one. This is seen in different mono-and di-symbiotic systems observed in weevils 93 , aphids 41,94,95 , mealybugs 96,97 , and several Auchenorrhyncha 46,98,99 . As observed in all other currently sequenced Buchnera from Lachninae aphids, BCs is unable to provide two essential B vitamins: biotin (B7) and riboflavin (B2).…”

Section: Discussionmentioning

confidence: 99%

A Freeloader?: The Highly Eroded Yet large Genome of theSerratia symbioticasymbiont ofCinara strobi

Manzano-Marı́n

d’Acier

Clamens

et al. 2018

Preprint

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Genome reduction is pervasive among maternally-inherited bacterial endosymbionts. This genome reduction can eventually lead to serious deterioration of essential metabolic pathways, thus rendering an obligate endosymbiont unable to provide essential nutrients to its host. This loss of essential pathways can lead to either symbiont complementation (sharing of the nutrient production with a novel co-obligate symbiont) or symbiont replacement (complete takeover of nutrient production by the novel symbiont). However, the process by which these two evolutionary events happen remains somewhat enigmatic by the lack of examples of intermediate stages of this process. Cinara aphids (Hemiptera: Aphididae) typically harbour two obligate bacterial symbionts: Buchnera and Serratia symbiotica. However, the latter has been replaced by different bacterial taxa in specific lineages, and thus species within this aphid lineage could provide important clues into the process of symbiont replacement. In the present study, using 16S rRNA high-throughput amplicon sequencing, we determined that the aphid Cinara strobi harbours not two, but three fixed bacterial symbionts: Buchnera aphidicola, a Sodalis sp., and S. symbiotica. Through genome assembly and genome-based metabolic inference, we have found that only the first two symbionts (Buchnera and Sodalis) actually contribute to the hosts' supply of essential nutrients while S. symbiotica has become unable to contribute towards this task. We found that S. symbiotica has a rather large and highly eroded genome which codes only for a few proteins and displays extensive pseudogenisation. Thus, we propose an ongoing symbiont replacement within C. strobi, in which a once "competent" S. symbiotica does no longer contribute towards the beneficial association. These results suggest that in dual symbiotic systems, when a substitute co-symbiont is available, genome deterioration can precede genome reduction and a symbiont can be maintained despite the apparent lack of benefit to its host. Sodalis, and Hamiltonella).Most of our current knowledge from these co-obligate endosymbionts comes from S. symbiotica strains harboured by Lachninae aphids. These symbionts display very different genomic features, ranging from strains holding rather large genomes rich in mobile elements to small genomes rich in A+T and deprived of mobile elements 42 . The S. symbiotica strain held by the aphid Cinara tujafilina (hereafter SsCt), shares a considerable genomic similarity to a facultative strain harboured by the pea aphid Acyrthosiphon pisum (hereafter SsAp) 35 . This reflects the early stage of genome reduction SsCt is at, which is characterised by a moderately reduced and highly rearranged genome (when compared to free-living relatives), an enrichment of mobile elements (hereafter MEs), and a large-scale pseudogenisation 35,[43][44][45][46][47] . On the other side, the co-obligate S. symbiotica from Tuberolachnus salignus (hereafter SsTs) shows a very small and gene dense genome 36 , similarly to ancient obligate...

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“…aphidicola association. And, in a recent study, Chong and Moran (2018) have shown how the aphids from the Geopemphigus species have naturally replaced their B. aphidicola for a different symbiont closely related to the phylum Bacteroides. These types of species replacements can be tolerated without the holobiont losing its identity insofar as the functions that the microbiota realizes are the same, which strongly suggests that the adaptive traits that are arguably etiological adaptations of the holobiont still remain.…”

Section: The Inter-identity Of the Holobiontmentioning

confidence: 99%

What Is a Hologenomic Adaptation? Emergent Individuality and Inter-Identity in Multispecies Systems

Suárez

Triviño

2020

Front. Psychol.

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Contemporary biological research has suggested that some host-microbiome multispecies systems (referred to as "holobionts") can in certain circumstances evolve as unique biological individual, thus being a unit of selection in evolution. If this is so, then it is arguably the case that some biological adaptations have evolved at the level of the multispecies system, what we call hologenomic adaptations. However, no research has yet been devoted to investigating their nature, or how these adaptations can be distinguished from adaptations at the species-level (genomic adaptations). In this paper, we cover this gap by investigating the nature of hologenomic adaptations. By drawing on the case of the evolution of sanguivory diet in vampire bats, we argue that a trait constitutes a hologenomic adaptation when its evolution can only be explained if the holobiont is considered the biological individual that manifests this adaptation, while the bacterial taxa that bear the trait are only opportunistic beneficiaries of it. We then use the philosophical notions of emergence and inter-identity to explain the nature of this form of individuality and argue why it is special of holobionts. Overall, our paper illustrates how the use of philosophical concepts can illuminate scientific discussions, in the trend of what has recently been called metaphysics of biology.

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Evolutionary loss and replacement of Buchnera, the obligate endosymbiont of aphids

Cited by 77 publications

References 62 publications

Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches

Multi-scale characterization of symbiont diversity in the pea aphid complex through metagenomic approaches

A Freeloader?: The Highly Eroded Yet large Genome of theSerratia symbioticasymbiont ofCinara strobi

What Is a Hologenomic Adaptation? Emergent Individuality and Inter-Identity in Multispecies Systems

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