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      Enrichment of intracellular sulphur cycle –associated bacteria in intertidal benthic foraminifera revealed by 16S and aprA gene analysis

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          Abstract

          Benthic foraminifera are known to play an important role in marine carbon and nitrogen cycles. Here, we report an enrichment of sulphur cycle -associated bacteria inside intertidal benthic foraminifera ( Ammonia sp. (T6), Haynesina sp. (S16) and Elphidium sp. (S5)), using a metabarcoding approach targeting the 16S rRNA and aprA -genes. The most abundant intracellular bacterial groups included the genus Sulfurovum and the order Desulfobacterales. The bacterial 16S OTUs are likely to originate from the sediment bacterial communities, as the taxa found inside the foraminifera were also present in the sediment. The fact that 16S rRNA and aprA –gene derived intracellular bacterial OTUs were species-specific and significantly different from the ambient sediment community implies that bacterivory is an unlikely scenario, as benthic foraminifera are known to digest bacteria only randomly. Furthermore, these foraminiferal species are known to prefer other food sources than bacteria. The detection of sulphur-cycle related bacterial genes in this study suggests a putative role for these bacteria in the metabolism of the foraminiferal host. Future investigation into environmental conditions under which transcription of S-cycle genes are activated would enable assessment of their role and the potential foraminiferal/endobiont contribution to the sulphur-cycle.

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          Methods of Seawater Analysis

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            Evidence for complete denitrification in a benthic foraminifer.

            Benthic foraminifera are unicellular eukaryotes found abundantly in many types of marine sediments. Many species survive and possibly reproduce in anoxic habitats, but sustainable anaerobic metabolism has not been previously described. Here we demonstrate that the foraminifer Globobulimina pseudospinescens accumulates intracellular nitrate stores and that these can be respired to dinitrogen gas. The amounts of nitrate detected are estimated to be sufficient to support respiration for over a month. In a Swedish fjord sediment where G. pseudospinescens is the dominant foraminifer, the intracellular nitrate pool in this species accounted for 20% of the large, cell-bound, nitrate pool present in an oxygen-free zone. Similarly high nitrate concentrations were also detected in foraminifera Nonionella cf. stella and a Stainforthia species, the two dominant benthic taxa occurring within the oxygen minimum zone of the continental shelf off Chile. Given the high abundance of foraminifera in anoxic marine environments, these new findings suggest that foraminifera may play an important role in global nitrogen cycling and indicate that our understanding of the complexity of the marine nitrogen cycle is far from complete.
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              The Santa Barbara Basin is a symbiosis oasis.

              It is generally agreed that the origin and initial diversification of Eucarya occurred in the late Archaean or Proterozoic Eons when atmospheric oxygen levels were low and the risk of DNA damage due to ultraviolet radiation was high. Because deep water provides refuge against ultraviolet radiation and early eukaryotes may have been aerotolerant anaerobes, deep-water dysoxic environments are likely settings for primeval eukaryotic diversification. Fossil evidence shows that deep-sea microbial mats, possibly of sulphur bacteria similar to Beggiatoa, existed during that time. Here we report on the eukaryotic community of a modern analogue, the Santa Barbara Basin (California, USA). The Beggiatoa mats of these severely dysoxic and sulphidic sediments support a surprisingly abundant protistan and metazoan meiofaunal community, most members of which harbour prokaryotic symbionts. Many of these taxa are new to science, and both microaerophilic and anaerobic taxa appear to be represented. Compared with nearby aerated sites, the Santa Barbara Basin is a 'symbiosis oasis' offering a new source of organisms for testing symbiosis hypotheses of eukaryogenesis.
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                Author and article information

                Contributors
                iines.salonen@helsinki.fi
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                12 August 2019
                12 August 2019
                2019
                : 9
                : 11692
                Affiliations
                [1 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, University of Helsinki, Faculty of Biological and Environmental Sciences, Ecosystems and Environment Research Program, P.O. Box 65 (Viikinkaari 1), FI-00014 University of Helsinki, ; Helsinki, Finland
                [2 ]ISNI 0000 0001 2248 4331, GRID grid.11918.30, University of Stirling, Biological and Environmental Sciences, FK9 ALA, ; Stirling, United Kingdom
                [3 ]ISNI 0000 0001 2227 4609, GRID grid.10914.3d, Department of Ocean Systems, , NIOZ-Royal Netherlands Institute for Sea Research and Utrecht University, ; Den Burg, The Netherlands
                [4 ]ISNI 0000000120346234, GRID grid.5477.1, Department of Earth Sciences – Geochemistry, Faculty of Geosciences, , Utrecht University, ; P.O. Box 80.021, 3508 TA Utrecht, The Netherlands
                Author information
                http://orcid.org/0000-0002-4951-9319
                Article
                48166
                10.1038/s41598-019-48166-5
                6690927
                31406214
                babc18d9-ce20-434b-8b58-42b324241d89
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 April 2019
                : 30 July 2019
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                © The Author(s) 2019

                Uncategorized
                biogeochemistry,ocean sciences,microbial ecology
                Uncategorized
                biogeochemistry, ocean sciences, microbial ecology

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