Sample records for bacteriocytes
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Wolbachia as a bacteriocyte-associated nutritional mutualist
Hosokawa, Takahiro; Koga, Ryuichi; Kikuchi, Yoshitomo; Meng, Xian-Ying; Fukatsu, Takema
2009-01-01
Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid–Buchnera and tsetse–Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed γ-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the γ-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum. PMID:20080750
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Toenshoff, Elena R; Penz, Thomas; Narzt, Thomas; Collingro, Astrid; Schmitz-Esser, Stephan; Pfeiffer, Stefan; Klepal, Waltraud; Wagner, Michael; Weinmaier, Thomas; Rattei, Thomas; Horn, Matthias
2012-01-01
Adelgids (Insecta: Hemiptera: Adelgidae) are known as severe pests of various conifers in North America, Canada, Europe and Asia. Here, we present the first molecular identification of bacteriocyte-associated symbionts in these plant sap-sucking insects. Three geographically distant populations of members of the Adelges nordmannianae/piceae complex, identified based on coI and ef1alpha gene sequences, were investigated. Electron and light microscopy revealed two morphologically different endosymbionts, coccoid or polymorphic, which are located in distinct bacteriocytes. Phylogenetic analyses of their 16S and 23S rRNA gene sequences assigned both symbionts to novel lineages within the Gammaproteobacteria sharing <92% 16S rRNA sequence similarity with each other and showing no close relationship with known symbionts of insects. Their identity and intracellular location were confirmed by fluorescence in situ hybridization, and the names ‘Candidatus Steffania adelgidicola' and ‘Candidatus Ecksteinia adelgidicola' are proposed for tentative classification. Both symbionts were present in all individuals of all investigated populations and in different adelgid life stages including eggs, suggesting vertical transmission from mother to offspring. An 85 kb genome fragment of ‘Candidatus S. adelgidicola' was reconstructed based on a metagenomic library created from purified symbionts. Genomic features including the frequency of pseudogenes, the average length of intergenic regions and the presence of several genes which are absent in other long-term obligate symbionts, suggested that ‘Candidatus S. adelgidicola' is an evolutionarily young bacteriocyte-associated symbiont, which has been acquired after diversification of adelgids from their aphid sister group. PMID:21833037
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Szklarzewicz, Teresa; Kalandyk-Kołodziejczyk, Małgorzata; Michalik, Katarzyna; Jankowska, Władysława; Michalik, Anna
2018-01-01
The scale insect Puto superbus (Putoidae) lives in mutualistic symbiotic association with bacteria. Molecular phylogenetic analyses have revealed that symbionts of P. superbus belong to the gammaproteobacterial genus Sodalis. In the adult females, symbionts occur both in the bacteriocytes constituting compact bacteriomes and in individual bacteriocytes, which are dispersed among ovarioles. The bacteriocytes also house a few small, rod-shaped Wolbachia bacteria in addition to the numerous large, elongated Sodalis-allied bacteria. The symbiotic microorganisms are transovarially transmitted from generation to generation. In adult females which have choriogenic oocytes in the ovarioles, the bacteriocytes gather around the basal part of the tropharium. Next, the entire bacteriocytes pass through the follicular epithelium surrounding the neck region of the ovariole and enter the space between oocyte and follicular epithelium (perivitelline space). In the perivitelline space, the bacteriocytes assemble extracellularly in the deep depression of the oolemma at the anterior pole of the oocyte, forming a "symbiont ball".
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Gruwell, Matthew E.; Flarhety, Meghan; Dittmar, Katharina
2012-01-01
It has long been known that armored scale insects harbor endosymbiotic bacteria inside specialized cells called bacteriocytes. Originally, these endosymbionts were thought to be fungal symbionts but they are now known to be bacterial and have been named Uzinura diaspidicola. Bacteriocyte and endosymbiont distribution patterns within host insects were visualized using in situ hybridization via 16S rRNA specific probes. Images of scale insect embryos, eggs and adult scale insects show patterns of localized bacteriocytes in embryos and randomly distributed bacteriocytes in adults. The symbiont pocket was not found in the armored scale insect eggs that were tested. The pattern of dispersed bacteriocytes in adult scale insects suggest that Uzinura and Blattabacteria may share some homologous traits that coincide with similar life style requirements, such as dispersal in fat bodies and uric acid recycling. PMID:26467959
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Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis.
Poliakov, Anton; Russell, Calum W; Ponnala, Lalit; Hoops, Harold J; Sun, Qi; Douglas, Angela E; van Wijk, Klaas J
2011-06-01
Many insects are nutritionally dependent on symbiotic microorganisms that have tiny genomes and are housed in specialized host cells called bacteriocytes. The obligate symbiosis between the pea aphid Acyrthosiphon pisum and the γ-proteobacterium Buchnera aphidicola (only 584 predicted proteins) is particularly amenable for molecular analysis because the genomes of both partners have been sequenced. To better define the symbiotic relationship between this aphid and Buchnera, we used large-scale, high accuracy tandem mass spectrometry (nanoLC-LTQ-Orbtrap) to identify aphid and Buchnera proteins in the whole aphid body, purified bacteriocytes, isolated Buchnera cells and the residual bacteriocyte fraction. More than 1900 aphid and 400 Buchnera proteins were identified. All enzymes in amino acid metabolism annotated in the Buchnera genome were detected, reflecting the high (68%) coverage of the proteome and supporting the core function of Buchnera in the aphid symbiosis. Transporters mediating the transport of predicted metabolites were present in the bacteriocyte. Label-free spectral counting combined with hierarchical clustering, allowed to define the quantitative distribution of a subset of these proteins across both symbiotic partners, yielding no evidence for the selective transfer of protein among the partners in either direction. This is the first quantitative proteome analysis of bacteriocyte symbiosis, providing a wealth of information about molecular function of both the host cell and bacterial symbiont.
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Mealybugs with distinct endosymbiotic systems living on the same host plant.
Koga, Ryuichi; Nikoh, Naruo; Matsuura, Yu; Meng, Xian-Ying; Fukatsu, Takema
2013-01-01
Mealybugs (Homoptera: Coccoidea: Pseudococcidae) possess a large bacteriome consisting of a number of bacteriocytes whose cytoplasm is populated by endosymbiotic bacteria. In many mealybugs of the subfamily Pseudococcinae, a peculiar endosymbiotic configuration has been identified: within the bacteriocytes, the primary betaproteobacterial endosymbiont Tremblaya princeps endocellularly harbor secondary gammaproteobacterial endosymbionts in a nested manner. Meanwhile, some mealybugs of the subfamily Phenacoccinae are associated only with a betaproteobacterial endosymbiont, designated as Tremblaya phenacola, which constitutes a distinct sister clade of T. princeps. However, cytological configuration of the endosymbiotic system in the phenacoccine mealybugs has not been established. Here, we investigated the endosymbiotic systems of the azalea mealybugs Crisicoccus azaleae (Pseudococcinae) and Phenacoccus azaleae (Phenacoccinae) living on the same host plants. Crisicoccus azaleae possessed a nested endosymbiotic system with T. princeps within the bacteriocyte cytoplasm and itself endocellularly harboring gammaproteobacterial cells, whereas P. azaleae exhibited a simple endosymbiotic system in which T. phenacola cells are localized within the bacteriocytes without additional gammaproteobacterial associates. Considering that these mealybugs live on the identical plant phloem sap, these different endosymbiotic consortia likely play similar biological roles for their host insects. The findings presented here should be helpful for future functional and comparative genomics toward elucidating evolutionary pathways of mealybugs and their endosymbionts. © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.
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Hongo, Yuki; Ikuta, Tetsuro; Takaki, Yoshihiro; Shimamura, Shigeru; Shigenobu, Shuji; Maruyama, Tadashi; Yoshida, Takao
2016-07-10
Deep-sea vesicomyid clams, including the genus Phreagena (formerly Calyptogena), harbor thioautotrophic bacterial symbionts in the host symbiosome, which consists of cytoplasmic vacuoles in gill epithelial cells called bacteriocytes. The symbiont requires inorganic carbon (Ci), such as CO2, HCO3(-), and CO3(2-), to synthesize organic compounds, which are utilized by the host clam. The dominant Ci in seawater is HCO3(-), which is impermeable to cell membranes. Within the bacteriocyte, cytoplasmic carbonic anhydrase (CA) from the host, which catalyzes the inter-conversion between CO2 and HCO3(-), has been shown to be abundant and is thought to supply intracellular CO2 to symbionts in the symbiosome. However, the mechanism of Ci uptake by the host gill from seawater is poorly understood. To elucidate the influx pathway of Ci into the bacteriocyte, we isolated the genes related to Ci uptake via the pyrosequencing of cDNA from the gill of Phreagena okutanii, and investigated their expression patterns. Using phylogenetic and amino acid sequence analyses, three solute carrier family 4 (SLC4) bicarbonate transporters (slc4co1, slc4co2, and slc4co4) and two membrane-associated CAs (mcaco1 and mcaco2) were identified as candidate genes for Ci uptake. In an in situ hybridization analysis of gill sections, the expression of mcaco1 and mcaco2 was detected in the bacteriocytes and asymbiotic non-ciliated cells, respectively, and the expression of slc4co1 and slc4co2 was detected in the asymbiotic cells, including the intermediate cells of the inner area and the non-ciliated cells of the external area. Although subcellular localizations of the products of these genes have not been fully elucidated, they may play an important role in the uptake of Ci into the bacteriocytes. These findings will improve our understanding of the Ci transport system in the symbiotic relationships of chemosynthetic bivalves. Copyright © 2016 Elsevier B.V. All rights reserved.
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Antimicrobial peptides keep insect endosymbionts under control.
Login, Frédéric H; Balmand, Séverine; Vallier, Agnès; Vincent-Monégat, Carole; Vigneron, Aurélien; Weiss-Gayet, Michèle; Rochat, Didier; Heddi, Abdelaziz
2011-10-21
Vertically transmitted endosymbionts persist for millions of years in invertebrates and play an important role in animal evolution. However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. Although this family of peptides is commonly linked with microbe clearance, this work shows that endosymbiosis benefits from ColA, suggesting that long-term host-symbiont coevolution might have shaped immune effectors for symbiont maintenance.
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Caro, Audrey; Got, Patrice; Bouvy, Marc; Troussellier, Marc; Gros, Olivier
2009-01-01
The bivalve Codakia orbicularis, hosting sulfur-oxidizing gill endosymbionts, was starved (in artificial seawater filtered through a 0.22-μm-pore-size membrane) for a long-term experiment (4 months). The effects of starvation were observed using transmission electron microscopy, fluorescence in situ hybridization and catalyzed reporter deposition (CARD-FISH), and flow cytometry to monitor the anatomical and physiological modifications in the gill organization of the host and in the symbiotic population housed in bacteriocytes. The abundance of the symbiotic population decreased through starvation, with a loss of one-third of the bacterial population each month, as shown by CARD-FISH. At the same time, flow cytometry revealed significant changes in the physiology of symbiotic cells, with a decrease in cell size and modifications to the nucleic acid content, while most of the symbionts maintained a high respiratory activity (measured using the 5-cyano-2,3-ditolyl tetrazolium chloride method). Progressively, the number of symbiont subpopulations was reduced, and the subsequent multigenomic state, characteristic of this symbiont in freshly collected clams, turned into one and five equivalent genome copies for the two remaining subpopulations after 3 months. Concomitant structural modifications appeared in the gill organization. Lysosymes became visible in the bacteriocytes, while large symbionts disappeared, and bacteriocytes were gradually replaced by granule cells throughout the entire lateral zone. Those data suggested that host survival under these starvation conditions was linked to symbiont digestion as the main nutritional source. PMID:19346359
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Insect immune system maintains long-term resident bacteria through a local response.
Login, Frédéric H; Heddi, Abdelaziz
2013-02-01
Long-term associations between bacteria and animals are widely represented in nature and play an important role in animal adaptation and evolution. In insects thriving on nutritionally unbalanced diets, intracellular symbiotic bacteria (endosymbionts) complement the host nutrients with amino acids and vitamins and interfere with host physiology and reproduction. Endosymbionts permanently infect host cells, called bacteriocytes, which express an adapted local immune response that permits symbiont maintenance and control. Among the immune players in bacteriocytes, the coleoptericin A (ColA) antimicrobial peptide of the cereal weevil, Sitophilus zeamais, was recently found to specifically trigger endosymbionts and to inhibit their cytokinesis, thereby limiting bacterial cell division and dispersion throughout the insect tissues. This review focuses on the biological and evolutionary features of Sitophilus symbiosis, and discusses the possible interactions of ColA with weevil endosymbiont proteins and pathways. Copyright © 2012 Elsevier Ltd. All rights reserved.
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Cooper, W. Rodney; Garczynski, Stephen F.; Horton, David R.
2015-01-01
Carsonella ruddii (Gamma Proteobacterium) is an obligate bacterial endosymbiont of psyllids that produces essential amino acids that are lacking in the insect’s diet. Accurate estimations of Carsonella populations are important to studies of Carsonella-psyllid interactions and to developing ways to target Carsonella for control of psyllid pests including pear psylla, Cacopsylla pyricola (Förster) (Hemiptera: Psyllidae) and potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae). We used two methods, namely fluorescence in situ hybridization and quantitative polymerase chain reaction (qPCR), to estimate relative abundance of Carsonella in bacteriocytes and whole bodies of psyllids, respectively. Using these two methods, we compared Carsonella populations between female and male insects. Estimations using fluorescence in situ hybridization indicated that Carsonella was more abundant in bacteriocytes of female C. pyricola than in those of males, but Carsonella abundance in bacteriocytes did not differ between sexes of B. cockerelli. Analyses by qPCR using whole-body specimens indicated Carsonella was more abundant in females than in males of both psyllids. Neither fluorescence in situ hybridization nor qPCR indicated that Carsonella populations differed in abundance among adults of different ages (0–3 wk after adult eclosion). Using fluorescence in situ hybridization, Carsonella was observed in ovarioles of newly emerged females and formed an aggregation in the posterior end of mature oocytes. Results of our study indicate that female psyllids harbor greater populations of Carsonella than do males and that sex should be controlled for in studies which require estimations of Carsonella populations. PMID:26056318
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Elisabeth, Nathalie H; Gustave, Sylvie D D; Gros, Olivier
2012-08-01
The shallow-water bivalve Codakia orbiculata which harbors gill-endosymbiotic sulfur-oxidizing γ-proteobacteria can lose and acquire its endosymbionts throughout its life. Long-term starvation and recolonization experiments led to changes in the organization of cells in the lateral zone of gill filaments. This plasticity is linked to the presence or absence of gill-endosymbionts. Herein, we propose that this reorganization can be explained by three hypotheses: (a) a variation in the number of bacteriocytes and granule cells due to proliferation or apoptosis processes, (b) a variation of the volume of these two cell types without modification in the number, and (c) a combination of both number and cell volume variation. To test these hypotheses, we analyzed cell reorganization in terms of proliferation and apoptosis in adults submitted to starvation and returned to the field using catalyzed reporter deposition fluorescence in situ hybridization, immunohistochemistry, and structural analyses. We observed that cell and tissue reorganization in gills filaments is due to a variation in cell relative abundance that maybe associated with a variation in cell apparent volume and depends on the environment. In fact, bacteriocytes mostly multiply in freshly collected and newly recolonized individuals, and excess bacteriocytes are eliminated in later recolonization stages. We highlight that host tissue regeneration in gill filaments of this symbiotic bivalve can occur by both replication of existing cells and division of undifferentiated cells localized in tissular bridges, which might be a tissue-specific multipotent stem cell zone. Copyright © 2012 Wiley Periodicals, Inc.
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Caspi-Fluger, Ayelet; Inbar, Moshe; Mozes-Daube, Netta; Mouton, Laurence; Hunter, Martha S.; Zchori-Fein, Einat
2011-01-01
Intracellular symbionts of arthropods have diverse influences on their hosts, and their functions generally appear to be associated with their localization within the host. The effect of localization pattern on the role of a particular symbiont cannot normally be tested since the localization pattern within hosts is generally invariant. However, in Israel, the secondary symbiont Rickettsia is unusual in that it presents two distinct localization patterns throughout development and adulthood in its whitefly host, Bemisia tabaci (B biotype). In the “scattered” pattern, Rickettsia is localized throughout the whitefly hemocoel, excluding the bacteriocytes, where the obligate symbiont Portiera aleyrodidarum and some other secondary symbionts are housed. In the “confined” pattern, Rickettsia is restricted to the bacteriocytes. We examined the effects of these patterns on Rickettsia densities, association with other symbionts (Portiera and Hamiltonella defensa inside the bacteriocytes) and on the potential for horizontal transmission to the parasitoid wasp, Eretmocerus mundus, while the wasp larvae are developing within the whitefly nymph. Sequences of four Rickettsia genes were found to be identical for both localization patterns, suggesting that they are closely related strains. However, real-time PCR analysis showed very different dynamics for the two localization types. On the first day post-adult emergence, Rickettsia densities were 21 times higher in the “confined” pattern vs. “scattered” pattern whiteflies. During adulthood, Rickettsia increased in density in the “scattered” pattern whiteflies until it reached the “confined” pattern Rickettsia density on day 21. No correlation between Rickettsia densities and Hamiltonella or Portiera densities were found for either localization pattern. Using FISH technique, we found Rickettsia in the gut of the parasitoid wasps only when they developed on whiteflies with the “scattered” pattern. The
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Caspi-Fluger, Ayelet; Inbar, Moshe; Mozes-Daube, Netta; Mouton, Laurence; Hunter, Martha S; Zchori-Fein, Einat
2011-01-01
Intracellular symbionts of arthropods have diverse influences on their hosts, and their functions generally appear to be associated with their localization within the host. The effect of localization pattern on the role of a particular symbiont cannot normally be tested since the localization pattern within hosts is generally invariant. However, in Israel, the secondary symbiont Rickettsia is unusual in that it presents two distinct localization patterns throughout development and adulthood in its whitefly host, Bemisia tabaci (B biotype). In the "scattered" pattern, Rickettsia is localized throughout the whitefly hemocoel, excluding the bacteriocytes, where the obligate symbiont Portiera aleyrodidarum and some other secondary symbionts are housed. In the "confined" pattern, Rickettsia is restricted to the bacteriocytes. We examined the effects of these patterns on Rickettsia densities, association with other symbionts (Portiera and Hamiltonella defensa inside the bacteriocytes) and on the potential for horizontal transmission to the parasitoid wasp, Eretmocerus mundus, while the wasp larvae are developing within the whitefly nymph. Sequences of four Rickettsia genes were found to be identical for both localization patterns, suggesting that they are closely related strains. However, real-time PCR analysis showed very different dynamics for the two localization types. On the first day post-adult emergence, Rickettsia densities were 21 times higher in the "confined" pattern vs. "scattered" pattern whiteflies. During adulthood, Rickettsia increased in density in the "scattered" pattern whiteflies until it reached the "confined" pattern Rickettsia density on day 21. No correlation between Rickettsia densities and Hamiltonella or Portiera densities were found for either localization pattern. Using FISH technique, we found Rickettsia in the gut of the parasitoid wasps only when they developed on whiteflies with the "scattered" pattern. The results suggest that the
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Coexistence of Wolbachia with Buchnera aphidicola and a Secondary Symbiont in the Aphid Cinara cedri
Gómez-Valero, Laura; Soriano-Navarro, Mario; Pérez-Brocal, Vicente; Heddi, Abdelaziz; Moya, Andrés; García-Verdugo, José Manuel; Latorre, Amparo
2004-01-01
Intracellular symbiosis is very common in the insect world. For the aphid Cinara cedri, we have identified by electron microscopy three symbiotic bacteria that can be characterized by their different sizes, morphologies, and electrodensities. PCR amplification and sequencing of the 16S ribosomal DNA (rDNA) genes showed that, in addition to harboring Buchnera aphidicola, the primary endosymbiont of aphids, C. cedri harbors a secondary symbiont (S symbiont) that was previously found to be associated with aphids (PASS, or R type) and an α-proteobacterium that belongs to the Wolbachia genus. Using in situ hybridization with specific bacterial probes designed for symbiont 16S rDNA sequences, we have shown that Wolbachia was represented by only a few minute bacteria surrounding the S symbionts. Moreover, the observed B. aphidicola and the S symbionts had similar sizes and were housed in separate specific bacterial cells, the bacteriocytes. Interestingly, in contrast to the case for all aphids examined thus far, the S symbionts were shown to occupy a similarly sized or even larger bacteriocyte space than B. aphidicola. These findings, along with the facts that C. cedri harbors the B. aphidicola strain with the smallest bacterial genome and that the S symbionts infect all Cinara spp. analyzed so far, suggest the possibility of bacterial replacement in these species. PMID:15375144
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The evolutionary development of plant-feeding insects and their nutritional endosymbionts.
Skidmore, Isabel H; Hansen, Allison K
2017-12-01
Herbivorous insects have evolved diverse mechanisms enabling them to feed on plants with suboptimal nutrient availability. Low nutrient availability negatively impacts insect herbivore development and fitness. To overcome this obstacle numerous insect lineages have evolved intimate associations with nutritional endosymbionts. This is especially true for insects that specialize on nitrogen-poor substrates, as these insects are highly dependent on intracellular symbionts to provide nitrogen lacking in their insect host's diet. Emerging evidence in these systems suggest that the symbiont's and/or the insect's biosynthetic pathways are dynamically regulated throughout the insect's development to potentially cope with the insect's changing nutritional demands. In this review, we evaluate the evolutionary development of symbiotic insect cells (bacteriocytes) by comparing and contrasting genes and mechanisms involved in maintaining and regulating the nutritional symbiosis throughout insect development in a diversity of insect herbivore-endosymbiont associations. With new advances in genome sequencing and functional genomics, we evaluate to what extent nutritional symbioses are shaped by (i) the regulation of symbiont titer, (ii) the regulation of insect symbiosis genes, and (iii) the regulation of symbiont genes. We discuss how important these mechanisms are for the biosynthesis of essential amino acids and vitamins across insect life stages in divergent insect-symbiont systems. We conclude by suggesting future directions of research to further elucidate the evolutionary development of bacteriocytes and the impact of these nutritional symbioses on insect-plant interactions. © 2017 Institute of Zoology, Chinese Academy of Sciences.
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Kim, Dohyup; Minhas, Bushra F; Li-Byarlay, Hongmei; Hansen, Allison K
2018-05-25
Microbes are known to influence insect-plant interactions; however, it is unclear if host-plant diet influences the regulation of nutritional insect symbioses. The pea aphid, Acyrthosiphon pisum , requires its nutritional endosymbiont, Buchnera , for the production of essential amino acids. We hypothesize that key aphid genes that regulate the nutritional symbioses respond to host-plant diet when aphids feed on a specialized (alfalfa) compared to a universal host-plant diet (fava), which vary in amino acid profiles. Using RNA-Seq and whole genome bisulfite sequencing, we measured gene expression and DNA methylation profiles for such genes when aphids fed on either their specialized or universal host-plant diets. Our results reveal that when aphids feed on their specialized host-plant they significantly up-regulate and/or hypo-methylate key aphid genes in bacteriocytes related to the amino acid metabolism, including glutamine synthetase in the GOGAT cycle that recycles ammonia into glutamine and the glutamine transporter ApGLNT1 Moreover, regardless of what host-plant aphids feed on we observed significant up-regulation and differential methylation of key genes involved in the amino acid metabolism and the glycine/serine metabolism, a metabolic program observed in proliferating cancer cells potentially to combat oxidative stress. Based on our results, we suggest that this regulatory response of key symbiosis genes in bacteriocytes allows aphids to feed on a suboptimal host-plant that they specialize on. Copyright © 2018, G3: Genes, Genomes, Genetics.
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Large-scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera)
Sabater-Muñoz, Beatriz; Legeai, Fabrice; Rispe, Claude; Bonhomme, Joël; Dearden, Peter; Dossat, Carole; Duclert, Aymeric; Gauthier, Jean-Pierre; Ducray, Danièle Giblot; Hunter, Wayne; Dang, Phat; Kambhampati, Srini; Martinez-Torres, David; Cortes, Teresa; Moya, Andrès; Nakabachi, Atsushi; Philippe, Cathy; Prunier-Leterme, Nathalie; Rahbé, Yvan; Simon, Jean-Christophe; Stern, David L; Wincker, Patrick; Tagu, Denis
2006-01-01
Aphids are the leading pests in agricultural crops. A large-scale sequencing of 40,904 ESTs from the pea aphid Acyrthosiphon pisum was carried out to define a catalog of 12,082 unique transcripts. A strong AT bias was found, indicating a compositional shift between Drosophila melanogaster and A. pisum. An in silico profiling analysis characterized 135 transcripts specific to pea-aphid tissues (relating to bacteriocytes and parthenogenetic embryos). This project is the first to address the genetics of the Hemiptera and of a hemimetabolous insect. PMID:16542494
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Kono, Marie; Koga, Ryuichi; Shimada, Masakazu; Fukatsu, Takema
2008-01-01
We investigated the infection dynamics of endosymbiotic bacteria in the developmental course of the mealybugs Planococcus kraunhiae and Pseudococcus comstocki. Molecular phylogenetic analyses identified a betaproteobacterium and a gammaproteobacterium from each of the mealybug species. The former bacterium was related to the β-endosymbionts of other mealybugs, i.e., “Candidatus Tremblaya princeps,” and formed a compact clade in the Betaproteobacteria. Meanwhile, the latter bacterium was related to the γ-endosymbionts of other mealybugs but belonged to distinct clades in the Gammaproteobacteria. Whole-mount in situ hybridization confirmed the peculiar nested formation in the endosymbiotic system of the mealybugs: the β-endosymbiont cells were present in the cytoplasm of the bacteriocytes, and the γ-endosymbiont cells were located in the β-endosymbiont cells. In nymphal and female development, a large oval bacteriome consisting of a number of bacteriocytes was present in the abdomen, wherein the endosymbionts were harbored. In male development, strikingly, the bacteriome progressively degenerated in prepupae and pupae and became almost unrecognizable in adult males. In the degeneration process, the γ-endosymbionts disappeared more rapidly than the β-endosymbionts did. Quantitative PCR analyses revealed that (i) the population dynamics of the endosymbionts in female development reflected the reproductive activity of the insects, (ii) the population dynamics of the endosymbionts were strikingly different between female development and male development, (iii) the endosymbiont populations drastically decreased in male development, and (iv) the γ-endosymbiont populations decreased more rapidly than the β-endosymbiont populations in male development. Possible mechanisms underlying the uncoupled regulation of the β- and γ-endosymbiont populations are discussed in relation to the establishment and evolution of this unique prokaryote-prokaryote endosymbiotic
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Toenshoff, Elena R; Gruber, Daniela; Horn, Matthias
2012-05-01
The Adelgidae (Insecta: Hemiptera), a small group of insects, are known as severe pests on various conifers of the northern hemisphere. Despite of this, little is known about their bacteriocyte-associated endosymbionts, which are generally important for the biology and ecology of plant sap-sucking insects. Here, we investigated the adelgid species complexes Adelges laricis/tardus, Adelges abietis/viridis and Adelges cooleyi/coweni, identified based on their coI and ef1alpha genes. Each of these insect groups harboured two phylogenetically different bacteriocyte-associated symbionts belonging to the Betaproteobacteria and the Gammaproteobacteria, respectively, as inferred from phylogenetic analyses of 16S rRNA gene sequences and demonstrated by fluorescence in situ hybridization. The betaproteobacterial symbionts of all three adelgid complexes ('Candidatus Vallotia tarda', 'Candidatus Vallotia virida' and 'Candidatus Vallotia cooleyia') share a common ancestor and show a phylogeny congruent with that of their respective hosts. Similarly, there is evidence for co-evolution between the gammaproteobacterial symbionts ('Candidatus Profftia tarda', 'Candidatus Profftia virida') and A. laricis/tardus and A. abietis/viridis. In contrast, the gammaproteobacterial symbiont of A. cooleyi/coweni ('Candidatus Gillettellia cooleyia') is different from that of the other two adelgids but shows a moderate relationship to the symbiont 'Candidatus Ecksteinia adelgidicola' of A. nordmannianae/piceae. All symbionts were present in all adelgid populations and life stages analysed, suggesting vertical transmission from mother to offspring. In sharp contrast to their sister group, the aphids, adelgids do not consistently contain a single obligate (primary) symbiont but have acquired phylogenetically different bacterial symbionts during their evolution, which included multiple infections and symbiont replacement. © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd.
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Symbiotic Bacteria Associated with Stomach Discs of Human Lice▿ †
Sasaki-Fukatsu, Kayoko ; Koga, Ryuichi; Nikoh, Naruo; Yoshizawa, Kazunori; Kasai, Shinji; Mihara, Minoru; Kobayashi, Mutsuo; Tomita, Takashi; Fukatsu, Takema
2006-01-01
The symbiotic bacteria associated with the stomach disc, a large aggregate of bacteriocytes on the ventral side of the midgut, of human body and head lice were characterized. Molecular phylogenetic analysis of 16S rRNA gene sequences showed that the symbionts formed a distinct and well-defined clade in the Gammaproteobacteria. The sequences exhibited AT-biased nucleotide composition and accelerated molecular evolution. In situ hybridization revealed that in nymphs and adult males, the symbiont was localized in the stomach disc, while in adult females, the symbiont was not in the stomach disc but in the lateral oviducts and the posterior pole of the oocytes due to female-specific symbiont migration. We propose the designation “Candidatus Riesia pediculicola” for the louse symbionts. PMID:16950915
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Sacchi, L
2004-06-01
This paper reviews the Author's contribution to the knowledge of the ultrastructural basis of the prokaryote-eukaryote interactions in different models assessed by an ultrastructural approach. In agreement with the hypothesis of the origin of eukaryotic cells, which are chimeras of several prokaryotes with different morpho-functional specializations, symbiosis had major consequence for evolution of life. In Arthropods, one of the most successful lifestyles, the presence of endosymbiotic prokaryotes, plays an important role in their metabolism. In some cases, genome integration has occurred in the endosymbiotic relationships with the host, proving that intracellular symbiosis is not merely a nutritional supplement. Intracellular symbiotic bacteria are also described in nematodes. In particular, the presence of intracellular Wolbachia in filariae, even if its function is not yet completely known, influences positively the reproductive biology and the survival of the host, as proved by antibiotic treatment against this bacterium. The ultrastructural images reported in this review were obtained using different species of cockroaches, termites, ticks and filarial nematodes. The traditional methods of transmission (TEM), scansion (SEM) and immuno electron microscopy were used. In addition, also freeze-fracture and deep-etching techniques were employed. The cockroaches and the primitive termite Mastotermes darwiniensis host symbiotic bacteria in the ovary and in specialized cells (bacteriocytes) of the fat body. These bacteria have the typical cell boundary profile of gram-negative bacteria and are enveloped in a vacuolar membrane produced by the host cell. Molecular sequence data of 16S rDNA of endosymbionts of five species of cockroaches and M. darwiniensis indicate that they are members of the Flavobacteria-bacteroides group and that the infection occurred in an ancestor common to cockroaches and termites probably after the end of the Paleozoic (250 Ma BP). The
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Michalik, Anna; Szwedo, Jacek; Stroiński, Adam; Świerczewski, Dariusz; Szklarzewicz, Teresa
2018-03-07
In contrast to Cicadomorpha, in which numerous symbiotic bacteria have been identified and characterized, the symbionts of fulgoromorphans are poorly known. Here, we present the results of histological, ultrastructural, and molecular analyses of the symbiotic system of the planthopper Ommatidiotus dissimilis. Amplification, cloning, and sequencing of bacterial 16S RNA genes have revealed that O. dissimilis is host to five types of bacteria. Apart from bacteria Sulcia and Vidania, which are regarded as ancestral symbionts of Fulgoromorpha, three additional types of bacteria belonging to the genera Sodalis, Wolbachia, and Rickettsia have been detected. Histological and ultrastructural investigations have shown that bacteria Sulcia, Vidania, and Sodalis house separate bacteriocytes, whereas bacteria Wolbachia and Rickettsia are dispersed within various insect tissue. Additionally, bacteria belonging to the genus Vidania occupy the bacteriome localized in the lumen of the hindgut. Both molecular and microscopic analyses have revealed that all the symbionts are transovarially transmitted between generations.
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Brentassi, María Eugenia; Franco, Ernesto; Balatti, Pedro; Medina, Rocío; Bernabei, Franco; Marino de Remes Lenicov, Ana M
2017-05-01
In this study, we surveyed the bacteriome-associated microbiota of the corn leafhopper Dalbulus maidis by means of histological, ultrastructural, and molecular analyses. Amplification and sequencing of 16S rDNA genes revealed that the endosymbiont "Candidatus Sulcia muelleri" (Phylum Bacteroidetes) resides in bacteriomes of D. maidis. Phylogenetic analysis showed that the sequence was closely allied to others found in representatives of the subfamily Deltocephalinae. We failed to amplify other sequences as "Candidatus Nasuia deltocephalinicola," a co-primary symbiont frequently associated to deltocephaline leafhoppers. In addition, a metagenetic analysis carried out in order to investigate the presence of other bacteriome-associated bacteria of D. maidis showed that the sequence of Sulcia accounted for 98.56 % of all the sequences. Histological and ultrastructural observations showed that microorganisms harbored in bacteriomes (central syncytium and cytoplasm of uninucleate bacteriocytes) look like others Sulcia described in hemipteran species and they were transovarially transmitted from mother to offspring which is typical of obligate endosymbionts. The only presence of Sulcia in the bacteriomes of D. maidis was discussed.
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Betcher, Meghan A.; Fung, Jennifer M.; Han, Andrew W.; O’Connor, Roberta; Seronay, Romell; Concepcion, Gisela P.; Distel, Daniel L.; Haygood, Margo G.
2012-01-01
Marine bivalves of the family Teredinidae (shipworms) are voracious consumers of wood in marine environments. In several shipworm species, dense communities of intracellular bacterial endosymbionts have been observed within specialized cells (bacteriocytes) of the gills (ctenidia). These bacteria are proposed to contribute to digestion of wood by the host. While the microbes of shipworm gills have been studied extensively in several species, the abundance and distribution of microbes in the digestive system have not been adequately addressed. Here we use Fluorescence In-Situ Hybridization (FISH) and laser scanning confocal microscopy with 16S rRNA directed oligonucleotide probes targeting all domains, domains Bacteria and Archaea, and other taxonomic groups to examine the digestive microbiota of 17 specimens from 5 shipworm species (Bankia setacea, Lyrodus pedicellatus, Lyrodus massa, Lyrodus sp. and Teredo aff. triangularis). These data reveal that the caecum, a large sac-like appendage of the stomach that typically contains large quantities of wood particles and is considered the primary site of wood digestion, harbors only very sparse microbial populations. However, a significant number of bacterial cells were observed in fecal pellets within the intestines. These results suggest that due to low abundance, bacteria in the caecum may contribute little to lignocellulose degradation. In contrast, the comparatively high population density of bacteria in the intestine suggests a possible role for intestinal bacteria in the degradation of lignocellulose. PMID:23028923
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Manzano-Marín, Alejandro; Oceguera-Figueroa, Alejandro; Latorre, Amparo; Jiménez-García, Luis F.; Moya, Andres
2015-01-01
Endosymbiosis is a common phenomenon in nature, especially between bacteria and insects, whose typically unbalanced diets are usually complemented by their obligate endosymbionts. While much interest and focus has been directed toward phloem-feeders like aphids and mealybugs, blood-feeders such as the Lone star tick (Amblyomma americanum), Glossina flies, and the human body louse (Pediculus humanus corporis) depend on obligate endosymbionts which complement their B-vitamin-deficient diets, and thus are required for growth and survival. Glossiphoniid leeches have also been found to harbor distinct endosymbionts housed in specialized organs. Here, we present the genome of the bacterial endosymbiont from Haementeria officinalis, first of a glossiphoniid leech. This as-yet-unnamed endosymbiont belongs to the Gammaproteobacteria, has a pleomorphic shape and is restricted to bacteriocytes. For this bacterial endosymbiont, we propose the name Candidatus Providencia siddallii. This symbiont possesses a highly reduced genome with high A+T content and a reduced set of metabolic capabilities, all of which are common characteristics of ancient obligate endosymbionts of arthropods. Its genome has retained many pathways related to the biosynthesis of B-vitamins, pointing toward a role in supplementing the blood-restricted diet of its host. Through comparative genomics against the endosymbionts of A. americanum, Glossina flies, and P. humanus corporis, we were able to detect a high degree of metabolic convergence among these four very distantly related endosymbiotic bacteria. PMID:26454017
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The Life of a Sponge in a Sandy Lagoon.
Ilan, M; Abelson, A
1995-12-01
Infaunal soft-bottom invertebrates benefit from the presence of sediment, but sedimentation is potentially harmful for hard-bottom dwellers. Most sponges live on hard bottom, but on coral reefs in the Red Sea, the species Biemna ehrenbergi (Keller, 1889) is found exclusively in soft-bottom lagoons, usually in the shallowest part. This location is a sink environment, which increases the deposition of particulate organic matter. Most of the sponge body is covered by sediment, but the chimney-like siphons protrude from the sediment surface. The sponge is attached to the buried beach-rock, which reduces the risk of dislodgment during storms. Dye injected above and into the sediment revealed, for the first time, a sponge pumping interstitial water (rich with particles and nutrients) into its aquiferous system. Visual examination of plastic replicas of the aquiferous system and electron microscopical analysis of sponge tissue revealed that the transcellular ostia are mostly located on the buried surface of the sponge. The oscula, however, are located on top of the siphons; their elevated position and their ability to close combine to prevent the filtering system outflow from clogging. The transcellular ostia presumably remain open due to cellular mobility. The sponge maintains a large population of bacteriocytes, which contains bacteria of several different species. Some of these bacteria disintegrate, and may be consumed by the sponge.
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How to get into bones: proton pump and carbonic anhydrase in Osedax boneworms
Tresguerres, Martin; Katz, Sigrid; Rouse, Greg W.
2013-01-01
Osedax are gutless siboglinid worms that thrive on vertebrate bones lying on the ocean floor, mainly those of whales. The posterior body of female Osedax penetrates into the bone forming extensions known as ‘roots’, which host heterotrophic symbiotic bacteria in bacteriocytes beneath the epidermis. The Osedax root epithelium presumably absorbs bone collagen and/or lipids, which are metabolized by the symbiotic bacteria that in turn serve for Osedax's nutrition. Here, we show that Osedax roots express extremely high amounts of vacuolar-H+-ATPase (VHA), which is located in the apical membrane and in cytoplasmic vesicles of root and ovisac epithelial cells. The enzyme carbonic anhydrase (CA), which catalyses the hydration of CO2 into H+ and HCO3−, is also expressed in roots and throughout Osedax body. These results suggest Osedax roots have massive acid-secreting capacity via VHA, fuelled by H+ derived from the CA-catalysed hydration of CO2 produced by aerobic metabolism. We propose the secreted acid dissolves the bone carbonate matrix to then allow the absorption of bone-derived nutrients across the skin. In an exciting example of convergent evolution, this model for acid secretion is remarkably similar to mammalian osteoclast cells. However, while osteoclasts dissolve bone for repairing and remodelling, the Osedax root epithelium secretes acid to dissolve foreign bone to access nutrients. PMID:23760644
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Betcher, Meghan A; Fung, Jennifer M; Han, Andrew W; O'Connor, Roberta; Seronay, Romell; Concepcion, Gisela P; Distel, Daniel L; Haygood, Margo G
2012-01-01
Marine bivalves of the family Teredinidae (shipworms) are voracious consumers of wood in marine environments. In several shipworm species, dense communities of intracellular bacterial endosymbionts have been observed within specialized cells (bacteriocytes) of the gills (ctenidia). These bacteria are proposed to contribute to digestion of wood by the host. While the microbes of shipworm gills have been studied extensively in several species, the abundance and distribution of microbes in the digestive system have not been adequately addressed. Here we use Fluorescence In-Situ Hybridization (FISH) and laser scanning confocal microscopy with 16S rRNA directed oligonucleotide probes targeting all domains, domains Bacteria and Archaea, and other taxonomic groups to examine the digestive microbiota of 17 specimens from 5 shipworm species (Bankia setacea, Lyrodus pedicellatus, Lyrodus massa, Lyrodus sp. and Teredo aff. triangularis). These data reveal that the caecum, a large sac-like appendage of the stomach that typically contains large quantities of wood particles and is considered the primary site of wood digestion, harbors only very sparse microbial populations. However, a significant number of bacterial cells were observed in fecal pellets within the intestines. These results suggest that due to low abundance, bacteria in the caecum may contribute little to lignocellulose degradation. In contrast, the comparatively high population density of bacteria in the intestine suggests a possible role for intestinal bacteria in the degradation of lignocellulose.
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Takaki, Yoshihiro; Chikaraishi, Yoshito; Ikuta, Tetsuro; Ozawa, Genki; Yoshida, Takao; Ohkouchi, Naohiko; Fujikura, Katsunori
2017-01-01
Sterols are key cyclic triterpenoid lipid components of eukaryotic cellular membranes, which are synthesized through complex multi-enzyme pathways. Similar to most animals, Bathymodiolus mussels, which inhabit deep-sea chemosynthetic ecosystems and harbor methanotrophic and/or thiotrophic bacterial endosymbionts, possess cholesterol as their main sterol. Based on the stable carbon isotope analyses, it has been suggested that host Bathymodiolus mussels synthesize cholesterol using a sterol intermediate derived from the methanotrophic endosymbionts. To test this hypothesis, we sequenced the genome of the methanotrophic endosymbiont in Bathymodiolus platifrons. The genome sequence data demonstrated that the endosymbiont potentially generates up to 4,4-dimethyl-cholesta-8,14,24-trienol, a sterol intermediate in cholesterol biosynthesis, from methane. In addition, transcripts for a subset of the enzymes of the biosynthetic pathway to cholesterol downstream from a sterol intermediate derived from methanotroph endosymbionts were detected in our transcriptome data for B. platifrons. These findings suggest that this mussel can de novo synthesize cholesterol from methane in cooperation with the symbionts. By in situ hybridization analyses, we showed that genes associated with cholesterol biosynthesis from both host and endosymbionts were expressed exclusively in the gill epithelial bacteriocytes containing endosymbionts. Thus, cholesterol production is probably localized within these specialized cells of the gill. Considering that the host mussel cannot de novo synthesize cholesterol and depends largely on endosymbionts for nutrition, the capacity of endosymbionts to synthesize sterols may be important in establishing symbiont–host relationships in these chemosynthetic mussels. PMID:28453654
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Brumin, Marina; Levy, Maggie
2012-01-01
The whitefly Bemisia tabaci is a cosmopolitan insect pest that harbors Portiera aleyrodidarum, the primary obligatory symbiotic bacterium, and several facultative secondary symbionts. Secondary symbionts in B. tabaci are generally associated with the bacteriome, ensuring their vertical transmission; however, Rickettsia is an exception and occupies most of the body cavity, except the bacteriome. The mode of Rickettsia transfer between generations and its subcellular localization in insect organs have not been investigated. Using electron and fluorescence microscopy, we show that Rickettsia infects the digestive, salivary, and reproductive organs of the insect; however, it was not observed in the bacteriome. Rickettsia invades the oocytes during early developmental stages and resides in follicular cells and cytoplasm; it is mostly excluded when the egg matures; however, some bacterial cells remain in the egg, ensuring their transfer to subsequent generations. Rickettsia was localized to testicles and the spermatheca, suggesting a horizontal transfer between males and females during mating. The bacterium was further observed at large amounts in midgut cells, concentrating in vacuole-like structures, and was located in the hemolymph, specifically at exceptionally large amounts around bacteriocytes and in fat bodies. Organs further infected by Rickettsia included the primary salivary glands and stylets, sites of possible secretion of the bacterium outside the whitefly body. The close association between Rickettsia and the B. tabaci digestive system might be important for digestive purposes. The vertical transmission of Rickettsia to subsequent generations occurs via the oocyte and not, like other secondary symbionts, the bacteriome. PMID:22660706
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Manzano-Marín, Alejandro; Oceguera-Figueroa, Alejandro; Latorre, Amparo; Jiménez-García, Luis F; Moya, Andres
2015-10-09
Endosymbiosis is a common phenomenon in nature, especially between bacteria and insects, whose typically unbalanced diets are usually complemented by their obligate endosymbionts. While much interest and focus has been directed toward phloem-feeders like aphids and mealybugs, blood-feeders such as the Lone star tick (Amblyomma americanum), Glossina flies, and the human body louse (Pediculus humanus corporis) depend on obligate endosymbionts which complement their B-vitamin-deficient diets, and thus are required for growth and survival. Glossiphoniid leeches have also been found to harbor distinct endosymbionts housed in specialized organs. Here, we present the genome of the bacterial endosymbiont from Haementeria officinalis, first of a glossiphoniid leech. This as-yet-unnamed endosymbiont belongs to the Gammaproteobacteria, has a pleomorphic shape and is restricted to bacteriocytes. For this bacterial endosymbiont, we propose the name Candidatus Providencia siddallii. This symbiont possesses a highly reduced genome with high A+T content and a reduced set of metabolic capabilities, all of which are common characteristics of ancient obligate endosymbionts of arthropods. Its genome has retained many pathways related to the biosynthesis of B-vitamins, pointing toward a role in supplementing the blood-restricted diet of its host. Through comparative genomics against the endosymbionts of A. americanum, Glossina flies, and P. humanus corporis, we were able to detect a high degree of metabolic convergence among these four very distantly related endosymbiotic bacteria. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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Hosokawa, Takahiro; Nikoh, Naruo; Koga, Ryuichi; Satô, Masahiko; Tanahashi, Masahiko; Meng, Xian-Ying; Fukatsu, Takema
2012-01-01
Bat flies of the family Nycteribiidae are known for their extreme morphological and physiological traits specialized for ectoparasitic blood-feeding lifestyle on bats, including lack of wings, reduced head and eyes, adenotrophic viviparity with a highly developed uterus and milk glands, as well as association with endosymbiotic bacteria. We investigated Japanese nycteribiid bat flies representing 4 genera, 8 species and 27 populations for their bacterial endosymbionts. From all the nycteribiid species examined, a distinct clade of gammaproteobacteria was consistently detected, which was allied to endosymbionts of other insects such as Riesia spp. of primate lice and Arsenophonus spp. of diverse insects. In adult insects, the endosymbiont was localized in specific bacteriocytes in the abdomen, suggesting an intimate host–symbiont association. In adult females, the endosymbiont was also found in the cavity of milk gland tubules, which suggests uterine vertical transmission of the endosymbiont to larvae through milk gland secretion. In adult females of Penicillidia jenynsii, we discovered a previously unknown type of symbiotic organ in the Nycteribiidae: a pair of large bacteriomes located inside the swellings on the fifth abdominal ventral plate. The endosymbiont genes consistently exhibited adenine/thymine biased nucleotide compositions and accelerated rates of molecular evolution. The endosymbiont genome was estimated to be highly reduced, ∼0.76 Mb in size. The endosymbiont phylogeny perfectly mirrored the host insect phylogeny, indicating strict vertical transmission and host–symbiont co-speciation in the evolutionary course of the Nycteribiidae. The designation ‘Candidatus Aschnera chinzeii' is proposed for the endosymbiont clade. PMID:21938025
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Caro, Audrey; Gros, Olivier; Got, Patrice; De Wit, Rutger; Troussellier, Marc
2007-01-01
We investigated the characteristics of the sulfur-oxidizing symbiont hosted in the gills of Codakia orbicularis, a bivalve living in shallow marine tropical environments. Special attention was paid to describing the heterogeneity of the population by using single-cell approaches including flow cytometry (FCM) and different microscopic techniques and by analyzing a cell size fractionation experiment. Up to seven different subpopulations were distinguished by FCM based on nucleic acid content and light side scattering of the cells. The cell size analysis of symbionts showed that the symbiotic population was very heterogeneous in size, i.e., ranging from 0.5 to 5 μm in length, with variable amounts of intracellular sulfur. The side-scatter signal analyzed by FCM, which is often taken as a proxy of cell size, was greatly influenced by the sulfur content of the symbionts. FCM revealed an important heterogeneity in the relative nucleic acid content among the subclasses. The larger cells contained exceptionally high levels of nucleic acids, suggesting that these cells contained multiple copies of their genome, i.e., ranging from one copy for the smaller cells to more than four copies for the larger cells. The proportion of respiring symbionts (5-cyano-2,3-ditolyl-terazolium chloride positive) in the bacteriocytes of Codakia revealed that around 80% of the symbionts hosted by Codakia maintain respiratory activity throughout the year. These data allowed us to gain insight into the functioning of the symbionts within the host and to propose some hypotheses on how the growth of the symbionts is controlled by the host. PMID:17259363
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Opatovsky, Itai; Santos-Garcia, Diego; Ruan, Zhepu; Lahav, Tamar; Ofaim, Shany; Mouton, Laurence; Barbe, Valérie; Jiang, Jiandong; Zchori-Fein, Einat; Freilich, Shiri
2018-05-25
Individual organisms are linked to their communities and ecosystems via metabolic activities. Metabolic exchanges and co-dependencies have long been suggested to have a pivotal role in determining community structure. In phloem-feeding insects such metabolic interactions with bacteria enable complementation of their deprived nutrition. The phloem-feeding whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) harbors an obligatory symbiotic bacterium, as well as varying combinations of facultative symbionts. This well-defined bacterial community in B. tabaci serves here as a case study for a comprehensive and systematic survey of metabolic interactions within the bacterial community and their associations with documented occurrences of bacterial combinations. We first reconstructed the metabolic networks of five common B. tabaci symbionts genera (Portiera, Rickettsia, Hamiltonella, Cardinium and Wolbachia), and then used network analysis approaches to predict: (1) species-specific metabolic capacities in a simulated bacteriocyte-like environment; (2) metabolic capacities of the corresponding species' combinations, and (3) dependencies of each species on different media components. The predictions for metabolic capacities of the symbionts in the host environment were in general agreement with previously reported genome analyses, each focused on the single-species level. The analysis suggests several previously un-reported routes for complementary interactions and estimated the dependency of each symbiont in specific host metabolites. No clear association was detected between metabolic co-dependencies and co-occurrence patterns. The analysis generated predictions for testable hypotheses of metabolic exchanges and co-dependencies in bacterial communities and by crossing them with co-occurrence profiles, contextualized interaction patterns into a wider ecological perspective.
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Manzano-Marín, Alejandro; Simon, Jean-Christophe; Latorre, Amparo
2016-01-01
Virtually all aphids (Aphididae) harbor Buchnera aphidicola as an obligate endosymbiont to compensate nutritional deficiencies arising from their phloem diet. Many species within the Lachninae subfamily seem to be consistently associated also with Serratia symbiotica. We have previously shown that both Cinara (Cinara) cedri and Cinara (Cupressobium) tujafilina (Lachninae: Eulachnini tribe) have indeed established co-obligate associations with both Buchnera and S. symbiotica. However, while Buchnera genomes of both Cinara species are similar, genome degradation differs greatly between the two S. symbiotica strains. To gain insight into the essentiality and degree of integration of S. symbiotica within the Lachninae, we sequenced the genome of both Buchnera and S. symbiotica endosymbionts from the distantly related aphid Tuberolachnus salignus (Lachninae: Tuberolachnini tribe). We found a striking level of similarity between the endosymbiotic system of this aphid and that of C. cedri. In both aphid hosts, S. symbiotica possesses a highly reduced genome and is found exclusively intracellularly inside bacteriocytes. Interestingly, T. salignus’ endosymbionts present the same tryptophan biosynthetic metabolic complementation as C. cedri’s, which is not present in C. tujafilina’s. Moreover, we corroborate the riboflavin-biosynthetic-role take-over/rescue by S. symbiotica in T. salignus, and therefore, provide further evidence for the previously proposed establishment of a secondary co-obligate endosymbiont in the common ancestor of the Lachninae aphids. Finally, we propose that the putative convergent split of the tryptophan biosynthetic role between Buchnera and S. symbiotica could be behind the establishment of S. symbiotica as an obligate intracellular symbiont and the triggering of further genome degradation. PMID:27190007
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Synergistic activity of antibiotics combined with ivermectin to kill body lice.
Sangaré, Abdoul Karim; Rolain, Jean Marc; Gaudart, Jean; Weber, Pascal; Raoult, Didier
2016-03-01
Ivermectin and doxycycline have been found to be independently effective in killing body lice. In this study, 450 body lice were artificially fed on a Parafilm™ membrane with human blood associated with antibiotics (doxycycline, erythromycin, rifampicin and azithromycin) alone and in combination with ivermectin. Fluorescence in situ hybridisation and spectral deconvolution were performed to evaluate bacterial transcriptional activity following antibiotic intake by the lice. In the first series, a lethal effect of antibiotics on lice was observed compared with the control group at 18 days (log-rank test, P≤10(-3)), with a significant difference between groups in the production of nits (P=0.019, Kruskal-Wallis test). A high lethal effect of ivermectin alone (50ng/mL) was observed compared with the control group (log-rank test, P≤10(-3)). Fluorescence of bacteriocytes in lice treated with 20μg/mL doxycycline was lower than in untreated lice (P<0.0001, Kruskal-Wallis test). In the second series with antibiotic-ivermectin combinations, a synergistic lethal effect on treated lice (log-rank test, P<10(-6)) was observed compared with the control group at 18 days, associated with a significant decrease in the production of nits (P≤0.001, Kruskal-Wallis test). Additionally, survival of lice in the combination treatment groups compared with ivermectin alone was significant (log-rank test, P=0.0008). These data demonstrate that the synergistic effect of combinations of antibiotics and ivermectin could be used to achieve complete eradication of lice and to avoid selection of a resistant louse population. Copyright © 2016 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.
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Endosymbiotic Microbiota of the Bamboo Pseudococcid Antonina crawii (Insecta, Homoptera)
Fukatsu, Takema; Nikoh, Naruo
2000-01-01
We characterized the intracellular symbiotic microbiota of the bamboo pseudococcid Antonina crawii by performing a molecular phylogenetic analysis in combination with in situ hybridization. Almost the entire length of the bacterial 16S rRNA gene was amplified and cloned from A. crawii whole DNA. Restriction fragment length polymorphism analysis revealed that the clones obtained included three distinct types of sequences. Nucleotide sequences of the three types were determined and subjected to a molecular phylogenetic analysis. The first sequence was a member of the γ subdivision of the division Proteobacteria (γ-Proteobacteria) to which no sequences in the database were closely related, although the sequences of endosymbionts of other homopterans, such as psyllids and aphids, were distantly related. The second sequence was a β-Proteobacteria sequence and formed a monophyletic group with the sequences of endosymbionts from other pseudococcids. The third sequence exhibited a high level of similarity to sequences of Spiroplasma spp. from ladybird beetles and a tick. Localization of the endosymbionts was determined by using tissue sections of A. crawii and in situ hybridization with specific oligonucleotide probes. The γ- and β-Proteobacteria symbionts were packed in the cytoplasm of the same mycetocytes (or bacteriocytes) and formed a large mycetome (or bacteriome) in the abdomen. The spiroplasma symbionts were also present intracellularly in various tissues at a low density. We observed that the anterior poles of developing eggs in the ovaries were infected by the γ- and β-Proteobacteria symbionts in a systematic way, which ensured vertical transmission. Five representative pseudococcids were examined by performing diagnostic PCR experiments with specific primers; the β-Proteobacteria symbiont was detected in all five pseudococcids, the γ-Proteobacteria symbiont was found in three, and the spiroplasma symbiont was detected only in A. crawii. PMID:10653730
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Han, Andrew W.; Sandy, Moriah; Fishman, Brian; Trindade-Silva, Amaro E.; Soares, Carlos A. G.; Distel, Daniel L.; Butler, Alison; Haygood, Margo G.
2013-01-01
Shipworms are marine bivalve mollusks (Family Teredinidae) that use wood for shelter and food. They harbor a group of closely related, yet phylogenetically distinct, bacterial endosymbionts in bacteriocytes located in the gills. This endosymbiotic community is believed to support the host's nutrition in multiple ways, through the production of cellulolytic enzymes and the fixation of nitrogen. The genome of the shipworm endosymbiont Teredinibacter turnerae T7901 was recently sequenced and in addition to the potential for cellulolytic enzymes and diazotrophy, the genome also revealed a rich potential for secondary metabolites. With nine distinct biosynthetic gene clusters, nearly 7% of the genome is dedicated to secondary metabolites. Bioinformatic analyses predict that one of the gene clusters is responsible for the production of a catecholate siderophore. Here we describe this gene cluster in detail and present the siderophore product from this cluster. Genes similar to the entCEBA genes of enterobactin biosynthesis involved in the production and activation of dihydroxybenzoic acid (DHB) are present in this cluster, as well as a two-module non-ribosomal peptide synthetase (NRPS). A novel triscatecholate siderophore, turnerbactin, was isolated from the supernatant of iron-limited T. turnerae T7901 cultures. Turnerbactin is a trimer of N-(2,3-DHB)-L-Orn-L-Ser with the three monomeric units linked by Ser ester linkages. A monomer, dimer, dehydrated dimer, and dehydrated trimer of 2,3-DHB-L-Orn-L-Ser were also found in the supernatant. A link between the gene cluster and siderophore product was made by constructing a NRPS mutant, TtAH03. Siderophores could not be detected in cultures of TtAH03 by HPLC analysis and Fe-binding activity of culture supernatant was significantly reduced. Regulation of the pathway by iron is supported by identification of putative Fur box sequences and observation of increased Fe-binding activity under iron restriction. Evidence of a
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NASA Astrophysics Data System (ADS)
Powell, Eric N.; Barber, Robert D.; Kennicutt, Mahlon C., II; Ford, Susan E.
1999-12-01
Petroleum seep mussels are often exposed to high hydrocarbon concentrations in their natural habitat and, thus, offer the opportunity to examine the relationship between parasitism, disease and contaminant exposure under natural conditions. This is the first report on the histopathology of cold-seep mussels. Seep mussels were collected by submersible from four primary sites in the Gulf of Mexico, lease blocks Green Canyon (GC) 184, GC-234, GC-233, and Garden Banks 425 in 550-650 m water depth. Five types of parasites were identified in section: (1) gill "rosettes" of unknown affinity associated with the gill bacteriocytes, (2) gill "inclusions" similar to chlamydia/rickettsia inclusions, (3) extracellular gill ciliates, (4) body "inclusions" that also resemble chlamydial/rickettsial inclusions, and (5) Bucephalus-like trematodes. Comparison to shallow-water mytilids demonstrates that: (1) both have similar parasite faunas; (2) seep mytilids are relatively heavily parasitized; and (3) infection intensities are extremely high in comparison to shallow-water mytilids for Bucephalus and chlamydia/rickettsia. In this study, the lowest prevalence for chlamydia/rickettsia was 67%. Prevalences of 100% were recorded from three populations. Bucephalus prevalence was ⩾70% in three of 10 populations. The parasite fauna was highly variable between populations. Some important parasites were not observed in some primary sites. Even within primary sites, some important parasites were not observed in some populations. Bucephalus may exert a significant influence on seep mussel population dynamics. Forty percent of the populations in this study are severely reproductively compromised by Bucephalus infection. Only a fraction of petroleum seep mussel populations are maintaining the entire beta-level population structure of this species. Variation in two parasites, gill ciliates and Bucephalus, explained most of the variation in PAH body burden between mussel populations. PAHs are
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NASA Astrophysics Data System (ADS)
Zielinski, F.; Pape, T.; Wenzhöfer, F.; Seifert, R.; Dubilier, N.
2005-12-01
The ultramafic hosted Logatchev hydrothermal vent field at the slow spreading Mid-Atlantic Ridge (MAR) exhibits unusually high hydrogen concentrations due to serpentinization of ultramafic rocks. Endmember H2-concentrations here have been calculated to be as high as 12 mM which is significantly higher than at most other vent sites along the MAR. Hydrogen is a potential energy source for bacteria providing an energy yield of roughly 240 kJ/mol if oxidized with oxygen. Hence, the energy yield is even higher than for conventional aerobic respiration which liberates 220 kJ/mol. The ability to use H2 as an energy source has been shown for a variety of free-living bacteria. However, to date no other energy sources besides methane and sulfide have been identified for vent (or seep) symbionts. Here we show that H2 is consumed by endosymbiotic bacteria of the Logatchev vent mussel Bathymodiolus puteoserpentis. B. puteoserpentis is known to live in dual symbiosis with methane- and sulfide-oxidizing bacteria that occur intracellularly in specialized gill cells called bacteriocytes. The methanotrophic symbionts use methane as both an energy and carbon source whereas the thiotrophic symbionts use H2S as an energy and dissolved CO2 as a carbon source. Hydrothermal fluids carrying methane and sulfide provide the energy for the bacteria and the bacteria in turn provide the mussel with carbon compounds. The mussel on the other hand supplies its symbionts with a constant fluid flow and, by hosting them offers an ideal ecological niche. Freshly dissected gill pieces of B. puteoserpentis incubated in chilled sea water containing hydrogen gas readily consumed H2. The consumption of H2 over time was significantly higher in gill tissues than in symbiont-free mussel tissue indicating that the symbiotic bacteria are responsible for the observed activity. H2-consumption rates were similar in mussels from two different sampling sites, Irina II: 37 nmol h-1 (ml gill)-1 and Quest: 31 nmol h-1