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  • 1
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    Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis (2019)
    American Society for Microbiology
    In:  mBio, 10 (6). e02243-19.
    Details
    Publication Date: 2022-01-31
    Description: The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1128/mBio.02243-19
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 2
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    Unexpected diversity of bacteria capable of carbon monoxide oxidation in a coastal marine environment, and contribution of the Roseobacter-cssociated clade to total CO oxidation (2006)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © American Society for Microbiology, 2006. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 72 (2006): 1966-1973, doi:10.1128/AEM.72.3.1966-1973.2006.
    Description: The species diversity, phylogenetic affiliations, and physiological activity rates of carbon monoxide-oxidizing microorganisms were investigated, using new isolates from surface waters collected from the coast of New England and type strains from established collections. A direct isolation method allowed the simultaneous recovery of organisms with different growth rates and nutritional requirements and the identification of marine microorganisms that oxidize CO at an environmentally relevant concentration (42 nM CO). Isolates that oxidized CO at environmentally relevant rates (〉4.5 x 10–11 nmol CO oxidized cell–1 h–1) were taxonomically diverse, with representatives in the alpha and gamma subclasses of the Proteobacteria and the phylum Bacteroidetes, and represent a hitherto unreported metabolic function for several diverse microbial types. Isolates and type strains having the greatest specific rates of CO metabolism (1.1 x 10–10 to 2.3 x 10–10 nmol CO oxidized cell–1 h–1) belonged to the Roseobacter-associated clade (RAC) of the alpha subclass of the Proteobacteria. By using triple-labeled slide preparations, differential counts of active CO-oxidizing RAC cells, total RAC cells, and total bacterial cell counts in environmental samples were obtained. RAC organisms were a major component of total cell numbers (36%). Based on the density of active CO-oxidizing RAC cells in natural samples and RAC-specific metabolic activities determined for pure cultures, active CO-oxidizing RAC cells may contribute up to 15% of the total CO oxidation occurring in coastal waters.
    Description: Funding was provided by National Science Foundation grant OCE-0136876, Coastal Ocean Institute and Rinehart Coastal Research Center grant BI10918, and the Woods Hole Oceanographic Institution Academic Programs Office.
    Repository Name: Woods Hole Open Access Server
    Type: Article
    Format: 160565 bytes
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  • 3
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    Spatiotemporal distribution of marine magnetotactic bacteria in a aeasonally stratified coastal salt pond (2005)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © American Society for Microbiology, 2004. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 70 (2004): 6230-6239, doi:10.1128/AEM.70.10.6230-6239.2004.
    Description: The occurrence and distribution of magnetotactic bacteria (MB) were studied as a function of the physical and chemical conditions in meromictic Salt Pond, Falmouth, Mass., throughout summer 2002. Three dominant MB morphotypes were observed to occur within the chemocline. Small microaerophilic magnetite-producing cocci were present at the top of the chemocline, while a greigite-producing packet-forming bacterium occurred at the base of the chemocline. The distributions of these groups displayed sharp changes in abundance over small length scales within the water column as well as strong seasonal fluctuations in population abundance. We identified a novel, greigite-producing rod in the sulfidic hypolimnion that was present in relatively constant abundance over the course of the season. This rod is the first MB that appears to belong to the {gamma}-Proteobacteria, which may suggest an iron- rather than sulfur-based respiratory metabolism. Its distribution and phylogenetic identity suggest that an alternative model for the ecological and physiological role of magnetotaxis is needed for greigite-producing MB.
    Description: This work was partially funded by a grant from the Woods Hole Oceanographic Institution Reinhart Coastal Research Center to S.L.S. and K.J.E. S.L.S. was supported by a National Defense Science and Engineering graduate fellowship. D.A.B. was supported by National Science Foundation grant EAR-0311950 and National Aeronautics and Space Administration (NASA) Johnson Space Center grant NAG 9-1115.
    Keywords: Magnetotactic bacteria (MB) ; {gamma}-Proteobacteria
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 4
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    Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the ε subdivision of proteobacteria (2005)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © American Society for Microbiology, 2005. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Journal of Bacteriology 187 (2005): 3020-3027, doi:10.1128/JB.187.9.3020-3027.2005.
    Description: Based on 16S rRNA gene surveys, bacteria of the ε subdivision of proteobacteria have been identified to be important members of microbial communities in a variety of environments, and quite a few have been demonstrated to grow autotrophically. However, no information exists on what pathway of autotrophic carbon fixation these bacteria might use. In this study, Thiomicrospira denitrificans and Candidatus Arcobacter sulfidicus, two chemolithoautotrophic sulfur oxidizers of the ε subdivision of proteobacteria, were examined for activities of the key enzymes of the known autotrophic CO2 fixation pathways. Both organisms contained activities of the key enzymes of the reductive tricarboxylic acid cycle, ATP citrate lyase, 2-oxoglutarate:ferredoxin oxidoreductase, and pyruvate:ferredoxin oxidoreductase. Furthermore, no activities of key enzymes of other CO2 fixation pathways, such as the Calvin cycle, the reductive acetyl coenzyme A pathway, and the 3-hydroxypropionate cycle, could be detected. In addition to the key enzymes, the activities of the other enzymes involved in the reductive tricarboxylic acid cycle could be measured. Sections of the genes encoding the {alpha}- and ß-subunits of ATP citrate lyase could be amplified from both organisms. These findings represent the first direct evidence for the operation of the reductive tricarboxylic acid cycle for autotrophic CO2 fixation in {varepsilon}-proteobacteria. Since {varepsilon}-proteobacteria closely related to these two organisms are important in many habitats, such as hydrothermal vents, oxic-sulfidic interfaces, or oilfields, these results suggest that autotrophic CO2 fixation via the reductive tricarboxylic acid cycle might be more important than previously considered.
    Description: This study was supported by the National Science Foundation “Ecological and Evolutionary Physiology” program (grant IBN-0131557) and the NASA Astrobiology Institute (“From Early Biospheric Metabolism to the Evolution of Complex Systems”; grant NNA04CC04A).
    Keywords: Thiomicrospira denitrificans ; Candidatus Arcobacter sulfidicus ; Autotrophic CO2 fixation
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 5
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    Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans (2009)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © American Society for Microbiology, 2008. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 74 (2008): 1145-1156, doi:10.1128/AEM.01844-07.
    Description: Sulfur-oxidizing epsilonproteobacteria are common in a variety of sulfidogenic environments. These autotrophic and mixotrophic sulfur-oxidizing bacteria are believed to contribute substantially to the oxidative portion of the global sulfur cycle. In order to better understand the ecology and roles of sulfur-oxidizing epsilonproteobacteria, in particular those of the widespread genus Sulfurimonas, in biogeochemical cycles, the genome of Sulfurimonas denitrificans DSM1251 was sequenced. This genome has many features, including a larger size (2.2 Mbp), that suggest a greater degree of metabolic versatility or responsiveness to the environment than seen for most of the other sequenced epsilonproteobacteria. A branched electron transport chain is apparent, with genes encoding complexes for the oxidation of hydrogen, reduced sulfur compounds, and formate and the reduction of nitrate and oxygen. Genes are present for a complete, autotrophic reductive citric acid cycle. Many genes are present that could facilitate growth in the spatially and temporally heterogeneous sediment habitat from where Sulfurimonas denitrificans was originally isolated. Many resistance-nodulation-development family transporter genes (10 total) are present; of these, several are predicted to encode heavy metal efflux transporters. An elaborate arsenal of sensory and regulatory protein-encoding genes is in place, as are genes necessary to prevent and respond to oxidative stress.
    Description: This work was performed under the auspices of the U.S. Department of Energy by Lawrence Livermore National Laboratory, University of California, under contract W-7405-ENG-48. Genome closure was funded in part by a USF Innovative Teaching Grant (K.M.S.). S.M.S. received partial support through a fellowship from the Hanse Wissenschaftskolleg in Delmenhorst, Germany (http://www.h-w-k.de), and NSF grant OCE-0452333. K.M.S. is grateful for support from NSF grant MCB-0643713. M.H. was supported by a WHOI postdoctoral scholarship. M.G.K. was supported in part by incentive funds provided by the UofL-EVPR office, the KY Science and Engineering Foundation (KSEF-787-RDE-007), and the National Science Foundation (EF-0412129).
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 6
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    Genus-specific carbon fixation activity measurements reveal distinct responses to oxygen among hydrothermal vent campylobacteria (2022)
    American Society for Microbiology
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © American Society for Microbiology, 2022. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 88(2),(2022): e02083-21, https://doi.org/10.1128/AEM.02083-21.
    Description: Molecular surveys of low temperature deep-sea hydrothermal vent fluids have shown that Campylobacteria (previously Epsilonproteobacteria) often dominate the microbial community and that three genera, Arcobacter, Sulfurimonas, and Sulfurovum, frequently coexist. In this study, we used replicated radiocarbon incubations of deep-sea hydrothermal fluids to investigate activity of each genus under three experimental conditions. To quantify genus-specific radiocarbon incorporation, we used newly designed oligonucleotide probes for Arcobacter, Sulfurimonas, and Sulfurovum to quantify their activity using catalyzed-reporter deposition fluorescence in situ hybridization (CARD-FISH) combined with fluorescence-activated cell sorting. All three genera actively fixed CO2 in short-term (∼ 20 h) incubations, but responded differently to the additions of nitrate and oxygen. Oxygen additions had the largest effect on community composition, and caused a pronounced shift in community composition at the amplicon sequence variant (ASV) level after only 20 h of incubation. The effect of oxygen on carbon fixation rates appeared to depend on the initial starting community. The presented results support the hypothesis that these chemoautotrophic genera possess functionally redundant core metabolic capabilities, but also reveal finer-scale differences in growth likely reflecting adaptation of physiologically-distinct phylotypes to varying oxygen concentrations in situ. Overall, our study provides new insights into how oxygen controls community composition and total chemoautotrophic activity, and underscores how quickly deep-sea vent microbial communities respond to disturbances.
    Description: This research was funded by the U.S. National Science Foundation grants OCE-1131095 (S.M.S.) and OCE-1136727 (S.M.S., J.S.S.). Further support was provided by the WHOI Investment in Science Fund (S.M.S.). Funding for J.M. was further provided by doctoral fellowships from the Natural Sciences and Engineering Research Council of Canada (PGSD3-430487-2013, PGSM-405117-2011) and the National Aeronautics and Space Administration Earth Systems Science Fellowship (PLANET14F-0075), an award from the Canadian Meteorological and Oceanographic Society, and the WHOI Academic Programs Office.
    Keywords: Arcobacter ; CARD-FISH ; Campylobacteria ; Chemoautotrophy ; Deep-sea hydrothermal vents ; FACS ; Niche differentiation ; Sulfur oxidation ; Sulfurimonas ; Sulfurovum
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 7
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    Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur (2005)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © American Society for Microbiology, 2002. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 68 (2002): 316-325, doi:10.1128/AEM.68.1.316-325.2002.
    Description: A coastal marine sulfide-oxidizing autotrophic bacterium produces hydrophilic filamentous sulfur as a novel metabolic end product. Phylogenetic analysis placed the organism in the genus Arcobacter in the epsilon subdivision of the Proteobacteria. This motile vibrioid organism can be considered difficult to grow, preferring to grow under microaerophilic conditions in flowing systems in which a sulfide-oxygen gradient has been established. Purified cell cultures were maintained by using this approach. Essentially all 4',6-diamidino-2-phenylindole dihydrochloride-stained cells in a flowing reactor system hybridized with Arcobacter-specific probes as well as with a probe specific for the sequence obtained from reactor-grown cells. The proposed provisional name for the coastal isolate is "Candidatus Arcobacter sulfidicus." For cells cultured in a flowing reactor system, the sulfide optimum was higher than and the CO2 fixation activity was as high as or higher than those reported for other sulfur oxidizers, such as Thiomicrospira spp. Cells associated with filamentous sulfur material demonstrated nitrogen fixation capability. No ribulose 1,5-bisphosphate carboxylase/oxygenase could be detected on the basis of radioisotopic activity or by Western blotting techniques, suggesting an alternative pathway of CO2 fixation. The process of microbial filamentous sulfur formation has been documented in a number of marine environments where both sulfide and oxygen are available. Filamentous sulfur formation by "Candidatus Arcobacter sulfidicus" or similar strains may be an ecologically important process, contributing significantly to primary production in such environments.
    Description: This work was supported by National Science Foundation grant IBN-9630054.
    Keywords: Sulfide-oxidizing autotrophic bacterium ; Hydrophilic filamentous sulfur
    Repository Name: Woods Hole Open Access Server
    Type: Article
    Format: 1027760 bytes
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  • 8
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    Host-microbe interactions in the chemosynthetic Riftia pachyptila symbiosis (2020)
    American Society for Microbiology
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hinzke, T., Kleiner, M., Breusing, C., Felbeck, H., Häsler, R., Sievert, S. M., Schlüter, R., Rosenstiel, P., Reusch, T. B. H., Schweder, T., & Markert, S. Host-microbe interactions in the chemosynthetic Riftia pachyptila symbiosis. Mbio, 10(6), (2019): e02243-19, doi:10.1128/mBio.02243-19.
    Description: The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis.
    Description: This work was supported by the German Research Foundation DFG (grant MA 6346/2-1 to S.M., grant BR 5488/1-1 to C.B.), the German Academic Exchange Service DAAD (T.H.), a fellowship of the Institute of Marine Biotechnology Greifswald (T.H.), the Canada Foundation for Innovation, the Government of Alberta and the Natural Sciences and Engineering Research Council of Canada NSERC through a Banting Fellowship (M.K.), the U.S. National Science Foundation (grants OCE-0452333, OCE-1136727, OCE-1131095, and OCE-1559198 to S.M.S.), and the WHOI Investment in Science Fund (S.M.S.). P.R. was supported by a grant from the DFG CCGA Comprehensive Center for Genome Analysis, Kiel, and the DFG CRC1182 “Origin and Function of Metaorganisms.” R.H. and T.B.H.R. were supported by the DFG CRC1182 “Origin and Function of Metaorganisms,” subprojects B2, Z3, and INF.
    Keywords: host-microbe interactions ; symbiosis ; holobiont ; chemosynthesis ; hydrothermal vents ; metaproteomics
    Repository Name: Woods Hole Open Access Server
    Type: Article
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