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      What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus

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          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.

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          Most cited references107

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          Multiorganismal insects: diversity and function of resident microorganisms.

          All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.
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            Learning how to live together: genomic insights into prokaryote-animal symbioses.

            Our understanding of prokaryote-eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.
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              The tiniest tiny genomes.

              Starting in 2006, surprisingly tiny genomes have been discovered from numerous bacterial symbionts of insect hosts. Despite their size, each retains some genes that enable provisioning of limiting nutrients or other capabilities required by hosts. Genome sequence analyses show that genome reduction is an ongoing process, resulting in a continuum of sizes, with the smallest genome currently known at 112 kilobases. Genome reduction is typical in host-restricted symbionts and pathogens, but the tiniest genomes are restricted to symbionts required by hosts and restricted to specialized host cells, resulting from long coevolution with hosts. Genes are lost in all functional categories, but core genes for central informational processes, including genes encoding ribosomal proteins, are mostly retained, whereas genes underlying production of cell envelope components are especially depleted. Thus, these entities retain cell-like properties but are heavily dependent on coadaptation of hosts, which continuously evolve to support the symbionts upon which they depend.
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                Author and article information

                Contributors
                anna.zaidman@insa-lyon.fr
                aurelien.vigneron@yale.edu
                brian.weiss@yale.edu
                abdelaziz.heddi@insa-lyon.fr
                Journal
                BMC Microbiol
                BMC Microbiol
                BMC Microbiology
                BioMed Central (London )
                1471-2180
                23 November 2018
                23 November 2018
                2018
                : 18
                Issue : Suppl 1 Issue sponsor : Publication of this supplement was funded by the International Atomic Energy Agency. The peer review process for articles published in this supplement was overseen by the Supplement Editors in accordance with BioMed Central's peer review guidelines for supplements. The Supplement Editors declare that they were not involved in the peer review of any article on which they are an author. They declare no other competing interests.
                : 150
                Affiliations
                [1 ]GRID grid.464147.4, Univ Lyon, INSA-Lyon, INRA, BF2I, UMR0203, ; F-69621 Villeurbanne, France
                [2 ]ISNI 0000000419368710, GRID grid.47100.32, Department of Epidemiology of Microbial Diseases, , Yale School of Public Health, ; New Haven, CT USA
                Article
                1278
                10.1186/s12866-018-1278-5
                6251153
                30470176
                d0d73e17-febe-4e1d-bdb8-18b4a885f3e9
                © 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.

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                © The Author(s) 2018

                Microbiology & Virology
                cereal weevil,tsetse fly,endosymbiosis,immunity,evolution,insects,homeostasis
                Microbiology & Virology
                cereal weevil, tsetse fly, endosymbiosis, immunity, evolution, insects, homeostasis

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