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Abdelaziz Heddi - One of the best experts on this subject based on the ideXlab platform.
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An IMD-like pathway mediates both Endosymbiont control and host immunity in the cereal weevil Sitophilus spp.
Microbiome, 2018Co-Authors: Justin Maire, Carole Vincent-monégat, Anna Zaidman-rémy, Florent Masson, Abdelaziz HeddiAbstract:Many insects developing on nutritionally unbalanced diets have evolved symbiotic associations with vertically transmitted intracellular bacteria (Endosymbionts) that provide them with metabolic components, thereby improving the host’s abilities to thrive on such poor ecological niches. While host-Endosymbiont coevolutionary constraints are known to entail massive genomic changes in the microbial partner, host’s genomic evolution remains elusive, particularly with regard to the immune system. In the cereal weevil Sitophilus spp., which houses Sodalis pierantonius, Endosymbionts are secluded in specialized host cells, the bacteriocytes that group together as an organ, the bacteriome. We previously reported that at standard conditions, the bacteriome highly expresses the coleoptericin A (colA) antimicrobial peptide (AMP), which was shown to prevent Endosymbiont escape from the bacteriocytes. However, following the insect systemic infection by pathogens, the bacteriome upregulates a cocktail of AMP encoding genes, including colA. The regulations that allow these contrasted immune responses remain unknown. In this short report, we provide evidence that an IMD-like pathway is conserved in two sibling species of cereal weevils, Sitophilus oryzae and Sitophilus zeamais. RNA interference (RNAi) experiments showed that imd and relish genes are essential for (i) colA expression in the bacteriome under standard conditions, (ii) AMP up-regulation in the bacteriome following a systemic immune challenge, and (iii) AMP systemic induction following an immune challenge. Histological analyses also showed that relish inhibition by RNAi resulted in Endosymbiont escape from the bacteriome, strengthening the involvement of an IMD-like pathway in Endosymbiont control. We conclude that Sitophilus’ IMD-like pathway mediates both the bacteriome immune program involved in Endosymbiont seclusion within the bacteriocytes and the systemic and local immune responses to exogenous challenges. This work provides a striking example of how a conserved immune pathway, initially described as essential in pathogen clearance, also functions in the control of mutualistic associations.
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Antimicrobial peptides and cell processes tracking Endosymbiont dynamics
Philosophical Transactions of the Royal Society B: Biological Sciences, 2016Co-Authors: F. Masson, Anna Zaidman-rémy, Abdelaziz HeddiAbstract:Many insects sustain long-term relationships with intracellular symbiotic bacteria that provide them with essential nutrients. Such endosymbiotic relationships likely emerged from ancestral infections of the host by free-living bacteria, the genomes of which experience drastic gene losses and rearrangements during the host–symbiont coevolution. While it is well documented that Endosymbiont genome shrinkage results in the loss of bacterial virulence genes, whether and how the host immune system evolves towards the tolerance and control of bacterial partners remains elusive. Remarkably, many insects rely on a ‘compartmentalization strategy’ that consists in secluding Endosymbionts within specialized host cells, the bacteriocytes, thus preventing direct symbiont contact with the host systemic immune system. In this review, we compile recent advances in the understanding of the bacteriocyte immune and cellular regulators involved in Endosymbiont maintenance and control. We focus on the cereal weevils Sitophilus spp., in which bacteriocytes form bacteriome organs that strikingly evolve in structure and number according to insect development and physiological needs. We discuss how weevils track Endosymbiont dynamics through at least two mechanisms: (i) a bacteriome local antimicrobial peptide synthesis that regulates Endosymbiont cell cytokinesis and helps to maintain a homeostatic state within bacteriocytes and (ii) some cellular processes such as apoptosis and autophagy which adjust Endosymbiont load to the host developmental requirements, hence ensuring a fine-tuned integration of symbiosis costs and benefits.
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Weevil Endosymbiont dynamics is associated with a clamping of immunity
BMC genomics, 2015Co-Authors: Florent Masson, Nicolas Parisot, Agnès Vallier, Séverine Balmand, Carole Vincent-monégat, Anna Zaidman-rémy, Aurélien Vigneron, Yves Mone, Marie-christine Carpentier, Abdelaziz HeddiAbstract:Insects subsisting on nutritionally unbalanced diets have evolved long-term mutualistic relationships with intracellular symbiotic bacteria (Endosymbionts). The Endosymbiont population load undergoes changes along with insect development. In the cereal weevil Sitophilus oryzae, the midgut Endosymbionts Sodalis pierantonius drastically multiply following adult metamorphosis and rapidly decline until total elimination when the insect achieves its cuticle synthesis. Whilst symbiont load was shown to timely meet insect metabolic needs, little is known about the host molecular and immune processes underlying this dynamics. We performed RNA sequencing analysis on weevil midguts at three representative phases of the Endosymbiont dynamics (i.e. increase, climax and decrease). To screen genes which transcriptional changes are specifically related to symbiont dynamics and not to the intrinsic development of the midgut, we further have monitored by RT-qPCR sixteen gene transcript levels in symbiotic and artificially non-symbiotic (aposymbiotic) weevils. We also localized the Endosymbionts during the elimination process by fluorescence microscopy. Functional analysis of the host differentially expressed genes by RNA sequencing showed that the main transcriptional changes occur during Endosymbiont growth phase and affect cell proliferation, apoptosis, autophagy, phagocytosis, and metabolism of fatty acids and nucleic acids. We also showed that symbiont dynamics alters the expression of several genes involved in insect development. Our results strengthened the implication of apoptosis and autophagy processes in symbiont elimination and recycling. Remarkably, apart from the coleoptericin A that is known to target Endosymbionts and controls their division and location, no gene coding antimicrobial peptide was upregulated during the symbiont growth and elimination phases. We show that Endosymbiont dynamics parallels numerous transcriptional changes in weevil developing adults and affects several biological processes, including metabolism and development. It also triggers cell apoptosis, autophagy and gut epithelial cell swelling and delamination. Strikingly, immunity is repressed during the whole process, presumably avoiding tissue inflammation and allowing insects to optimize nutrient recovery from recycled Endosymbiont.
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Insects recycle Endosymbionts when the benefit is over.
Current biology : CB, 2014Co-Authors: Aurélien Vigneron, Agnès Vallier, Séverine Balmand, Carole Vincent-monégat, Anna Zaidman-rémy, Florent Masson, Marjolaine Rey, Emre Aksoy, Etienne Aubailly-giraud, Abdelaziz HeddiAbstract:Symbiotic associations are widespread in nature and represent a driving force in evolution. They are known to impact fitness, and thereby shape the host phenotype. Insects subsisting on nutritionally poor substrates have evolved mutualistic relationships with intracellular symbiotic bacteria (Endosymbionts) that supply them with metabolic components lacking in their diet. In many species, Endosymbionts are hosted within specialized host cells, called the bacteriocytes, and transmitted vertically across host generations. How hosts balance the costs and benefits of having Endosymbionts, and whether and how they adjust symbiont load to their physiological needs, remains largely unexplored. By investigating the cereal weevil Sitophilus association with the Sodalis pierantonius Endosymbiont, we discover that Endosymbiont populations intensively multiply in young adults, before being rapidly eliminated within few days. We show that young adults strongly depend on Endosymbionts and that Endosymbiont proliferation after metamorphosis matches a drastic host physiological need for the tyrosine (Tyr) and phenylalanine (Phe) amino acids to rapidly build their protective exoskeleton. Tyr and Phe are precursors of the dihydroxyphenylalanine (DOPA) molecule that is an essential component for the cuticle synthesis. Once the cuticle is achieved, DOPA reaches high amounts in insects, which triggers Endosymbiont elimination. This elimination relies on apoptosis and autophagy activation, allowing digestion and recycling of the Endosymbiont material. Thus, the weevil-Endosymbiont association reveals an adaptive interplay between metabolic and cellular functions that minimizes the cost of symbiosis and speeds up the exoskeleton formation during a critical phase when emerging adults are especially vulnerable.
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Endosymbiont diversity among sibling weevil species competing for the same resource
BMC Evolutionary Biology, 2013Co-Authors: Adrien Merville, Agnès Vallier, Abdelaziz Heddi, Samuel Venner, Hélène Henri, Frédéric Menu, Fabrice Vavre, Marie-claude Bel-vennerAbstract:BACKGROUND: Whereas the impact of Endosymbionts on the ecology of their hosts is well known in some insect species, the question of whether host communities are influenced by Endosymbionts remains largely unanswered. Notably, the coexistence of host species competing with each other, which is expected to be stabilized by their ecological differences, could be facilitated by differences in their Endosymbionts. Yet, the composition of endosymbiotic communities housed by natural communities of competing host species is still almost unknown. In this study, we started filling this gap by describing and comparing the bacterial endosymbiotic communities of four sibling weevil species (Curculio spp.) that compete with each other to lay eggs into oak acorns (Quercus spp.) and exhibit marked ecological differences. RESULTS: All four species housed the primary Endosymbiont Candidatus Curculioniphilus buchneri, yet each of these had a clearly distinct community of secondary Endosymbionts, including Rickettsia, Spiroplasma, and two Wolbachia strains. Notably, three weevil species harbored their own predominant facultative Endosymbiont and possessed the remaining symbionts at a residual infection level. CONCLUSIONS: The four competing species clearly harbor distinct endosymbiotic communities. We discuss how such endosymbiotic communities could spread and keep distinct in the four insect species, and how these symbionts might affect the organization and species richness of host communities.
Mitsunori Iwataki - One of the best experts on this subject based on the ideXlab platform.
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Dinoflagellates with relic Endosymbiont nuclei as models for elucidating organellogenesis
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Chihiro Sarai, Takuro Nakayama, Goro Tanifuji, Ryoma Kamikawa, Kazuya Takahashi, Ken-ichiro Ishida, Hideaki Miyashita, Euki Yazaki, Eriko Matsuo, Mitsunori IwatakiAbstract:Nucleomorphs are relic Endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an Endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the Endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the Endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which Endosymbiont-to-host DNA transfer is on-going and for which Endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal Endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of Endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and Endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the Endosymbionts at the genus level. With the combined evidence, we conclude that the host-Endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.
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Dinoflagellates with relic Endosymbiont nuclei as novel models for elucidating organellogenesis
bioRxiv, 2019Co-Authors: Chihiro Sarai, Takuro Nakayama, Goro Tanifuji, Ryoma Kamikawa, Kazuya Takahashi, Ken-ichiro Ishida, Mitsunori Iwataki, Hideaki Miyashita, Yuji InagakiAbstract:Nucleomorphs are relic Endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process integrating an Endosymbiont alga into be a host-governed plastid (organellogenesis). Nevertheless, past studies suggested that DNA transfer from the Endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making difficult to infer how organellogenesis altered the Endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which from-Endosymbiont-to-host DNA transfer is on-going and of which Endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal Endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide the evidence for the presence of DNA in the two nucleomorphs and transfer of Endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and Endosymbiont nuclei was found to be in progress in both MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the Endosymbionts at the genus level. Combined, we conclude that the host-Endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as new models for elucidating organellogenesis.
Chihiro Sarai - One of the best experts on this subject based on the ideXlab platform.
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Dinoflagellates with relic Endosymbiont nuclei as models for elucidating organellogenesis
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Chihiro Sarai, Takuro Nakayama, Goro Tanifuji, Ryoma Kamikawa, Kazuya Takahashi, Ken-ichiro Ishida, Hideaki Miyashita, Euki Yazaki, Eriko Matsuo, Mitsunori IwatakiAbstract:Nucleomorphs are relic Endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an Endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the Endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the Endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which Endosymbiont-to-host DNA transfer is on-going and for which Endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal Endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of Endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and Endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the Endosymbionts at the genus level. With the combined evidence, we conclude that the host-Endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.
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Dinoflagellates with relic Endosymbiont nuclei as novel models for elucidating organellogenesis
bioRxiv, 2019Co-Authors: Chihiro Sarai, Takuro Nakayama, Goro Tanifuji, Ryoma Kamikawa, Kazuya Takahashi, Ken-ichiro Ishida, Mitsunori Iwataki, Hideaki Miyashita, Yuji InagakiAbstract:Nucleomorphs are relic Endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process integrating an Endosymbiont alga into be a host-governed plastid (organellogenesis). Nevertheless, past studies suggested that DNA transfer from the Endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making difficult to infer how organellogenesis altered the Endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which from-Endosymbiont-to-host DNA transfer is on-going and of which Endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal Endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide the evidence for the presence of DNA in the two nucleomorphs and transfer of Endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and Endosymbiont nuclei was found to be in progress in both MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the Endosymbionts at the genus level. Combined, we conclude that the host-Endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as new models for elucidating organellogenesis.
Hugh A. Smith - One of the best experts on this subject based on the ideXlab platform.
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Bacterial Endosymbiont Diversity Among Bemisia tabaci (Hemiptera: Aleyrodidae) Populations in Florida.
Insects, 2020Co-Authors: Bruno Rossitto De Marchi, Hugh A. SmithAbstract:The sweetpotato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), is a pest of many economically important agricultural crops and a vector of plant viruses. Bemisia tabaci harbors facultative Endosymbiont species that have been implicated in pest status, including tolerance to insecticides, virus transmission efficiency and tolerance to high-temperatures. The facultative Endosymbionts reported in B. tabaci include Arsenophonus, Hamiltonella, Wolbachia, Cardinium, Fritschea and Rickettsia. We collected whitefly populations from weed and crop hosts in south Florida and identified the whitefly species as well as the facultative Endosymbionts present in these populations by molecular analysis. In addition, a phylogenetic analysis of whiteflies and their Endosymbionts was performed. The only facultative Endosymbionts found among the B. tabaci populations collected in Florida were Hamiltonella and Rickettsia. The phylogenetic analysis revealed the low genetic diversity of whiteflies and their Endosymbionts. Additionally, the phylogenetic tree clustered Rickettsia from Florida in the R1 genetic group. The results will aid to understand the role of the bacterial Endosymbionts in the whitefly host.
Einat Zchorifein - One of the best experts on this subject based on the ideXlab platform.
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Endosymbiont metacommunities mtdna diversity and the evolution of the bemisia tabaci hemiptera aleyrodidae species complex
Molecular Ecology, 2010Co-Authors: Gwenaelle Gueguen, Murad Ghanim, Fabrice Vavre, Olivier Gnankine, Michel Peterschmitt, Delphine Charif, Elad Chiel, Yuval Gottlieb, Einat ZchorifeinAbstract:Bemisia tabaci, an invasive pest that causes crop damage worldwide, is a highly differentiated species complex, divided into biotypes that have mainly been defined based on mitochondrial DNA sequences. Although Endosymbionts can potentially induce population differentiation, specialization and indirect selection on mtDNA, studies have largely ignored these influential passengers in B. tabaci, despite as many as seven bacterial Endosymbionts have been identified. Here, we investigate the composition of the whole bacterial community in worldwide populations of B. tabaci, together with host genetic differentiation, focusing on the invasive B and Q biotypes. Among 653 individuals studied, more than 95% of them harbour at least one secondary Endosymbiont, and multiple infections are very common. In addition, sequence analyses reveal a very high diversity of facultative Endosymbionts in B. tabaci, with some bacterial genus being represented by more than one strain. In the B and Q biotypes, nine different strains of bacteria have been identified. The mtDNA-based phylogeny of B. tabaci also reveals a very high nucleotide diversity that partitions the two ITS clades (B and Q) into six CO1 genetic groups. Each genetic group is in linkage disequilibrium with a specific combination of Endosymbionts. All together, our results demonstrate the rapid dynamics of the bacterial Endosymbiont–host associations at a small evolutionary scale, questioning the role of endosymbiotic communities in the evolution of the Bemisia tabaci species complex and strengthening the need to develop a metacommunity theory of inherited Endosymbionts.