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Takema Fukatsu - One of the best experts on this subject based on the ideXlab platform.
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Diversity and evolution of bacterial Symbionts in the gut symbiotic organ of jewel stinkbugs (Hemiptera: Scutelleridae)
Applied Entomology and Zoology, 2019Co-Authors: Takahiro Hosokawa, Ryuichi Koga, Megumi Imanishi, Takema FukatsuAbstract:The majority of plant-sucking stinkbugs of the superfamily Pentatomoidea possess numerous crypts in the midgut as the symbiotic organ, where specific and beneficial symbiotic bacteria are harbored extracellularly. The host–Symbiont relationships are co-speciating in the families Plataspidae, Acanthosomatidae and Urostylididae, but promiscuous in the families Pentatomidae and Cydnidae. As for the family Scutelleridae, only a few species have been examined for their gut symbiotic bacteria. Here, we comprehensively investigated Japanese scutellerid stinkbugs representing 6 genera, 8 species, and 24 individuals. Molecular phylogenetic analysis revealed that the scutellerid gut Symbionts are polyphyletic, consisting of at least seven distinct phylogenetic groups in the Gammaproteobacteria. In four of the seven groups, the Symbionts were closely related to each other, to the pentatomid gut Symbionts, and to environmental bacteria of the genus Pantoea . These results strongly suggest that the scutellerid gut Symbionts are of multiple evolutionary origins, presumably entailing repeated Symbiont acquisitions, replacements and/or horizontal transfers in a promiscuous manner. Elimination of the gut Symbionts from Lampromicra miyakona resulted in high mortality without adult emergence, confirming that the gut Symbionts are of beneficial nature. In conclusion, the host–Symbiont associations in the Scutelleridae seem to be similar to those in the Pentatomidae and Cydnidae.
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Recurrent Symbiont recruitment from fungal parasites in cicadas
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Yu Matsuura, Xian-ying Meng, Masahiko Tanahashi, Minoru Moriyama, Piotr Łukasik, Dan Vanderpool, John P. Mccutcheon, Takema FukatsuAbstract:Diverse insects are associated with ancient bacterial Symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such Symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient Symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate Symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeast-like fungal Symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal Symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal Symbionts. Most fungal Symbionts of cicadas were uncultivable, but the fungal Symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal Symbiont replacement. Genome sequencing of the fungal Symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.
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Fungal and bacterial endoSymbionts of eared leafhoppers of the subfamily Ledrinae (Hemiptera: Cicadellidae)
Applied Entomology and Zoology, 2016Co-Authors: Takanori Nishino, Ryuichi Koga, Masahiko Tanahashi, Takema FukatsuAbstract:In general, leafhoppers (Hemiptera: Cicadellidae) possess a pair of bacteriomes in the abdomen, which harbor two types of obligate bacterial Symbionts: a very ancient Sulcia Symbiont and another ancient Nasuia -allied co-Symbiont (or a younger Baumannia co-Symbiont). However, when we inspected three eared leafhoppers of the subfamily Ledrinae, namely Ledra auditura Walker, Ledropsis discolor (Uhler) and Tituria angulata (Matsumura), L. discolor harbored only Sulcia Symbiont while L. auditura and T. angulata possessed no bacterial Symbionts. Instead, all the species possessed specialized cells full of yeast-like fungal Symbionts within fat bodies. Molecular phylogenetic analysis revealed that the fungal Symbionts are placed within the entomoparasitic fungal genus Ophiocordyceps (Ascomycota: Hypocreales: Ophiocordycipitaceae). These results suggest the possibility that (1) the fungal Symbiont was acquired in the evolutionary course of the Ledrinae, (2) the original fungus was likely an entomoparasite of the genus Ophiocordyceps , (3) the fungal Symbiont replaced the Nasuia -allied Symbiont in an ancestral lineage, and (4) even the ancient Sulcia Symbiont was finally lost and taken over by the fungal Symbiont. Meanwhile, the possibility of multiple independent fungal acquisitions from closely related entomoparasitic Ophiocordyceps fungi cannot be excluded. Our finding uncovers an evolutionary process from a prokaryotic essential symbiosis to a eukaryotic one.
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Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations
Nature Microbiology, 2016Co-Authors: Takahiro Hosokawa, Naruo Nikoh, Yoshiko Ishii, Manabu Fujie, Nori Satoh, Takema FukatsuAbstract:Bacterial Symbionts in natural populations of the stinkbug Plautia stali are undergoing an evolutionary transition from a free-living lifestyle in the environment to obligate mutualism. Diverse organisms are associated with obligate microbial mutualists. How such essential Symbionts have originated from free-living ancestors is of evolutionary interest. Here we report that, in natural populations of the stinkbug Plautia stali , obligate bacterial mutualists are evolving from environmental bacteria. Of six distinct bacterial lineages associated with insect populations, two are uncultivable with reduced genomes, four are cultivable with non-reduced genomes, one uncultivable Symbiont is fixed in temperate populations, and the other uncultivable Symbiont coexists with four cultivable Symbionts in subtropical populations. Symbiont elimination resulted in host mortality for all Symbionts, while re-infection with any of the Symbionts restored normal host growth, indicating that all the Symbionts are indispensable and almost equivalent functionally. Some aseptic newborns incubated with environmental soils acquired the cultivable Symbionts and normal growth was restored, identifying them as environmental Pantoea spp. Our finding uncovers an evolutionary transition from a free-living lifestyle to obligate mutualism that is currently ongoing in nature.
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Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)
Applied and environmental microbiology, 2014Co-Authors: Yu Matsuura, Takahiro Hosokawa, Mario Serracin, Genet M. Tulgetske, Thomas A. Miller, Takema FukatsuAbstract:ABSTRACT Stinkbugs of the genus Antestiopsis, so-called antestia bugs or variegated coffee bugs, are notorious pests of coffee plants in Africa. We investigated the symbiotic bacteria associated with Antestiopsis thunbergii, a major coffee plant pest in Rwanda. PCR, cloning, sequencing, and phylogenetic analysis of bacterial genes identified four distinct bacterial lineages associated with A. thunbergii: a gammaproteobacterial gut Symbiont and Symbionts representing the genera Sodalis, Spiroplasma, and Rickettsia. In situ hybridization showed that the gut Symbiont densely occupied the lumen of midgut crypts, whereas the Sodalis Symbiont, the Spiroplasma Symbiont, and the Rickettsia Symbiont sparsely and sporadically infected various cells and tissues. Diagnostic PCR survey of 154 A. thunbergii individuals collected at 8 localities in Rwanda revealed high infection frequencies (100% for the gut Symbiont, 51.3% for the Sodalis Symbiont, 52.6% for the Spiroplasma Symbiont, and 24.0% for the Rickettsia Symbiont). These results suggest that the gut Symbiont is the primary symbiotic associate of obligate nature for A. thunbergii, whereas the Sodalis Symbiont, the Spiroplasma Symbiont, and the Rickettsia Symbiont are the secondary symbiotic associates of facultative nature. We observed high coinfection frequencies, i.e., 7.8% of individuals with quadruple infection with all the Symbionts, 32.5% with triple infections with the gut Symbiont and two of the secondary Symbionts, and 39.6% with double infections with the gut Symbiont and any of the three secondary Symbionts, which were statistically not different from the expected coinfection frequencies and probably reflected random associations. The knowledge of symbiotic microbiota in A. thunbergii will provide useful background information for controlling this devastating coffee plant pest.
Dörte Becher - One of the best experts on this subject based on the ideXlab platform.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host–Symbiont interactions
The ISME Journal, 2020Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host–microbe associations. However, how host–Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus , hosting a thiotrophic Symbiont, and Atlantic B. azoricus , containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host–microbe interactions can be quite variable, even between closely related systems.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host-Symbiont interactions.
The ISME journal, 2019Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host-microbe associations. However, how host-Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic Symbiont, and Atlantic B. azoricus, containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host-microbe interactions can be quite variable, even between closely related systems.
Takahiro Hosokawa - One of the best experts on this subject based on the ideXlab platform.
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Diversity and evolution of bacterial Symbionts in the gut symbiotic organ of jewel stinkbugs (Hemiptera: Scutelleridae)
Applied Entomology and Zoology, 2019Co-Authors: Takahiro Hosokawa, Ryuichi Koga, Megumi Imanishi, Takema FukatsuAbstract:The majority of plant-sucking stinkbugs of the superfamily Pentatomoidea possess numerous crypts in the midgut as the symbiotic organ, where specific and beneficial symbiotic bacteria are harbored extracellularly. The host–Symbiont relationships are co-speciating in the families Plataspidae, Acanthosomatidae and Urostylididae, but promiscuous in the families Pentatomidae and Cydnidae. As for the family Scutelleridae, only a few species have been examined for their gut symbiotic bacteria. Here, we comprehensively investigated Japanese scutellerid stinkbugs representing 6 genera, 8 species, and 24 individuals. Molecular phylogenetic analysis revealed that the scutellerid gut Symbionts are polyphyletic, consisting of at least seven distinct phylogenetic groups in the Gammaproteobacteria. In four of the seven groups, the Symbionts were closely related to each other, to the pentatomid gut Symbionts, and to environmental bacteria of the genus Pantoea . These results strongly suggest that the scutellerid gut Symbionts are of multiple evolutionary origins, presumably entailing repeated Symbiont acquisitions, replacements and/or horizontal transfers in a promiscuous manner. Elimination of the gut Symbionts from Lampromicra miyakona resulted in high mortality without adult emergence, confirming that the gut Symbionts are of beneficial nature. In conclusion, the host–Symbiont associations in the Scutelleridae seem to be similar to those in the Pentatomidae and Cydnidae.
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Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations
Nature Microbiology, 2016Co-Authors: Takahiro Hosokawa, Naruo Nikoh, Yoshiko Ishii, Manabu Fujie, Nori Satoh, Takema FukatsuAbstract:Bacterial Symbionts in natural populations of the stinkbug Plautia stali are undergoing an evolutionary transition from a free-living lifestyle in the environment to obligate mutualism. Diverse organisms are associated with obligate microbial mutualists. How such essential Symbionts have originated from free-living ancestors is of evolutionary interest. Here we report that, in natural populations of the stinkbug Plautia stali , obligate bacterial mutualists are evolving from environmental bacteria. Of six distinct bacterial lineages associated with insect populations, two are uncultivable with reduced genomes, four are cultivable with non-reduced genomes, one uncultivable Symbiont is fixed in temperate populations, and the other uncultivable Symbiont coexists with four cultivable Symbionts in subtropical populations. Symbiont elimination resulted in host mortality for all Symbionts, while re-infection with any of the Symbionts restored normal host growth, indicating that all the Symbionts are indispensable and almost equivalent functionally. Some aseptic newborns incubated with environmental soils acquired the cultivable Symbionts and normal growth was restored, identifying them as environmental Pantoea spp. Our finding uncovers an evolutionary transition from a free-living lifestyle to obligate mutualism that is currently ongoing in nature.
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Bacterial Symbionts of a Devastating Coffee Plant Pest, the Stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae)
Applied and environmental microbiology, 2014Co-Authors: Yu Matsuura, Takahiro Hosokawa, Mario Serracin, Genet M. Tulgetske, Thomas A. Miller, Takema FukatsuAbstract:ABSTRACT Stinkbugs of the genus Antestiopsis, so-called antestia bugs or variegated coffee bugs, are notorious pests of coffee plants in Africa. We investigated the symbiotic bacteria associated with Antestiopsis thunbergii, a major coffee plant pest in Rwanda. PCR, cloning, sequencing, and phylogenetic analysis of bacterial genes identified four distinct bacterial lineages associated with A. thunbergii: a gammaproteobacterial gut Symbiont and Symbionts representing the genera Sodalis, Spiroplasma, and Rickettsia. In situ hybridization showed that the gut Symbiont densely occupied the lumen of midgut crypts, whereas the Sodalis Symbiont, the Spiroplasma Symbiont, and the Rickettsia Symbiont sparsely and sporadically infected various cells and tissues. Diagnostic PCR survey of 154 A. thunbergii individuals collected at 8 localities in Rwanda revealed high infection frequencies (100% for the gut Symbiont, 51.3% for the Sodalis Symbiont, 52.6% for the Spiroplasma Symbiont, and 24.0% for the Rickettsia Symbiont). These results suggest that the gut Symbiont is the primary symbiotic associate of obligate nature for A. thunbergii, whereas the Sodalis Symbiont, the Spiroplasma Symbiont, and the Rickettsia Symbiont are the secondary symbiotic associates of facultative nature. We observed high coinfection frequencies, i.e., 7.8% of individuals with quadruple infection with all the Symbionts, 32.5% with triple infections with the gut Symbiont and two of the secondary Symbionts, and 39.6% with double infections with the gut Symbiont and any of the three secondary Symbionts, which were statistically not different from the expected coinfection frequencies and probably reflected random associations. The knowledge of symbiotic microbiota in A. thunbergii will provide useful background information for controlling this devastating coffee plant pest.
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Gut symbiotic bacteria in the cabbage bugs Eurydema rugosa and Eurydema dominulus (Heteroptera: Pentatomidae)
Applied Entomology and Zoology, 2012Co-Authors: Yoshitomo Kikuchi, Naruo Nikoh, Takahiro Hosokawa, Takema FukatsuAbstract:The cabbage bugs Eurydema rugosa Motschulsky and Eurydema dominulus (Scopoli) (Heteroptera: Pentatomidae: Strachiini) possess a number of crypts in a posterior region of the midgut, which are filled with bacterial Symbiont cells. Here we characterized the gut Symbionts of Eurydema stinkbugs using molecular phylogenetic and histological techniques. Specific gammaproteobacteria were consistently identified from the posterior midgut of E. rugosa representing nine populations and E. dominulus representing six populations, respectively. The bacterial 16S rRNA gene sequences were identical within the species but slightly different (98.2% sequence identity) between the species. Molecular phylogenetic analysis revealed that the Eurydema Symbionts formed a well-defined monophyletic group in the Gammaproteobacteria . The Symbionts were phylogenetically distinct from the gut Symbionts of the stinkbug families Acanthosomatidae, Plataspidae, Parastrachiidae, Scutelleridae, and other pentatomid species, suggesting multiple evolutionary origins of the gut symbiotic bacteria among diverse stinkbugs. In situ hybridization confirmed that the Symbiont is located in the cavity of the midgut crypts. Aposymbiotic insects of E. rugosa, which were produced by egg surface sterilization, were viable but suffered retarded growth, reduced body weight, and abnormal body color, suggesting the biological importance of the Symbiont for the host.
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an ancient but promiscuous host Symbiont association between burkholderia gut Symbionts and their heteropteran hosts
The ISME Journal, 2011Co-Authors: Yoshitomo Kikuchi, Takahiro Hosokawa, Takema FukatsuAbstract:Here, we investigated 124 stinkbug species representing 20 families and 5 superfamilies for their Burkholderia gut Symbionts, of which 39 species representing 6 families of the superfamilies Lygaeoidea and Coreoidea were Burkholderia-positive. Diagnostic PCR surveys revealed high frequencies of Burkholderia infection in natural populations of the stinkbugs, and substantial absence of vertical transmission of Burkholderia infection to their eggs. In situ hybridization confirmed localization of the Burkholderia in their midgut crypts. In the lygaeoid and coreoid stinkbugs, development of midgut crypts in their alimentary tract was coincident with the Burkholderia infection, suggesting that the specialized morphological configuration is pivotal for establishment and maintenance of the symbiotic association. The Burkholderia Symbionts were easily isolated as pure culture on standard microbiological media, indicating the ability of the gut Symbionts to survive outside the host insects. Molecular phylogenetic analysis showed that the gut Symbionts of the lygaeoid and coreoid stinkbugs belong to a β-proteobacterial clade together with Burkholderia isolates from soil environments and Burkholderia species that induce plant galls. On the phylogeny, the stinkbug-associated, environmental and gall-forming Burkholderia strains did not form coherent groups, indicating host–Symbiont promiscuity among these stinkbugs. Symbiont culturing revealed that slightly different Burkholderia genotypes often coexist in the same insects, which is also suggestive of host–Symbiont promiscuity. All these results strongly suggest an ancient but promiscuous host–Symbiont relationship between the lygaeoid/coreoid stinkbugs and the Burkholderia gut Symbionts. Possible mechanisms as to how the environmentally transmitted promiscuous symbiotic association has been stably maintained in the evolutionary course are discussed.
Horst Felbeck - One of the best experts on this subject based on the ideXlab platform.
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Metabolic differences between Symbiont subpopulations in the deep-sea tubeworm Riftia pachyptila
2020Co-Authors: Tjorven Hinzke, Horst Felbeck, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Mareike Meister, Jan Pané-farré, Petra Hildebrandt, Florian BonnAbstract:AbstractThe hydrothermal vent tube worm Riftia pachyptila lives in intimate symbiosis with intracellular sulfur-oxidizing gammaproteobacteria. Although the Symbiont population consists of a single 16S rRNA phylotype, bacteria in the same host animal exhibit a remarkable degree of metabolic diversity: They simultaneously utilize two carbon fixation pathways and various energy sources and electron acceptors. Whether these multiple metabolic routes are employed in the same Symbiont cells, or rather in distinct Symbiont subpopulations, was unclear. As Riftia Symbionts vary considerably in cell size and shape, we enriched individual Symbiont cell sizes by density gradient centrifugation in order to test whether Symbiont cells of different sizes show different metabolic profiles. Metaproteomic analysis and statistical evaluation using clustering and random forests, supported by microscopy and flow cytometry, strongly suggest that Riftia Symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: Small Symbionts actively divide and may establish cellular Symbiont-host interaction, as indicated by highest abundance of the cell division key protein FtsZ and highly abundant chaperones and porins in this initial phase. Large Symbionts, on the other hand, apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Highest abundance of enzymes for CO2 fixation, carbon storage and biosynthesis in large Symbionts indicates that in this late differentiation stage the Symbiont’s metabolism is efficiently geared towards the production of organic material. We propose that this division of labor between smaller and larger Symbionts benefits the productivity of the symbiosis as a whole.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host–Symbiont interactions
The ISME Journal, 2020Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host–microbe associations. However, how host–Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus , hosting a thiotrophic Symbiont, and Atlantic B. azoricus , containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host–microbe interactions can be quite variable, even between closely related systems.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host-Symbiont interactions.
The ISME journal, 2019Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host-microbe associations. However, how host-Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic Symbiont, and Atlantic B. azoricus, containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host-microbe interactions can be quite variable, even between closely related systems.
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A histidine protein kinase homolog from the endoSymbiont of the hydrothermal vent tubeworm Riftia pachyptila
Applied and environmental microbiology, 1997Co-Authors: Deborah S. Hughes, Horst Felbeck, Jeffrey L. SteinAbstract:The uncultivated bacterial endoSymbionts of the hydrothermal vent tubeworm Riftia pachyptila play a central role in providing their host with fixed carbon. While this intimate association between host and Symbiont indicates tight integration and coordination of function via cellular communication mechanisms, no such systems have been identified. To elucidate potential signal transduction pathways in Symbionts that may mediate Symbiont-host communication, we cloned and characterized a gene encoding a histidine protein kinase homolog isolated from a Symbiont fosmid library. The gene, designated rssA (for Riftia Symbiont signal kinase), resembles known sensor kinases and encodes a protein capable of phosphorylating response regulators in Escherichia coli. A second open reading frame, rssB (for Riftia Symbiont signal regulator), encodes a protein similar to known response regulators. These results suggest that the Symbionts utilize a phosphotransfer signal transduction mechanism to communicate external signals that may mediate recognition of or survival within the host. The specific signals eliciting a response by the signal transduction proteins of the Symbiont remain to be elucidated.
Manuel Kleiner - One of the best experts on this subject based on the ideXlab platform.
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Metabolic differences between Symbiont subpopulations in the deep-sea tubeworm Riftia pachyptila
2020Co-Authors: Tjorven Hinzke, Horst Felbeck, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Mareike Meister, Jan Pané-farré, Petra Hildebrandt, Florian BonnAbstract:AbstractThe hydrothermal vent tube worm Riftia pachyptila lives in intimate symbiosis with intracellular sulfur-oxidizing gammaproteobacteria. Although the Symbiont population consists of a single 16S rRNA phylotype, bacteria in the same host animal exhibit a remarkable degree of metabolic diversity: They simultaneously utilize two carbon fixation pathways and various energy sources and electron acceptors. Whether these multiple metabolic routes are employed in the same Symbiont cells, or rather in distinct Symbiont subpopulations, was unclear. As Riftia Symbionts vary considerably in cell size and shape, we enriched individual Symbiont cell sizes by density gradient centrifugation in order to test whether Symbiont cells of different sizes show different metabolic profiles. Metaproteomic analysis and statistical evaluation using clustering and random forests, supported by microscopy and flow cytometry, strongly suggest that Riftia Symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: Small Symbionts actively divide and may establish cellular Symbiont-host interaction, as indicated by highest abundance of the cell division key protein FtsZ and highly abundant chaperones and porins in this initial phase. Large Symbionts, on the other hand, apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Highest abundance of enzymes for CO2 fixation, carbon storage and biosynthesis in large Symbionts indicates that in this late differentiation stage the Symbiont’s metabolism is efficiently geared towards the production of organic material. We propose that this division of labor between smaller and larger Symbionts benefits the productivity of the symbiosis as a whole.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host–Symbiont interactions
The ISME Journal, 2020Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host–microbe associations. However, how host–Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus , hosting a thiotrophic Symbiont, and Atlantic B. azoricus , containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host–microbe interactions can be quite variable, even between closely related systems.
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Comparative proteomics of related symbiotic mussel species reveals high variability of host-Symbiont interactions.
The ISME journal, 2019Co-Authors: Ruby Ponnudurai, Horst Felbeck, Stefan E. Heiden, Lizbeth Sayavedra, Tjorven Hinzke, Manuel Kleiner, Christian Hentschker, Stefan M. Sievert, Rabea Schlüter, Dörte BecherAbstract:Deep-sea Bathymodiolus mussels and their chemoautotrophic Symbionts are well-studied representatives of mutualistic host-microbe associations. However, how host-Symbiont interactions vary on the molecular level between related host and Symbiont species remains unclear. Therefore, we compared the host and Symbiont metaproteomes of Pacific B. thermophilus, hosting a thiotrophic Symbiont, and Atlantic B. azoricus, containing two Symbionts, a thiotroph and a methanotroph. We identified common strategies of metabolic support between hosts and Symbionts, such as the oxidation of sulfide by the host, which provides a thiosulfate reservoir for the thiotrophic Symbionts, and a cycling mechanism that could supply the host with Symbiont-derived amino acids. However, expression levels of these processes differed substantially between both symbioses. Backed up by genomic comparisons, our results furthermore revealed an exceptionally large repertoire of attachment-related proteins in the B. thermophilus Symbiont. These findings imply that host-microbe interactions can be quite variable, even between closely related systems.
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chemosynthetic Symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm paracatenula
Proceedings of the National Academy of Sciences of the United States of America, 2019Co-Authors: Oliver Jackle, Manuel Kleiner, Brandon K B Seah, Malin Tietjen, Nikolaus Leisch, Manuel Liebeke, Jasmine S Berg, Harald R GrubervodickaAbstract:Hosts of chemoautotrophic bacteria typically have much higher biomass than their Symbionts and consume Symbiont cells for nutrition. In contrast to this, chemoautotrophic Candidatus Riegeria Symbionts in mouthless Paracatenula flatworms comprise up to half of the biomass of the consortium. Each species of Paracatenula harbors a specific Ca. Riegeria, and the endoSymbionts have been vertically transmitted for at least 500 million years. Such prolonged strict vertical transmission leads to streamlining of Symbiont genomes, and the retained physiological capacities reveal the functions the Symbionts provide to their hosts. Here, we studied a species of Paracatenula from Sant’Andrea, Elba, Italy, using genomics, gene expression, imaging analyses, as well as targeted and untargeted MS. We show that its Symbiont, Ca. R. santandreae has a drastically smaller genome (1.34 Mb) than the Symbiont´s free-living relatives (4.29–4.97 Mb) but retains a versatile and energy-efficient metabolism. It encodes and expresses a complete intermediary carbon metabolism and enhanced carbon fixation through anaplerosis and accumulates massive intracellular inclusions such as sulfur, polyhydroxyalkanoates, and carbohydrates. Compared with symbiotic and free-living chemoautotrophs, Ca. R. santandreae’s versatility in energy storage is unparalleled in chemoautotrophs with such compact genomes. Transmission EM as well as host and Symbiont expression data suggest that Ca. R. santandreae largely provisions its host via outer-membrane vesicle secretion. With its high share of biomass in the symbiosis and large standing stocks of carbon and energy reserves, it has a unique role for bacterial Symbionts—serving as the primary energy storage for its animal host.