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  • 1
    Publication Date: 2022-05-25
    Description: © The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 5 (2014): 605, doi:10.3389/fmicb.2014.00605.
    Description: Some of the most extreme marine habitats known are the Mediterranean deep hypersaline anoxic basins (DHABs; water depth ∼3500 m). Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB water-column haloclines and brines, the existence and activity of benthic DHAB protists have rarely been explored. Here, we report findings regarding protists and fungi recovered from sediments of three DHAB (Discovery, Urania, L’ Atalante) haloclines, and compare these to communities from sediments underlying normoxic waters of typical Mediterranean salinity. Halocline sediments, where the redoxcline impinges the seafloor, were studied from all three DHABs. Microscopic cell counts suggested that halocline sediments supported denser protist populations than those in adjacent control sediments. Pyrosequencing analysis based on ribosomal RNA detected eukaryotic ribotypes in the halocline sediments from each of the three DHABs, most of which were fungi. Sequences affiliated with Ustilaginomycotina Basidiomycota were the most abundant eukaryotic signatures detected. Benthic communities in these DHABs appeared to differ, as expected, due to differing brine chemistries. Microscopy indicated that only a low proportion of protists appeared to bear associated putative symbionts. In a considerable number of cases, when prokaryotes were associated with a protist, DAPI staining did not reveal presence of any nuclei, suggesting that at least some protists were carcasses inhabited by prokaryotic scavengers.
    Description: K. Kormas was partially supported by the University of Thessaly through a sabbatical in 2013. Supported by NSF grants OCE-0849578 to Virginia P. Edgcomb and Joan M. Bernhard and OCE-1061391 to Joan M. Bernhard and Virginia P. Edgcomb.
    Keywords: Eukaryote ; DHABs ; Discovery ; Urania, L’ Atalante ; Diversity ; rRNA
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 2
    Publication Date: 2022-05-26
    Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 7 (2016): 163, doi:10.3389/fmicb.2016.00163.
    Description: Some benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation with isotopically labeled nitrate and sulfate in dysoxic or anoxic conditions. After 2 weeks of incubation, foraminiferal specimens were fixed and prepared for Transmission Electron Microscopy (TEM) and correlative nanometer-scale secondary ion mass spectrometry (NanoSIMS) analyses. TEM observations revealed that there were characteristic ultrastructural features typically near the cell periphery in the youngest two or three chambers of the foraminifera exposed to anoxic conditions. These structures, which are electron dense and ~200–500 nm in diameter and co-occurred with possible endobionts, were labeled with 15N originated from 15N-labeled nitrate under anoxia and were labeled with both 15N and 34S under dysoxia. The labeling with 15N was more apparent in specimens from the dysoxic incubation, suggesting higher foraminiferal activity or increased availability of the label during exposure to oxygen depletion than to anoxia. Our results suggest that the electron dense bodies in Ammonia sp. play a significant role in nitrate incorporation and/or subsequent nitrogen assimilation during exposure to dysoxic to anoxic conditions.
    Description: This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (Young Scientists B No. 22740340 and Scientific Research C No. 24540504 to HN), an Invitation Fellowship for Research in Japan to JB by Japan Society for the Promotion of Science (JSPS), the Robert W. Morse Chair for Excellence in Oceanography at WHOI to JB, and The Investment in Science Fund at WHOI to JB.
    Keywords: Foraminifer ; Nitrate ; NanoSIMS ; Electron dense body ; Endobionts ; Ultrastructure ; Denitrification
    Repository Name: Woods Hole Open Access Server
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  • 3
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Schmidt, C., Geslin, E., Bernhard, J. M., LeKieffre, C., Svenning, M. M., Roberge, H., Schweizer, M., & Panieri, G. Deposit-feeding of Nonionellina labradorica (foraminifera) from an Arctic methane seep site and possible association with a methanotroph. Biogeosciences, 19(16), (2022): 3897–3909, https://doi.org/10.5194/bg-19-3897-2022.
    Description: Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material with entrained bacteria). However, the role of such foraminifera in the benthic food web remains understudied. Foraminifera feeding on methanotrophic bacteria, which are 13C-depleted, may cause negative cytoplasmic and/or calcitic δ13C values. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (20 h) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti and analysed N. labradorica cytology via transmission electron microscopy (TEM). We hypothesised that M. sedimenti would be visible post-experiment in degradation vacuoles, as evidenced by their ultrastructure. Sediment grains (mostly clay) occurred inside one or several degradation vacuoles in all foraminifers. In 24 % of the specimens from the feeding experiment degradation vacuoles also contained bacteria, although none could be confirmed to be the offered M. sedimenti. Observations of the apertural area after 20 h incubation revealed three putative methanotrophs, close to clay particles, based on bacterial ultrastructural characteristics. Furthermore, we noted the absence of bacterial endobionts in all examined N. labradorica but confirmed the presence of kleptoplasts, which were often partially degraded. In sum, we suggest that M. sedimenti can be consumed via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site.
    Description: This research has been supported by the French scientific programme MOPGA (Make our Planet Great Again) managed by the National Research Agency; the Norwegian Research Council through the Centre for Arctic Gas Hydrate, Environment and Climate (project number 223259); NORCRUST (project number 255250); and by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – 444059848.
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 4
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bernhard, J. M., Wit, J. C., Starczak, V. R., Beaudoin, D. J., Phalen, W. G., & McCorkle, D. C. Impacts of multiple stressors on a benthic foraminiferal community: a long-term experiment assessing response to ocean acidification, hypoxia and warming. Frontiers in Marine Science, 8, (2021): 643339, https://doi.org/10.3389/fmars.2021.643339.
    Description: Ocean chemistry is changing as a result of human activities. Atmospheric carbon dioxide (CO2) concentrations are increasing, causing an increase in oceanic pCO2 that drives a decrease in oceanic pH, a process called ocean acidification (OA). Higher CO2 concentrations are also linked to rising global temperatures that can result in more stratified surface waters, reducing the exchange between surface and deep waters; this stronger stratification, along with nutrient pollution, contributes to an expansion of oxygen-depleted zones (so called hypoxia or deoxygenation). Determining the response of marine organisms to environmental changes is important for assessments of future ecosystem functioning. While many studies have assessed the impact of individual or paired stressors, fewer studies have assessed the combined impact of pCO2, O2, and temperature. A long-term experiment (∼10 months) with different treatments of these three stressors was conducted to determine their sole or combined impact on the abundance and survival of a benthic foraminiferal community collected from a continental-shelf site. Foraminifera are well suited to such study because of their small size, relatively rapid growth, varied mineralogies and physiologies. Inoculation materials were collected from a ∼77-m deep site south of Woods Hole, MA. Very fine sediments (〈53 μm) were used as inoculum, to allow the entire community to respond. Thirty-eight morphologically identified taxa grew during the experiment. Multivariate statistical analysis indicates that hypoxia was the major driving factor distinguishing the yields, while warming was secondary. Species responses were not consistent, with different species being most abundant in different treatments. Some taxa grew in all of the triple-stressor samples. Results from the experiment suggest that foraminiferal species’ responses will vary considerably, with some being negatively impacted by predicted environmental changes, while other taxa will tolerate, and perhaps even benefit, from deoxygenation, warming and OA.
    Description: This work was supported by the US NSF SEES-OA grant OCE-1219948 to JB and the Investment in Science Program at WHOI. DM also received support from the NSF Independent Research and Development Program.
    Keywords: Deoxygenation ; Ocean acidification ; Benthic communities ; Benthic foraminifera ; Climate change ; Propagule bank ; Global warming
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 5
    Publication Date: 2022-11-15
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in LeKieffre, C., Jauffrais, T., Bernhard, J., Filipsson, H., Schmidt, C., Roberge, H., Maire, O., Panieri, G., Geslin, E., & Meibom, A. Ammonium and sulfate assimilation is widespread in benthic foraminifera. Frontiers in Marine Science, 9, (2022): 861945, https://doi.org/10.3389/fmars.2022.861945.
    Description: Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable 15N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding 15N and 34S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.
    Description: This work was supported by the Swiss National Science Foundation (grant no. 200021_149333), and a postdoctoral fellowship allowed to CL by the University Loire-Bretagne. SBB sampling was funded by US National Science Foundation grant BIO IOS 1557430 to JMB, who also acknowledges NASA grant #80NSSC21K0478 for partial support. HF acknowledges funding from the Swedish Research Council VR (grant number 2017-04190). Svalbard sampling was supported by the Research Council of Norway through CAGE (Center for Excellence in Arctic Gas Hydrate Environment and Climate, project number 223259) and NORCRUST (project number 255150) to GP and the fellowship MOPGA (Make Our Planet Great Again) by CAMPUS France to CS.
    Keywords: Marine protists ; Coastal environments ; Biogeochemical cycles ; NanoSIMS ; Nitrogen ; Sulfur
    Repository Name: Woods Hole Open Access Server
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  • 6
    Publication Date: 2022-05-26
    Description: © The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 3 (2012): 341, doi:10.3389/fmicb.2012.00341.
    Description: Symbioses between Bacteria, Archaea, and Eukarya in deep-sea marine environments represent a means for eukaryotes to exploit otherwise inhospitable habitats. Such symbioses are abundant in many low-oxygen benthic marine environments, where the majority of microbial eukaryotes contain prokaryotic symbionts. Here, we present evidence suggesting that in certain oxygen-depleted marine water-column habitats, the majority of microbial eukaryotes are also associated with prokaryotic cells. Ciliates (protists) associated with bacteria were found to be the dominant eukaryotic morphotype in the haloclines of two different deep-sea hypersaline anoxic basins (DHABs) in the Eastern Mediterranean Sea. These findings are compared to associations between ciliates and bacteria documented from the permanently anoxic waters of the Cariaco Basin (Caribbean Sea). The dominance of ciliates exhibiting epibiotic bacteria across three different oxygen-depleted marine water column habitats suggests that such partnerships confer a fitness advantage for ciliates in these environments.
    Description: This work was funded by NSF grant OCE-0849578 and to Virginia P. Edgcomb and Joan M. Bernhard, and OCE-1061774 to Virginia P. Edgcomb and Craig Taylor (WHOI).
    Keywords: Ciliate ; SEM ; rRNA ; Anoxic ; OMZ ; Hypersaline ; Symbiosis ; CARD-FISH
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 7
    Publication Date: 2022-05-26
    Description: © The Author(s), 2011. This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited. The definitive version was published in Frontiers in Microbiology 2 (2011): 55, doi:10.3389/fmicb.2011.00055.
    Description: Marine micro-oxic to sulfidic environments are sites of intensive biogeochemical cycling and elemental sequestration, where prokaryotes are major driving forces mediating carbon, nitrogen, sulfur, phosphorus, and metal cycles, important from both biogeochemical and evolutionary perspectives. Associations between single-celled eukaryotes and bacteria and/or archaea are common in such habitats. Here we describe a ciliate common in the micro-oxic to anoxic, typically sulfidic, sediments of Santa Barbara Basin (CA, USA). The ciliate is 95% similar to Parduzcia orbis (18S rRNA). Transmission electron micrographs reveal clusters of at least three different endobiont types organized within membrane-bound sub-cellular regions. Catalyzed reporter deposition–fluorescent in situ hybridization and 16S rRNA clone libraries confirm the symbionts include up to two sulfate reducers (Desulfobulbaceae, Desulfobacteraceae), a methanogen (Methanobacteriales), and possibly a Bacteroidete (Cytophaga) and a Type I methanotroph, suggesting synergistic metabolisms in this environment. This case study is discussed in terms of implications to biogeochemistry, and benthic ecology.
    Description: This research was supported by grants from NSF (MCB-0604084 to Virginia P. Edgcomb and Joan M. Bernhard and MCB-0702491 to Joan M. Bernhard, Virginia P. Edgcomb, and K. L. Casciotti).
    Keywords: Ciliate ; Anoxia ; Symbiosis ; TEM ; SSU rRNA ; FISH
    Repository Name: Woods Hole Open Access Server
    Type: Article
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