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Interaction of Host Immune Systems with Endosymbionts in Glossina and Sitophilus Anna Zaidman-Rémy, Aurélien Vigneron, Brian Weiss, Abdelaziz Heddi

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Interaction of Host Immune Systems with Endosymbionts in Glossina and Sitophilus Anna Zaidman-Rémy, Aurélien Vigneron, Brian Weiss, Abdelaziz Heddi What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus Anna Zaidman-Rémy, Aurélien Vigneron, Brian Weiss, Abdelaziz Heddi To cite this version: Anna Zaidman-Rémy, Aurélien Vigneron, Brian Weiss, Abdelaziz Heddi. What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus. BMC Microbiology, BioMed Central, 2018, 18 (S1), 10.1186/s12866-018-1278-5. hal-02051649 HAL Id: hal-02051649 https://hal.archives-ouvertes.fr/hal-02051649 Submitted on 27 Feb 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Zaidman-Rémy et al. BMC Microbiology 2018, 18(Suppl 1):150 https://doi.org/10.1186/s12866-018-1278-5 REVIEW Open Access What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus Anna Zaidman-Rémy1*, Aurélien Vigneron2, Brian L Weiss2 and Abdelaziz Heddi1* Abstract The tsetse fly (Glossina genus) is the main vector of African trypanosomes, which are protozoan parasites that cause human and animal African trypanosomiases in Sub-Saharan Africa. In the frame of the IAEA/FAO program ‘Enhancing Vector Refractoriness to Trypanosome Infection’, in addition to the tsetse, the cereal weevil Sitophilus has been introduced as a comparative system with regards to immune interactions with endosymbionts. The cereal weevil is an agricultural pest that destroys a significant proportion of cereal stocks worldwide. Tsetse flies are associated with three symbiotic bacteria, the multifunctional obligate Wigglesworthia glossinidia, the facultative commensal Sodalis glossinidius and the parasitic Wolbachia. Cereal weevils house an obligatory nutritional symbiosis with the bacterium Sodalis pierantonius, and occasionally Wolbachia. Studying insect host-symbiont interactions is highly relevant both for understanding the evolution of symbiosis and for envisioning novel pest control strategies. In both insects, the long co-evolution between host and endosymbiont has led to a stringent integration of the host-bacteria partnership. These associations were facilitated by the development of specialized host traits, including symbiont-housing cells called bacteriocytes and specific immune features that enable both tolerance and control of the bacteria. In this review, we compare the tsetse and weevil model systems and compile the latest research findings regarding their biological and ecological similarities, how the immune system controls endosymbiont load and location, and how host-symbiont interactions impact developmental features including cuticle synthesis and immune system maturation. We focus mainly on the interactions between the obligate symbionts and their host’s immune systems, a central theme in both model systems. Finally, we highlight how parallel studies on cereal weevils and tsetse flies led to mutual discoveries and stimulated research on each model, creating a pivotal example of scientific improvement through comparison between relatively distant models. Keywords: Cereal weevil, Tsetse fly, Endosymbiosis, Immunity, Evolution, Insects, Homeostasis Background feeding-pea aphid Acyrthosiphon pisum’s association with Symbiosis is ubiquitous in nature and is a driving force in the primary endosymbiont Buchnera aphidicola [4]; the evolution. Among invertebrates, insects living on nutri- carpenter ant Camponotus floridanus/Blochmannia flori- tionally unbalanced habitats have evolved long-term asso- danus association [5]; cereal weevils Sitophilus sp.’s associ- ciations with intracellular mutualistic bacteria ation with Sodalis pierantonius [6]; the mealybug (endosymbionts) that complement their diet with meta- Planococcus citri, which associates with Tremblaya prin- bolic components, including amino acids and vitamins ceps and Moranella endobia [7], the cockroach Blattella [1–3]. Some well-studied examples in terms of germanica and its endosymbiont Blattabacterium cuenoti host-symbiont metabolic interactions are the phloem sap [8] and the blood-feeding tsetse fly (Diptera: Glossinidae)’s association with its obligatory, mutualistic symbiont Wig- * Correspondence: [email protected]; [email protected] glesworthia glossinidia [9]. 1Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, F-69621 Villeurbanne, France Full list of author information is available at the end of the article © International Atomic Energy Agency; licensee BioMed Central Ltd. 2018 This is an open access article distributed under the terms of the Creative Commons Attribution IGO License (https://creativecommons.org/licenses/by/3.0/igo/) which permits unrestricted use, distribution, and reproduction in any medium, provided appropriate credit to the original author(s) and the source is given. Zaidman-Rémy et al. BMC Microbiology 2018, 18(Suppl 1):150 Page 280 of 292 Insect nutritional endosymbiosis has been largely stud- by: i) ecological features: all natural populations of the ied with regards to bacterial genome evolution [10], host two insects house obligate symbionts [6, 20, 21, 28], and ecology [11], and metabolic complementation [12]. In ii) functional analyses: experimental depletion of obligate contrast, data on the molecular processes that orches- symbionts leads to sterility in tsetse flies [29–31] and to trate host immune system interactions with symbionts various biological anomalies in cereal weevils [6, 32–35]. remain scarce [13–18]. Deciphering these relationships This deep integration with their insect host’s physi- is of high interest so as to figure out whether and how ology is also remarkable at the cellular level, as both ob- host-symbiont coevolution has shaped the host immune ligate symbionts are housed within specialized host cells response in the context of a chronic bacterial infection named bacteriocytes, which group into an organ called [19]. Investigating the mechanisms insect hosts employ the bacteriome [6, 36] (Fig. 1). Interestingly, the strict to maintain endosymbiont homeostasis will facilitate the intracellular status of these symbionts was recently chal- identification of specific molecules that disrupt this rela- lenged in both insects with the recurrent presence of tionship, thus providing a translational foundation for extracellular W. glossinidia in the milk gland of female the development of novel control strategies that target tsetse [37, 38] and sporadic externalization of S. pieran- major insect pests and disease vectors. tonius at a time-restricted step during metamorphosis In the frame of the IAEA/FAO program ‘Enhancing [39], during which time the unique larval bacteriome is Vector Refractoriness to Trypanosome Infection’, which transitioning into multiple adult bacteriomes [35, 40]. focuses on the tsetse fly (Diptera: Glossinidae) and its W. glossinidia supplements its host’s diet mainly by interaction with endosymbionts and trypanosomes, the producing essential vitamins that are absent from verte- cereal weevil Sitophilus (Coleopteran: Dryophthoridae) brate blood [41–43]. This function infers that, during has been introduced as a comparative system to investi- their 50–80 million years of coevolution [44], tsetse has gate common and divergent immune regulations and developed a metabolic dependence upon W. glossinidia functions involved in symbiont control and distribution. [43]. Likewise, S. pierantonius provides its weevil host In this review, we highlight common and divergent traits with vitamins and cofactors. However, this bacterium ap- between these two phylogenetically distant insects within pears especially important as a source of amino acids, in the holometabolous group. We discuss how research on particular tyrosine and phenylalanine [35, 45–49]. These the weevil symbiotic association positively impacted distinct, symbiont-specific metabolic contributions, studies performed using the tsetse model system, and which are clearly deduced from their respective genome vice-versa. We focus mainly on the topic of the interac- sequences [22, 50], are likely related to the unique bio- tions between the obligate symbionts and their host’s logical traits of their insect hosts. Specifically, tsetse flies immune system, which is a central theme in both model employ a reproductive strategy called ‘adenotrophic systems. While cereal weevils house only one endosym- viviparity’. During this process the female retains one biont, Sodalis pierantonius [20–22], tsetse may harbor offspring within her uterus throughout its entire larval the commensal bacteria Sodalis glossinidius [23, 24] and development, and provides it with nourishment in the parasitic Wolbachia [25–27], in addition to obligate Wig- form of glandular milk secretions [51] (Fig. 1). Female glesworthia glossinidia [9]. The relevance of studying the tsetse require W. glossinidia-derived vitamins and interaction with the other symbiotic partners in tsetse is co-factors to sustain the energetically
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