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      Food-Web Complexity in Guaymas Basin Hydrothermal Vents and Cold Seeps

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          Abstract

          In the Guaymas Basin, the presence of cold seeps and hydrothermal vents in close proximity, similar sedimentary settings and comparable depths offers a unique opportunity to assess and compare the functioning of these deep-sea chemosynthetic ecosystems. The food webs of five seep and four vent assemblages were studied using stable carbon and nitrogen isotope analyses. Although the two ecosystems shared similar potential basal sources, their food webs differed: seeps relied predominantly on methanotrophy and thiotrophy via the Calvin-Benson-Bassham (CBB) cycle and vents on petroleum-derived organic matter and thiotrophy via the CBB and reductive tricarboxylic acid (rTCA) cycles. In contrast to symbiotic species, the heterotrophic fauna exhibited high trophic flexibility among assemblages, suggesting weak trophic links to the metabolic diversity of chemosynthetic primary producers. At both ecosystems, food webs did not appear to be organised through predator-prey links but rather through weak trophic relationships among co-occurring species. Examples of trophic or spatial niche differentiation highlighted the importance of species-sorting processes within chemosynthetic ecosystems. Variability in food web structure, addressed through Bayesian metrics, revealed consistent trends across ecosystems. Food-web complexity significantly decreased with increasing methane concentrations, a common proxy for the intensity of seep and vent fluid fluxes. Although high fluid-fluxes have the potential to enhance primary productivity, they generate environmental constraints that may limit microbial diversity, colonisation of consumers and the structuring role of competitive interactions, leading to an overall reduction of food-web complexity and an increase in trophic redundancy. Heterogeneity provided by foundation species was identified as an additional structuring factor. According to their biological activities, foundation species may have the potential to partly release the competitive pressure within communities of low fluid-flux habitats. Finally, ecosystem functioning in vents and seeps was highly similar despite environmental differences (e.g. physico-chemistry, dominant basal sources) suggesting that ecological niches are not specifically linked to the nature of fluids. This comparison of seep and vent functioning in the Guaymas basin thus provides further supports to the hypothesis of continuity among deep-sea chemosynthetic ecosystems.

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          Abyssal food limitation, ecosystem structure and climate change.

          The abyssal seafloor covers more than 50% of the Earth and is postulated to be both a reservoir of biodiversity and a source of important ecosystem services. We show that ecosystem structure and function in the abyss are strongly modulated by the quantity and quality of detrital food material sinking from the surface ocean. Climate change and human activities (e.g. successful ocean fertilization) will alter patterns of sinking food flux to the deep ocean, substantially impacting the structure, function and biodiversity of abyssal ecosystems. Abyssal ecosystem response thus must be considered in assessments of the environmental impacts of global warming and ocean fertilization.
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            Beyond the Calvin cycle: autotrophic carbon fixation in the ocean.

            Organisms capable of autotrophic metabolism assimilate inorganic carbon into organic carbon. They form an integral part of ecosystems by making an otherwise unavailable form of carbon available to other organisms, a central component of the global carbon cycle. For many years, the doctrine prevailed that the Calvin-Benson-Bassham (CBB) cycle is the only biochemical autotrophic CO2 fixation pathway of significance in the ocean. However, ecological, biochemical, and genomic studies carried out over the last decade have not only elucidated new pathways but also shown that autotrophic carbon fixation via pathways other than the CBB cycle can be significant. This has ramifications for our understanding of the carbon cycle and energy flow in the ocean. Here, we review the recent discoveries in the field of autotrophic carbon fixation, including the biochemistry and evolution of the different pathways, as well as their ecological relevance in various oceanic ecosystems.
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              Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems.

              Mixing of hydrothermal fluids and seawater at the ocean floor, combined with slow reaction kinetics for oxidation/reduction reactions, provides a source of metabolic energy for chemolithotrophic microorganisms which are the primary biomass producers for an extensive submarine ecosystem that is essentially independent of photosynthesis. Thermodynamic models are used to explore geochemical constraints on the amount of metabolic energy potentially available from chemosynthetic reactions involving S, C, Fe, and Mn compounds during mixing of hydrothermal fluids with seawater. For the vent fluid used in the calculations (EPR 21 degrees N OBS), the model indicates that mixing environments are favorable for oxidation of H2S, CH4, Fe2+ and Mn2+ only below approximately 38 degrees C, with methanogenesis and reduction of sulfate or S degrees favored at higher temperatures, suggesting that environments dominated by mixing provide habitats for mesophilic (but not thermophilic) aerobes and thermophilic (but not mesophilic) anaerobes. A maximum of approximately 760 cal per kilogram vent fluid is available from sulfide oxidation while between 8 and 35 cal/kg vent fluid is available from methanotrophy, methanogenesis, oxidation of Fe or Mn, or sulfate reduction. The total potential for chemosynthetic primary production at deep-sea hydrothermal vents globally is estimated to be about 10(13) g biomass per year, which represents approximately 0.02% of the global primary production by photosynthesis in the oceans. Thermophilic methanogens and sulfate- and S degree-reducers are likely to be the predominant organisms in the walls of vent chimneys and in the diffuse mixing zones beneath warm vents, where biological processes may contribute to the high methane concentrations of vent fluids and heavy 34S/32S ratios of vent sulfide minerals. The metabolic processes taking place in these systems may be analogs of the first living systems to evolve on the Earth.
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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
                28 September 2016
                2016
                : 11
                : 9
                : e0162263
                Affiliations
                [1 ]Laboratoire Environnement Profond, REM/EEP, Institut Carnot Ifremer EDROME, Centre de Bretagne, Plouzané, France
                [2 ]Laboratoire Ecologie Benthique, DYNECO, Ifremer, Centre de Bretagne, Plouzané, France
                [3 ]Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City D.F., Mexico
                [4 ]GEOTOP and Chemistry and Biochemistry Department, Concordia University, Montréal, Québec, Canada
                Stockholm University, SWEDEN
                Author notes

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

                • Conceptualization: MP JS KO LM.

                • Data curation: MP JS KO.

                • Formal analysis: MP LM.

                • Funding acquisition: JS KO.

                • Investigation: MP JS KO EEB.

                • Methodology: MP JS KO LM YG SFD EEB.

                • Project administration: JS KO.

                • Resources: JS KO YG SFD.

                • Supervision: JS KO.

                • Validation: MP JS KO.

                • Visualization: MP.

                • Writing – original draft: MP.

                • Writing – review & editing: MP JS KO LM YG SFD EEB.

                Author information
                http://orcid.org/0000-0002-8128-6922
                Article
                PONE-D-15-46237
                10.1371/journal.pone.0162263
                5040445
                27683216
                e5ec26f9-6220-4dfe-b36d-d753dc6e02d9
                © 2016 Portail 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
                : 21 October 2015
                : 20 August 2016
                Page count
                Figures: 10, Tables: 7, Pages: 33
                Funding
                Funded by: This study was supported by the "Laboratoire d'Excellence" LabexMER (ANR-10-LABX-19) and co-funded by a grant from the French government under the program "Investissements d'Avenir" scheme, and by a grant from the Brittany Regional Council of Brittany
                Award Recipient :
                MP PhD fellowship was supported by the "Laboratoire d'Excellence" LabexMER (ANR-10-LABX-19) and co-funded by a grant from the French government under the program "Investissements d'Avenir" scheme, and by a grant from the Regional Council of Brittany. The cruise was funded by IFREMER (France) and held a work permit for study in Mexican waters (DAPA/2/281009/3803, 28 October 2009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Community Ecology
                Food Web Structure
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Food Web Structure
                Biology and Life Sciences
                Ecology
                Ecosystems
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Biology and Life Sciences
                Ecology
                Ecosystems
                Ecosystem Functioning
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Ecosystem Functioning
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Geology
                Hydrothermal Vents
                Physical Sciences
                Chemistry
                Chemical Compounds
                Methane
                Biology and Life Sciences
                Ecology
                Ecological Niches
                Ecology and Environmental Sciences
                Ecology
                Ecological Niches
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Physical Sciences
                Physics
                Particle Physics
                Composite Particles
                Atoms
                Isotopes
                Stable Isotopes
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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