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  • 1
    Publication Date: 2019-03-05
    Description: Particles in aquatic environments host distinct communities of microbes, yet the evolution of particlespecialized taxa and the extent to which specialized microbial metabolism is associated with particles is largely unexplored. Here, we investigate the hypothesis that a widely distributed and uncultivated microbial group - the marine group II euryarchaea (MGII) - interacts with living and detrital particulate organic matter (POM) in the euphotic zone of the central California Current System. Using fluorescent in situ hybridization, we verified the association of euryarchaea with POM. We further quantified the abundance and distribution of MGII 16S ribosomal RNA genes in size-fractionated seawater samples and compared MGII functional capacity in metagenomes from the same fractions. The abundance of MGII in free-living and 〈3 μm fractions decreased with increasing distance from the coast, whereas MGII abundance in the 0.8-3 lm fraction remained constant. At several offshore sites, MGII abundance was highest in particle fractions, indicating that particle-attached MGII can outnumber free-living MGII under oligotrophic conditions. Compared with free-living MGII, the genome content of MGII in particleassociated fractions exhibits an increased capacity for surface adhesion, transcriptional regulation and catabolism of high molecular weight substrates. Moreover, MGII populations in POM fractions are phylogenetically distinct from and more diverse than free-living MGII. Eukaryotic phytoplankton additions stimulated MGII growth in bottle incubations, providing the first MGII net growth rate measurements. These ranged from 0.47 to 0.54 d-1. However, MGII were not recovered in wholegenome amplifications of flow-sorted picoeukaryotic phytoplankton and heterotrophic nanoflagellates, suggesting that MGII in particle fractions are not physically attached to living POM. Collectively, our results support a linkage between MGII ecophysiology and POM, implying that marine archaea have a role in elemental cycling through interactions with particles. © 2015 International Society for Microbial Ecology. All rights reserved.
    Type: Article , PeerReviewed
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  • 2
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Nature Publishing Group for personal use, not for redistribution. The definitive version was published in Nature 499 (2013): 205-208, doi:10.1038/nature12230.
    Description: Scientific ocean drilling has revealed a deep biosphere of widespread microbial life in sub-seafloor sediment. Microbial metabolism in the marine subsurface likely plays an important role in global biogeochemical cycles1-3 but deep biosphere activities are not well understood1. Here, we describe and analyze the first subseafloor metatranscriptomes from anaerobic Peru Margin sediment up to 159 meters below seafloor (mbsf) represented by over 1 billion cDNA sequence reads. Anaerobic metabolism of amino acids, carbohydrates, and lipids appear to be dominant metabolic processes, and profiles of dissimilatory sulfite reductase (Dsr) transcripts are consistent with porewater sulfate concentration profiles1. Moreover, transcripts involved in cell division increase as a function of microbial cell concentration, indicating that increases in subseafloor microbial abundance are a function of cell division across all three domains of life. These data support calculations1 and models4 of subseafloor microbial metabolism and represent the first holistic picture of deep biosphere activities.
    Description: This work was fostered by a Center for Dark Energy Biosphere Investigations (CDEBI) grant OCE-0939564 to WO and a NSF IOS grant 1238801 to JFB.
    Description: 2013-12-12
    Keywords: Marine subsurface ; mRNA ; Metatranscriptomics ; Deep biosphere ; Illumina sequencing ; Marine sediment ; Subseafloor ; ODP Leg 201 ; Gene expression
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 3
    Publication Date: 2022-05-25
    Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Scientific Reports 7 (2017): 6040, doi:10.1038/s41598-017-05590-9.
    Description: Selection of microorganisms in marine sediment is shaped by energy-yielding electron acceptors for respiration that are depleted in vertical succession. However, some taxa have been reported to reflect past depositional conditions suggesting they have experienced weak selection after burial. In sediments underlying the Arabian Sea oxygen minimum zone (OMZ), we performed the first metagenomic profiling of sedimentary DNA at centennial-scale resolution in the context of a multi-proxy paleoclimate reconstruction. While vertical distributions of sulfate reducing bacteria and methanogens indicate energy-based selection typical of anoxic marine sediments, 5–15% of taxa per sample exhibit depth-independent stratigraphies indicative of paleoenvironmental selection over relatively short geological timescales. Despite being vertically separated, indicator taxa deposited under OMZ conditions were more similar to one another than those deposited in bioturbated intervals under intervening higher oxygen. The genomic potential for denitrification also correlated with palaeo-OMZ proxies, independent of sediment depth and available nitrate and nitrite. However, metagenomes revealed mixed acid and Entner-Dourdoroff fermentation pathways encoded by many of the same denitrifier groups. Fermentation thus may explain the subsistence of these facultatively anaerobic microbes whose stratigraphy follows changing paleoceanographic conditions. At least for certain taxa, our analysis provides evidence of their paleoenvironmental selection over the last glacial-interglacial cycle.
    Description: his work was primarily supported by NSF MGG Grant #1357017 to MJLC, VG, and LG, and the KAUST-WHOI Special Academic Partnership Program OCRF-SP-WHOI-2013 (grants 7000000463 to XI and 7000000464 to MJLC). Additional financial support was provided via a C-DEBI grant #OCE-0939564 to WDO.
    Repository Name: Woods Hole Open Access Server
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  • 4
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2012. This is the author's version of the work. It is posted here by permission of Nature Publishing Group for personal use, not for redistribution. The definitive version was published in The ISME Journal 6 (2012): 1586–1601, doi:10.1038/ismej.2012.7.
    Description: Changes in ocean temperature and circulation patterns compounded by human activities are leading to oxygen minimum zone expansion with concomitant alteration in nutrient and climate active trace gas cycling. Here, we report the response of microbial eukaryote populations to seasonal changes in water column oxygen-deficiency using Saanich Inlet, a seasonally anoxic fjord on the coast of Vancouver Island British Columbia, as a model ecosystem. We combine small subunit ribosomal RNA gene sequencing approaches with multivariate statistical methods to reveal shifts in operational taxonomic units during successive stages of seasonal stratification and renewal. A meta-analysis is used to identify common and unique patterns of community composition between Saanich Inlet and the anoxic/sulfidic Cariaco Basin (Venezuela) and Framvaren Fjord (Norway) to show shared and unique responses of microbial eukaryotes to oxygen and sulfide in these three environments. Our analyses also reveal temporal fluctuations in rare populations of microbial eukaryotes, particularly anaerobic ciliates, that may be of significant importance to the biogeochemical cycling of methane in oxygen minimum zones.
    Description: This work was performed under the auspices of the US Department of Energy's Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory, Lawrence Livermore National Laboratory under Contract No., and Los Alamos National Laboratory (Contract No. DE-AC02-05CH11231, DE-AC52-07NA27344, DE-AC02-06NA25396), the Natural Sciences and Engineering Research Council (NSERC) of Canada 328256-07 and STPSC 356988, Canada Foundation for Innovation (CFI) 17444; Canadian Institute for Advanced Research (CIFAR), NSF MCB-0348407 to VE, NSF Center for Deep Energy Biosphere Investigations, and the Center for Bioinorganic Chemistry (CEBIC).
    Description: 2012-09-08
    Keywords: Protists ; Diversity ; Anoxic ; Oxygen minimum zone ; 18S rRNA approach
    Repository Name: Woods Hole Open Access Server
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  • 5
    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Microbiology 13 (2013): 150, doi:10.1186/1471-2180-13-150.
    Description: Deep hypersaline anoxic basins (DHABs) are isolated habitats at the bottom of the eastern Mediterranean Sea, which originate from the ancient dissolution of Messinian evaporites. The different basins have recruited their original biota from the same source, but their geological evolution eventually constituted sharp environmental barriers, restricting genetic exchange between the individual basins. Therefore, DHABs are unique model systems to assess the effect of geological events and environmental conditions on the evolution and diversification of protistan plankton. Here, we examine evidence for isolated evolution of unicellular eukaryote protistan plankton communities driven by geological separation and environmental selection. We specifically focused on ciliated protists as a major component of protistan DHAB plankton by pyrosequencing the hypervariable V4 fragment of the small subunit ribosomal RNA. Geospatial distributions and responses of marine ciliates to differential hydrochemistries suggest strong physical and chemical barriers to dispersal that influence the evolution of this plankton group. Ciliate communities in the brines of four investigated DHABs are distinctively different from ciliate communities in the interfaces (haloclines) immediately above the brines. While the interface ciliate communities from different sites are relatively similar to each other, the brine ciliate communities are significantly different between sites. We found no distance-decay relationship, and canonical correspondence analyses identified oxygen and sodium as most important hydrochemical parameters explaining the partitioning of diversity between interface and brine ciliate communities. However, none of the analyzed hydrochemical parameters explained the significant differences between brine ciliate communities in different basins. Our data indicate a frequent genetic exchange in the deep-sea water above the brines. The “isolated island character” of the different brines, that resulted from geological events and contemporary environmental conditions, create selective pressures driving evolutionary processes, and with time, lead to speciation and shape protistan community composition. We conclude that community assembly in DHABs is a mixture of isolated evolution (as evidenced by small changes in V4 primary structure in some taxa) and species sorting (as indicated by the regional absence/presence of individual taxon groups on high levels in taxonomic hierarchy).
    Description: This work was funded by NSF grants OCE-0849578 and OCE- 1061774 to VE and support from Carl Zeiss fellowship to AS and from the Deutsche Forschungsgemeinschaft (grants STO414/3-2 and STO414/7-1) to TS.
    Keywords: Ciliates ; Hypersaline ; Deep-sea anoxic basins ; DHABs ; Brine ; Species sorting ; Environmental filtering ; Niche separation
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 6
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Nature Publishing Group for personal use, not for redistribution. The definitive version was published in The ISME Journal 8 (2014): 418–429, doi:10.1038/ismej.2013.130.
    Description: Microbialites are organosedimentary structures that are formed through the interaction of benthic microbial communities and sediments and include mineral precipitation. These lithifying microbial mat structures include stromatolites and thrombolites. Exuma Sound in the Bahamas, and Hamelin Pool in Shark Bay, Western Australia are two locations where significant stands of modern microbialites exist. Although prokaryotic diversity in these structures is reasonably well documented, little is known about the eukaryotic component of these communities and their potential to influence sedimentary fabrics through grazing, binding and burrowing activities. Accordingly, comparisons of eukaryotic communities in modern stromatolitic and thrombolytic mats can potentially provide insight into the coexistence of both laminated and clotted mat structures in close proximity to one another. Here we examine this possibility by comparing eukaryotic diversity based on Sanger and high-throughput pyrosequencing of small subunit ribosomal RNA (18S rRNA) genes. Analyses were based on total RNA extracts as template to minimize input from inactive or deceased organisms. Results identified diverse eukaryotic communities particularly stramenopiles, Alveolata, Metazoa, Amoebozoa, and Rhizaria within different mat types at both locations, as well as abundant and diverse signatures of eukaryotes with 〈80% sequence similarity to sequences in GenBank. This suggests presence of significant novel eukaryotic diversity, particularly in hypersaline Hamelin Pool. There was evidence of vertical structuring of protist populations and foraminiferal diversity was highest in bioturbated/clotted thrombolite mats of Highborne Cay.
    Description: This work was funded by grant OCE-0926421 to JMB and VPE and OCE-0926372 to RES.
    Keywords: Eukaryote ; Protist ; Stromatolite ; Microbialite ; Thrombolite ; 18S rRNA ; Diversity ; Foraminifera ; Hamelin Pool ; Highborne Cay
    Repository Name: Woods Hole Open Access Server
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  • 7
    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Climate of the Past 14 (2018): 1669-1686, doi:10.5194/cp-14-1669-2018.
    Description: Climate exerted constraints on the growth and decline of past human societies but our knowledge of temporal and spatial climatic patterns is often too restricted to address causal connections. At a global scale, the inter-hemispheric thermal balance provides an emergent framework for understanding regional Holocene climate variability. As the thermal balance adjusted to gradual changes in the seasonality of insolation, the Intertropical Convergence Zone migrated southward accompanied by a weakening of the Indian summer monsoon. Superimposed on this trend, anomalies such as the Little Ice Age point to asymmetric changes in the extratropics of either hemisphere. Here we present a reconstruction of the Indian winter monsoon in the Arabian Sea for the last 6000 years based on paleobiological records in sediments from the continental margin of Pakistan at two levels of ecological complexity: sedimentary ancient DNA reflecting water column environmental states and planktonic foraminifers sensitive to winter conditions. We show that strong winter monsoons between ca. 4500 and 3000 years ago occurred during a period characterized by a series of weak interhemispheric temperature contrast intervals, which we identify as the early neoglacial anomalies (ENA). The strong winter monsoons during ENA were accompanied by changes in wind and precipitation patterns that are particularly evident across the eastern Northern Hemisphere and tropics. This coordinated climate reorganization may have helped trigger the metamorphosis of the urban Harappan civilization into a rural society through a push–pull migration from summer flood-deficient river valleys to the Himalayan piedmont plains with augmented winter rains. The decline in the winter monsoon between 3300 and 3000 years ago at the end of ENA could have played a role in the demise of the rural late Harappans during that time as the first Iron Age culture established itself on the Ghaggar-Hakra interfluve. Finally, we speculate that time-transgressive land cover changes due to aridification of the tropics may have led to a generalized instability of the global climate during ENA at the transition from the warmer Holocene thermal maximum to the cooler Neoglacial.
    Description: This work was supported by the NSF OCE grant no. 0634731 and internal WHOI funds to Liviu Giosan, NSF MGG grant no. 1357017 to Marco J. L. Coolen, Valier Galy and Liviu Giosan; and a C-DEBI grant no. OCE-0939564 to William D. Orsi.
    Repository Name: Woods Hole Open Access Server
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  • 8
    Publication Date: 2022-05-25
    Description: © The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 6 (2015): 197, doi:10.3389/fmicb.2015.00197.
    Description: Thawing of permafrost soils is expected to stimulate microbial decomposition and respiration of sequestered carbon. This could, in turn, increase atmospheric concentrations of greenhouse gasses, such as carbon dioxide and methane, and create a positive feedback to climate warming. Recent metagenomic studies suggest that permafrost has a large metabolic potential for carbon processing, including pathways for fermentation and methanogenesis. Here, we performed a pilot study using ultrahigh throughput Illumina HiSeq sequencing of reverse transcribed messenger RNA to obtain a detailed overview of active metabolic pathways and responsible organisms in up to 70 cm deep permafrost soils at a moist acidic tundra location in Arctic Alaska. The transcriptional response of the permafrost microbial community was compared before and after 11 days of thaw. In general, the transcriptional profile under frozen conditions suggests a dominance of stress responses, survival strategies, and maintenance processes, whereas upon thaw a rapid enzymatic response to decomposing soil organic matter (SOM) was observed. Bacteroidetes, Firmicutes, ascomycete fungi, and methanogens were responsible for largest transcriptional response upon thaw. Transcripts indicative of heterotrophic methanogenic pathways utilizing acetate, methanol, and methylamine were found predominantly in the permafrost table after thaw. Furthermore, transcripts involved in acetogenesis were expressed exclusively after thaw suggesting that acetogenic bacteria are a potential source of acetate for acetoclastic methanogenesis in freshly thawed permafrost. Metatranscriptomics is shown here to be a useful approach for inferring the activity of permafrost microbes that has potential to improve our understanding of permafrost SOM bioavailability and biogeochemical mechanisms contributing to greenhouse gas emissions as a result of permafrost thaw.
    Description: This work was fostered by grants from WHOI's Arctic Research Initiative to MJLC and AS, as well as a Center for Dark Energy Biosphere Investigations (CDEBI) grant OCE-0939564 to WDO.
    Repository Name: Woods Hole Open Access Server
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  • 9
    Publication Date: 2022-02-04
    Description: Fungi are ubiquitous in the ocean and hypothesized to be important members of marine ecosystems, but their roles in the marine carbon cycle are poorly understood. Here, we use 13C DNA stable isotope probing coupled with phylogenetic analyses to investigate carbon assimilation within diverse communities of planktonic and benthic fungi in the Benguela Upwelling System (Namibia). Across the redox stratified water column and in the underlying sediments, assimilation of 13C-labeled carbon from diatom extracellular polymeric substances (13C-dEPS) by fungi correlated with the expression of fungal genes encoding carbohydrate-active enzymes. Phylogenetic analysis of genes from 13C-labeled metagenomes revealed saprotrophic lineages related to the facultative yeast Malassezia were the main fungal foragers of pelagic dEPS. In contrast, fungi living in the underlying sulfidic sediments assimilated more 13C-labeled carbon from chemosynthetic bacteria compared to dEPS. This coincided with a unique seafloor fungal community and dissolved organic matter composition compared to the water column, and a 100-fold increased fungal abundance within the subseafloor sulfide-nitrate transition zone. The subseafloor fungi feeding on 13C-labeled chemolithoautotrophs under anoxic conditions were affiliated with Chytridiomycota and Mucoromycota that encode cellulolytic and proteolytic enzymes, revealing polysaccharide and protein-degrading fungi that can anaerobically decompose chemosynthetic necromass. These subseafloor fungi, therefore, appear to be specialized in organic matter that is produced in the sediments. Our findings reveal that the phylogenetic diversity of fungi across redox stratified marine ecosystems translates into functionally relevant mechanisms helping to structure carbon flow from primary producers in marine microbiomes from the surface ocean to the subseafloor.
    Repository Name: EPIC Alfred Wegener Institut
    Type: Article , isiRev
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  • 10
    Publication Date: 2022-05-26
    Description: © 2009 The Authors. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Biology 7 (2009): 72, doi:10.1186/1741-7007-7-72.
    Description: Recent advances in sequencing strategies make possible unprecedented depth and scale of sampling for molecular detection of microbial diversity. Two major paradigm-shifting discoveries include the detection of bacterial diversity that is one to two orders of magnitude greater than previous estimates, and the discovery of an exciting 'rare biosphere' of molecular signatures ('species') of poorly understood ecological significance. We applied a high-throughput parallel tag sequencing (454 sequencing) protocol adopted for eukaryotes to investigate protistan community complexity in two contrasting anoxic marine ecosystems (Framvaren Fjord, Norway; Cariaco deep-sea basin, Venezuela). Both sampling sites have previously been scrutinized for protistan diversity by traditional clone library construction and Sanger sequencing. By comparing these clone library data with 454 amplicon library data, we assess the efficiency of high-throughput tag sequencing strategies. We here present a novel, highly conservative bioinformatic analysis pipeline for the processing of large tag sequence data sets.The analyses of ca. 250,000 sequence reads revealed that the number of detected Operational Taxonomic Units (OTUs) far exceeded previous richness estimates from the same sites based on clone libraries and Sanger sequencing. More than 90% of this diversity was represented by OTUs with less than 10 sequence tags. We detected a substantial number of taxonomic groups like Apusozoa, Chrysomerophytes, Centroheliozoa, Eustigmatophytes, hyphochytriomycetes, Ichthyosporea, Oikomonads, Phaeothamniophytes, and rhodophytes which remained undetected by previous clone library-based diversity surveys of the sampling sites. The most important innovations in our newly developed bioinformatics pipeline employ (i) BLASTN with query parameters adjusted for highly variable domains and a complete database of public ribosomal RNA (rRNA) gene sequences for taxonomic assignments of tags; (ii) a clustering of tags at k differences (Levenshtein distance) with a newly developed algorithm enabling very fast OTU clustering for large tag sequence data sets; and (iii) a novel parsing procedure to combine the data from individual analyses. Our data highlight the magnitude of the under-sampled 'protistan gap' in the eukaryotic tree of life. This study illustrates that our current understanding of the ecological complexity of protist communities, and of the global species richness and genome diversity of protists, is severely limited. Even though 454 pyrosequencing is not a panacea, it allows for more comprehensive insights into the diversity of protistan communities, and combined with appropriate statistical tools, enables improved ecological interpretations of the data and projections of global diversity.
    Description: The International Census of Marine Microbes and the W.M. Keck Foundation award to the Marine Biological Laboratory at Woods Hole (MA) supported the pyrosequencing part of this study. Further financial support came from a grant from the Deutsche Forschungsgemeinschaft to TS (STO414/3-1). Support for the unpublished work on Cariaco Basin protists came from NSF MCB-0348407 to VE (collaborative project with S Epstein at Northeastern University, Boston, MA, USA). Financial support to AC was provided by NSF MCB-0348045. Financial support to RC was provided by the ANR-Biodiversité project Aquaparadox.
    Repository Name: Woods Hole Open Access Server
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