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Rol of obligate bacterial symbiosis in the diversification of a globally distributed aphid genus

Periodic Reporting for period 2 - MicroPhan (Rol of obligate bacterial symbiosis in the diversification of a globally distributed aphid genus)

Okres sprawozdawczy: 2019-06-15 do 2020-06-14

General context
Symbioses with microbial partners have facilitated the diversification of many eukaryotes. Many insect groups have made use of the metabolic capabilities of bacteria to colonize nutrient poor environments that would otherwise be unavailable to them These bacterial symbionts are generally sheltered within insect specialized cells and transmitted from mother to offspring. Hence nutritional obligate endosymbionts can be seen as “key adaptations’ which acquisitions have spurred the diversification of insects. Nutritional endosymbioses are prominent among sap feeders (e.g. aphids, cicadas, whiteflies…) and blood feeders (e.g. lice, bedbugs..). However these obligate mutualisms have their downsides. The maternal transfer of endosymbionts causes severe bottlenecks in bacterial populations, propelling the endosymbiont genome into a process of erosion. This can reduce the metabolic capability of bacteria, ultimately increasing their insect host extinction risks. One possible outcome of this situation is the acquisition of a new symbiont . An increasing body of evidence shows that, in many insect species, a new bacterial symbiont co-exists with the primary one, taking on a subset of the functions that the eroded symbiont cannot fulfill anymore. One particularity of these bacterial partnerships is that they are extremely dynamic: the newly arrived symbiont is often replaced during the diversification of the insect hosts. This project attempts to understand the dynamic of these endosymbiotic systems. Why are these new symbiont repeatedly replaced ? Do shifts in symbiotic associations lead to ecological shifts in the insect hosts? What are the potentially negative ramifications of obligate, heritable symbioses ? Can they overcome the initial benefits of the associations?

New data from large metagenomics studies are fundamentally altering our understanding of animal biology. Recent syntheses underline that bacterial associations can facilitate the evolution of animals and that these also have profound effect on genome evolution of symbionts and eukaryotic associates. We have no doubt that this project will make significant advances on these fundamental topics.
From an applied perspective, understanding the role of endosymbiosis in insect host-plant adaptation and climatic tolerance could be crucial for predicting their resilience to environmental changes and ultimately guide strategies for the control of agricultural pests.

The overall objective of the project is to understand the role of endosymbiotic bacteria in the long-term evolution of a globally-distributed insect clade.
Work Package 1: Rates and patterns of molecular evolution of bacterial symbionts (outgoing phase: Udem, Montreal Canada)
We conducted phylogenomic analyses on Buchnera (the primary symbiont of aphids) and Serratia symbiotica (one of the lineages that complements Buchnera in the Cinara genus) and inferred codiversification scenarios using reconciliation analyses. These analyses show that Serratia has been acquired and lost several times during the diversification of Cinara. Fossil calibrations of both the phylogenies of Serratia and Buchnerashow that both bacterial lineages have very similar substitution rates. These results suggest that they experience similar demographic events. Our results also show that the genome shrinkage experienced by Serratia symbiotica upon its integration as an obligate symbiont is very fast.
Similar analyses were conducted on the association between Erwinia and Buchnera aphidicola in specific clade of Cinara. These confirmed that Erwinia has cospeciated with its aphid hosts in this clade and experienced very similar substitution rates to Buchnera.

In order to investigate the process of genome shrinkage at a finer evolutionary scale, we also investigated intraspecifc variations in the endosymbiont genomes of two study systems: the association between Cinara strobi and its two endosymbionts (Buchnera and Serratia) and the association between Cinara pseudotaxifoliae and its two symbionts (Buchnera and Erwinia). In both systems, coding regions evolve at very similar rates in both Buchnera and its obligate associates, with few non synonymous substitutions which confirms that these genomes are under purifying selection. Deletions occur in non-coding regions (pseudogenes and intergenic regions) in both Serratia and Erwinia. In Serratia small deletions occur through replication slippage in homopolymers. In Erwinia, deletions occur mostly in more complex microsatellite repeat motifs. These results give an overview of the process of genomic erosion at a recent evolutionary scale.

Work package 2 : Role of bacterial associations in aphid evolutionary transitions
The annotation of Erwinia genomes showed that these bacteria carry a new metabolic function: Erwinia can synthetize Thiamin, while this B vitamin cannot be synthetized by any known Buchnera or the Serratia that are known to complement Buchnera in other aphids. The aphids hosting this symbiont are the only ones that feed on Larix and Pseudotsuga, this suggest that Erwinia acquisition could have played a key role in the colonisation of these conifer genera.
On the other hand, the ongoing annotation of Serratia genomes associated with Cinara, suggests that all Serratia (old and more recently acquired) fill the same metabolic functions, complementing Buchnera. The acquisition of a new serratia seems to be neutral for the aphids.

Through phylogenetic analyses of 16 phage genomes (APSE associated with Hamiltonella), we show that recombination has occurred repeatedly among phage. AWealso found acquisition of new genes in the toxin cassette. These variations are probably associated with the variable protective phenotypes these phages confer to their insect hosts.
This study provides a comparative analysis of the genomic changes that bacterial lineages undergo upon their integration as obligate nutritional symbionts in several independently acquired symbionts.

Its results allow us to draw some general trends for the evolution of di-symbiotic systems in aphids.
Our comparative analyses demonstrate that the process of genomic erosion is always very rapid and confirms that it occurs through the loss of the DNA repair systems in both Buchnera and the newly aqcuired endosymbionts (Serratia and Erwinia)
Our results further show, unlike previous analyses of di-symbiotic systems in aphids and other sap-feeders, that new symbionts in the Erwinia lineage can potentially carry new nutritional functions which hints towards a scenario in which multipartner endosymbioses actually play a role in the ecological expansion of the hosts.
Our analyses further demonstrate that horizontal gene transfers between co-occuring symbionts have played a key role in the event leading to the establishment of these partnerships and the succesion of symbionts throughout the diversification of the insect hosts.

We expect that further exploration of the intricacies of the di-symbiotic systems of aphids will continue to provide important clues into the emergence and maintenance of these multi-partner endosymbioses and the process of genome shrinkage in endosymbionts.
Schematic picture of symbiont replacements in aphids