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      Methane- and dissolved organic carbon-fueled microbial loop supports a tropical subterranean estuary ecosystem

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          Abstract

          Subterranean estuaries extend inland into density-stratified coastal carbonate aquifers containing a surprising diversity of endemic animals (mostly crustaceans) within a highly oligotrophic habitat. How complex ecosystems (termed anchialine) thrive in this globally distributed, cryptic environment is poorly understood. Here, we demonstrate that a microbial loop shuttles methane and dissolved organic carbon (DOC) to higher trophic levels of the anchialine food web in the Yucatan Peninsula (Mexico). Methane and DOC production and consumption within the coastal groundwater correspond with a microbial community capable of methanotrophy, heterotrophy, and chemoautotrophy, based on characterization by 16S rRNA gene amplicon sequencing and respiratory quinone composition. Fatty acid and bulk stable carbon isotope values of cave-adapted shrimp suggest that carbon from methanotrophic bacteria comprises 21% of their diet, on average. These findings reveal a heretofore unrecognized subterranean methane sink and contribute to our understanding of the carbon cycle and ecosystem function of karst subterranean estuaries.

          Abstract

          It remains unclear how oligotrophic habitats in subterranean estuaries sustain complex ecosystems. Here, using stable isotopic evidence from organic matter and pelagic shrimp, the authors show that a microbial loop fuelled by methane and dissolved organic carbon sustains the anchialine food web.

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          Submarine thermal sprirngs on the galapagos rift.

          The submarine hydrothermal activity on and near the Galápagos Rift has been explored with the aid of the deep submersible Alvin. Analyses of water samples from hydrothermal vents reveal that hydrothermal activity provides significant or dominant sources and sinks for several components of seawater; studies of conductive and convective heat transfer suggest that two-thirds of the heat lost from new oceanic lithosphere at the Galápagos Rift in the first million years may be vented from thermal springs, predominantly along the axial ridge within the rift valley. The vent areas are populated by animal communities. They appear to utilize chemosynthesis by sulfur-oxidizing bacteria to derive their entire energy supply from reactions between the seawater and the rocks at high temperatures, rather than photosynthesis.
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            A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast.

            Nitrogen cycling is normally thought to dominate the biogeochemistry and microbial ecology of oxygen-minimum zones in marine environments. Through a combination of molecular techniques and process rate measurements, we showed that both sulfate reduction and sulfide oxidation contribute to energy flux and elemental cycling in oxygen-free waters off the coast of northern Chile. These processes may have been overlooked because in nature, the sulfide produced by sulfate reduction immediately oxidizes back to sulfate. This cryptic sulfur cycle is linked to anammox and other nitrogen cycling processes, suggesting that it may influence biogeochemical cycling in the global ocean.
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              Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication.

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                Author and article information

                Contributors
                david.brankovits@gmail.com
                jpohlman@usgs.gov
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                28 November 2017
                28 November 2017
                2017
                : 8
                : 1835
                Affiliations
                [1 ]GRID grid.264764.5, Department of Marine Biology, , Texas A&M University at Galveston, ; Galveston, TX 77553 USA
                [2 ]U.S. Geological Survey, Woods Hole Coastal and Marine Science Center, Woods Hole, MA 02543 USA
                [3 ]ISNI 0000 0004 1937 0642, GRID grid.6612.3, Department of Environmental Sciences, , University of Basel, ; Basel, 4056 Switzerland
                [4 ]ISNI 0000 0001 2227 4609, GRID grid.10914.3d, Department of Marine Microbiology and Biogeochemistry, , NIOZ Royal Netherlands Institute for Sea Research, ; 1790 AB Den Burg, Netherlands
                [5 ]ISNI 0000 0004 1936 981X, GRID grid.70738.3b, Institute of Arctic Biology, , University of Alaska Fairbanks, ; Fairbanks, AK 99775 USA
                [6 ]U.S. Geological Survey, GMEG Science Center, Menlo Park, CA 94025 USA
                [7 ]ISNI 0000 0004 0504 7510, GRID grid.56466.37, Department of Marine Chemistry and Geochemistry, , Woods Hole Oceanographic Institution, ; Woods Hole, MA 02543 USA
                [8 ]ISNI 0000 0001 2159 0001, GRID grid.9486.3, Institute of Biology, National Autonomous University of Mexico (UNAM), ; 04510 Mexico, D.F. Mexico
                [9 ]Speleotech, Tulum, 77780 Quintana Roo Mexico
                [10 ]GRID grid.473786.9, Centre for Arctic Gas Hydrate (CAGE), ; 9037 Tromsø, Norway
                Author information
                http://orcid.org/0000-0001-9195-8115
                http://orcid.org/0000-0002-3563-4586
                http://orcid.org/0000-0002-3468-8304
                http://orcid.org/0000-0002-0414-9350
                http://orcid.org/0000-0001-6496-8094
                http://orcid.org/0000-0001-6317-1884
                http://orcid.org/0000-0002-4342-5960
                http://orcid.org/0000-0003-0626-5942
                Article
                1776
                10.1038/s41467-017-01776-x
                5703975
                29180666
                30179bd0-9ce2-4c05-bc74-167912287081
                © The Author(s) 2017

                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
                : 2 February 2017
                : 16 October 2017
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