Symbiont-assisted cuticle biosynthesis as a key innovation contributing to the evolutionary success of beetles

Informations projet

SYMBeetle

N° de convention de subvention: 819585

DOI

10.3030/819585

Projet clôturé

Date de signature de la CE 6 Février 2019

Date de début 1 Juin 2019

Date de fin 31 Mai 2024

Financé au titre de

• EXCELLENT SCIENCE - European Research Council (ERC)

Coût total

€ 1 997 750,00

Contribution de l’UE

€ 1 997 750,00

Coordonné par

MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN EV
Germany

Periodic Reporting for period 5 - SYMBeetle (Symbiont-assisted cuticle biosynthesis as a key innovation contributing to the evolutionary success of beetles)

Période du rapport: 2024-02-01 au 2024-05-31

Résumé du contexte et des objectifs généraux du projet

To elucidate the key adaptations underlying evolutionary success remains one of the central challenges in evolution and ecology. However, rigorous experimental tests are usually hampered by the lack of replicate evolutionary events or the inability to manipulate a candidate trait of importance. SYMBeetle exploits the naturally replicated evolution of an experimentally tractable, symbiont-assisted key adaptation in beetles to understand its impact on niche expansion and diversification. Recent evidence indicates that beetles across at least seven different families associate with microbial symbionts that provision their host with tyrosine, an aromatic amino acid necessary for cuticle biosynthesis, hardening, and tanning. SYMBeetle addresses the hypothesis that the acquisition of tyrosine-supplementing microbes constituted a key innovation across phylogenetically distinct beetles that allowed them to expand into novel ecological niches, by relaxing the dependence on nitrogen-rich diets for successful formation of the rigid exoskeleton and protective front wings. Specifically, tyrosine supplementation may facilitate the transition to herbivory and allow for subsisting at very low ambient humidity, by facilitating the production of a thick cuticular barrier to desiccation. To test this, SYMBeetle will uniquely combine experimental manipulation of symbiotic associations to assess the symbionts’ contribution to cuticle biosynthesis and its fitness consequences (desiccation resistance and defense) with large-scale comparative approaches aimed at elucidating the taxonomic distribution, ecological contexts, and evolutionary origins of cuticle-supplementing symbioses. The results are expected to transform our understanding of microbes as important facilitators for the evolution of herbivory and the colonization of dry habitats in beetles, two factors of major relevance for the emergence of economically relevant insect pests of agricultural crops and stored products.

Travail effectué depuis le début du projet jusqu’à la fin de la période considérée dans le rapport et principaux résultats atteints jusqu’à présent

Microbial symbionts are widespread in insects and play important roles for their ecological and evolutionary success. Within the SYMBeetle project, we investigated the importance and regulation of symbioses between beetles and bacteria that provision tyrosine or its precursors to their host. We discovered that such symbioses are very widespread, particularly in beetles, occurring across at least seven different beetle families. Molecular and phylogenetic analyses of beetles across these families reveal that taxonomically distinct bacterial symbionts have converged on similar genomic composition that is streamlined for tyrosine precursor biosynthesis. Additionally, we uncovered multiple cases of symbiont losses and replacement events, dual co-obligate symbioses, as well as one case of symbiont lineage splitting that expand our view on the evolutionary dynamics of symbiotic associations. The reason for the widespread distribution of tyrosine-supplementing symbioses in beetles is that tyrosine is not only important for protein biosynthesis, but also constitutes a key metabolite for the hardening and tanning of the cuticle, which is especially strong in beetles. As such, beetles have a high demand in tyrosine, and particularly herbivorous taxa often rely on bacterial symbionts to meet this demand. In the absence of their symbionts, the beetles build up a thinner and lighter cuticle, which renders them more vulnerable to desiccation, predation, and pathogen attack. On the downside, the association with tyrosine-supplementing microbes makes the beetles susceptible to the herbicide glyphosate, which targets the shikimate pathway that is confined to plants and microbes and underlies the biosynthesis of aromatic amino acids, including tyrosine. This is concerning, as phylogenetic analyses indicate that the shikimate pathways of many nutritional endosymbionts contain a glyphosate-sensitive enzyme. Our findings highlight the importance of symbiont-mediated tyrosine supplementation for cuticle biosynthesis in beetles, but also paint an alarming scenario regarding the use of glyphosate in light of recent declines in insect populations.

Progrès au-delà de l’état des connaissances et impact potentiel prévu (y compris l’impact socio-économique et les conséquences sociétales plus larges du projet jusqu’à présent)

Wierz, J.C. Dirksen, P., Kirsch, R., Krüsemer, R., Weiss, B., Pauchet, Y., Engl, T., Kaltenpoth, M. (2024) Intracellular symbiont Symbiodolus is vertically transmitted and widespread across insect orders. ISME J.
While characterizing the microbial communities across several different beetle families, we discovered a novel intracellular symbiont that is widespread across at least six different insect orders and appears to be especially common in beetles (Wierz et al. 2024b). The symbiont shows high prevalence in beetle populations and infects multiple host tissues including the ovaries as well as eggs, indicating vertical transmission. Genomic analyses reveal that the symbiont has the potential to be pathogenic, but it may also provide nutritional supplements to the host. This newly described symbiont that we called “Symbiodolus” may provide excellent opportunities to study the molecular underpinnings of the transition from pathogenicity to mutualism.

Kiefer, J.S.T. Batsukh, S., Bauer, E., Hirota, B., Weiss, B., Wierz, J., Fukatsu, T., Kaltenpoth, M., Engl, T. (2021) Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis. Communications Biology 4:554.
This study provides the first evidence that oral exposure to glyphosate can impact a bacteriome-localized symbiont of an insect, with detrimental effects on host fitness. As such, it reveals that xenobiotics can systemically penetrate an insects’ body and cause undesired side effects. Thus, if substantiated under ecologically relevant conditions, xenobiotics such as pesticides and herbicides may contribute to the currently observed decline in insect populations in nature.

Reis, F., Kirsch, R., Pauchet, Y., Bauer, E., Bilz, L.C. Fukomori, K., Fukatsu, T., Kölsch, G., Kaltenpoth, M. (2020) Bacterial symbionts support larval sap feeding and adult folivory in (semi-)aquatic reed beetles. Nature Communications 11: 2964.
In this study, we reconstructed the evolutionary history of the symbiosis in reed beetles (Chrysomelidae, Donaciinae) and uncovered two life-stage specific benefits provided by the symbionts, based on genomic data: While the larvae profit from the symbionts’ production of essential amino acids, the adults gain access to the carbon- and energy-rich plant cell wall components by the symbionts’ pectinases (Reis et al. 2020). In addition, phylogenetic analyses reveal that the symbiosis initially expanded the hosts’ ecological niche space, but later restricted its evolutionary potential, providing a rare example demonstrating the potential of symbionts to both broaden and confine a host’s ecological opportunities.

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