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      Effect of Nickel Levels on Hydrogen Partial Pressure and Methane Production in Methanogens

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          Abstract

          Hydrogen (H 2) consumption and methane (CH 4) production in pure cultures of three different methanogens were investigated during cultivation with 0, 0.2 and 4.21 μM added nickel (Ni). The results showed that the level of dissolved Ni in the anaerobic growth medium did not notably affect CH 4 production in the cytochrome-free methanogenic species Methanobacterium bryantii and Methanoculleus bourgensis MAB1, but affected CH 4 formation rate in the cytochrome-containing Methanosarcina barkeri grown on H 2 and CO 2 . Methanosarcina barkeri also had the highest amounts of Ni in its cells, indicating that more Ni is needed by cytochrome-containing than by cytochrome-free methanogenic species. The concentration of Ni affected threshold values of H 2 partial pressure ( pH 2) for all three methanogen species studied, with M. bourgensis MAB1 reaching pH 2 values as low as 0.1 Pa when Ni was available in amounts used in normal anaerobic growth medium. To our knowledge, this is the lowest pH 2 threshold recorded to date in pure methanogen culture, which suggests that M. bourgensis MAB1 have a competitive advantage over other species through its ability to grow at low H 2 concentrations. Our study has implications for research on the H 2-driven deep subsurface biosphere and biogas reactor performance.

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          Most cited references35

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          Methanogenic archaea: ecologically relevant differences in energy conservation.

          Most methanogenic archaea can reduce CO(2) with H(2) to methane, and it is generally assumed that the reactions and mechanisms of energy conservation that are involved are largely the same in all methanogens. However, this does not take into account the fact that methanogens with cytochromes have considerably higher growth yields and threshold concentrations for H(2) than methanogens without cytochromes. These and other differences can be explained by the proposal outlined in this Review that in methanogens with cytochromes, the first and last steps in methanogenesis from CO(2) are coupled chemiosmotically, whereas in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.
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            Inhibition of anaerobic digestion process: a review.

            Anaerobic digestion is an attractive waste treatment practice in which both pollution control and energy recovery can be achieved. Many agricultural and industrial wastes are ideal candidates for anaerobic digestion because they contain high levels of easily biodegradable materials. Problems such as low methane yield and process instability are often encountered in anaerobic digestion, preventing this technique from being widely applied. A wide variety of inhibitory substances are the primary cause of anaerobic digester upset or failure since they are present in substantial concentrations in wastes. Considerable research efforts have been made to identify the mechanism and the controlling factors of inhibition. This review provides a detailed summary of the research conducted on the inhibition of anaerobic processes. The inhibitors commonly present in anaerobic digesters include ammonia, sulfide, light metal ions, heavy metals, and organics. Due to the difference in anaerobic inocula, waste composition, and experimental methods and conditions, literature results on inhibition caused by specific toxicants vary widely. Co-digestion with other waste, adaptation of microorganisms to inhibitory substances, and incorporation of methods to remove or counteract toxicants before anaerobic digestion can significantly improve the waste treatment efficiency.
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              Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage.

              Most methanogenic archaea reduce CO(2) with H(2) to CH(4). For the activation of H(2), they use different [NiFe]-hydrogenases, namely energy-converting [NiFe]-hydrogenases, heterodisulfide reductase-associated [NiFe]-hydrogenase or methanophenazine-reducing [NiFe]-hydrogenase, and F(420)-reducing [NiFe]-hydrogenase. The energy-converting [NiFe]-hydrogenases are phylogenetically related to complex I of the respiratory chain. Under conditions of nickel limitation, some methanogens synthesize a nickel-independent [Fe]-hydrogenase (instead of F(420)-reducing [NiFe]-hydrogenase) and by that reduce their nickel requirement. The [Fe]-hydrogenase harbors a unique iron-guanylylpyridinol cofactor (FeGP cofactor), in which a low-spin iron is ligated by two CO, one C(O)CH(2)-, one S-CH(2)-, and a sp(2)-hybridized pyridinol nitrogen. Ligation of the iron is thus similar to that of the low-spin iron in the binuclear active-site metal center of [NiFe]- and [FeFe]-hydrogenases. Putative genes for the synthesis of the FeGP cofactor have been identified. The formation of methane from 4 H(2) and CO(2) catalyzed by methanogenic archaea is being discussed as an efficient means to store H(2).
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 December 2016
                2016
                : 11
                : 12
                : e0168357
                Affiliations
                [1 ]Department of Geological Sciences, Stockholm University, Stockholm, Sweden
                [2 ]Department of Physical Sciences, The Open University, Milton Keynes, United Kingdom
                [3 ]Department of Microbiology, BioCenter, Swedish University of Agricultural Sciences, Uppsala, Sweden
                Martin-Luther-Universitat Halle-Wittenberg, GERMANY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: AN.

                • Data curation: AN AS AP NC SS.

                • Formal analysis: AN.

                • Funding acquisition: AN AS.

                • Investigation: AN.

                • Methodology: AN AS.

                • Project administration: AN.

                • Resources: AN AS.

                • Supervision: AN AS.

                • Validation: AN AS.

                • Visualization: AN.

                • Writing – original draft: AN.

                • Writing – review & editing: AN AS AP NC SS.

                Author information
                http://orcid.org/0000-0002-1291-5529
                Article
                PONE-D-16-30245
                10.1371/journal.pone.0168357
                5161503
                27992585
                9d6824ae-3d02-4fe6-acec-f8a964bb3623
                © 2016 Neubeck et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 July 2016
                : 30 November 2016
                Page count
                Figures: 4, Tables: 3, Pages: 19
                Funding
                Funded by: Formas
                Award ID: 2012-807
                Funded by: funder-id http://dx.doi.org/10.13039/501100001859, Swedish National Space Board;
                Award ID: DNR-100/13
                Award Recipient :
                Funded by: Royal Swedish Academy of Sciences.
                This work was supported by the Swedish National Space Board (Project number DNR-100/13) ( http://www.rymdstyrelsen.se/), the Royal Swedish Academy of Sciences ( http://www.kva.se/), and Formas (2012-807) ( http://www.formas.se/).
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Archaeans
                Methanogens
                Biology and Life Sciences
                Organisms
                Fungi
                Yeast
                Physical Sciences
                Physics
                Classical Mechanics
                Pressure
                Partial Pressure
                Research and Analysis Methods
                Biological Cultures
                Cell Culturing Techniques
                Pure Culture
                Physical Sciences
                Chemistry
                Chemical Compounds
                Carbon Dioxide
                Physical Sciences
                Chemistry
                Chemical Compounds
                Methane
                Physical Sciences
                Chemistry
                Analytical Chemistry
                Trace Elements
                Physical Sciences
                Chemistry
                Chemical Elements
                Nickel
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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                Uncategorized

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