{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T00:11:04Z","timestamp":1790208664410,"version":"4.1.0"},"reference-count":78,"publisher":"National Academy of Sciences","issue":"17","license":[{"start":{"date-parts":[[2024,4,15]],"date-time":"2024-04-15T00:00:00Z","timestamp":1713139200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"name":"NSF EAR","award":["1829695"],"award-info":[{"award-number":["1829695"]}]},{"DOI":"10.13039\/100000104","name":"NASA","doi-asserted-by":"crossref","award":["80NSSC18K1139 RK558-G2"],"award-info":[{"award-number":["80NSSC18K1139 RK558-G2"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000104","name":"NASA","doi-asserted-by":"crossref","award":["80NSSC20K0228"],"award-info":[{"award-number":["80NSSC20K0228"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000104","name":"NASA","doi-asserted-by":"crossref","award":["NNH22ZDA001N"],"award-info":[{"award-number":["NNH22ZDA001N"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2024,4,23]]},"abstract":"<jats:p>\n                    The main sources of redox gradients supporting high-productivity life in the Europan and other icy ocean world oceans were proposed to be photolytically derived oxidants, such as reactive oxygen species (ROS) from the icy shell, and reductants (Fe(II), S(-II), CH\n                    <jats:sub>4<\/jats:sub>\n                    , H\n                    <jats:sub>2<\/jats:sub>\n                    ) from bottom waters reacting with a (ultra)mafic seafloor. Important roadblocks to maintaining life, however, are that the degree of ocean mixing to combine redox species is unknown, and ROS damage biomolecules. Here, we envisage a unique solution using an acid mine drainage (AMD)-filled pit lakes analog system for the Europan ocean, which previous models predicted to be acidic. We hypothesize that surface-generated ROS oxidize dissolved Fe(II) resulting in Fe(III) (hydr)oxide precipitates, that settle to the seafloor as \u201ciron snow.\u201d The iron snow provides a respiratory substrate for anaerobic microorganisms (\u201cbreathing iron\u201d), and limits harmful ROS exposure since they are now neutralized at the ice-water interface. Based on this scenario, we calculated Gibbs energies and maximal biomass productivities of various anaerobic metabolisms for a range of pH, temperatures, and H\n                    <jats:sub>2<\/jats:sub>\n                    fluxes. Productivity by iron reducers was greater for most environmental conditions considered, whereas sulfate reducers and methanogens were more favored at high pH. Participation of Fe in the metabolic redox processes is largely neglected in most models of Europan biogeochemistry. Our model overcomes important conceptual roadblocks to life in icy ocean worlds and broadens the potential metabolic diversity, thus increasing total primary productivity, the diversity and volume of habitable environmental niches and, ultimately, the probability of biosignature detection.\n                  <\/jats:p>","DOI":"10.1073\/pnas.2316452121","type":"journal-article","created":{"date-parts":[[2024,4,15]],"date-time":"2024-04-15T15:06:53Z","timestamp":1713193613000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":12,"title":["Bioenergetics of iron snow fueling life on Europa"],"prefix":"10.1073","volume":"121","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3852-0557","authenticated-orcid":false,"given":"Nita","family":"Sahai","sequence":"first","affiliation":[{"name":"School of Polymer Science and Polymer Engineering, The University of Akron, Akron, OH 44325"},{"name":"Department of Geosciences, The University of Akron, Akron, OH 44325"},{"name":"Department of Biology, The University of Akron, Akron, OH 44325"},{"name":"Integrated Biosciences Program, The University of Akron, Akron, OH 44325"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Doug","family":"LaRowe","sequence":"additional","affiliation":[{"name":"Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5854-0497","authenticated-orcid":false,"given":"John M.","family":"Senko","sequence":"additional","affiliation":[{"name":"Department of Geosciences, The University of Akron, Akron, OH 44325"},{"name":"Department of Biology, The University of Akron, Akron, OH 44325"},{"name":"Integrated Biosciences Program, The University of Akron, Akron, OH 44325"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2024,4,15]]},"reference":[{"key":"e_1_3_5_1_2","volume-title":"NASA Astrobiology Strategy","author":"Hayes L.","year":"2015","unstructured":"L. Hayes , NASA Astrobiology Strategy (NASA, 2015)."},{"key":"e_1_3_5_2_2","volume-title":"Europa","author":"Hand K. P.","year":"2009","unstructured":"K. P. Hand, C. F. Chyba, J. C. Priscu, R. W. Carlson, K. H. Nealson, \"Astrobiology and the potential for life on Europa\" in Europa, R. T. Pappalardo, W. B. McKinnon, K. Khurana, Eds. (University of Arizona Press, 2009)."},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/386765a0"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1038\/35000281"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.3847\/PSJ\/abfb7a"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1086\/587141"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1002\/2013JE004512"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1002\/2017JE005341"},{"key":"e_1_3_5_9_2","volume-title":"Europa","author":"McKinnon W. B.","year":"2009","unstructured":"W. B. McKinnon, R. T. Pappalardo, K. K. Khurana, \"Europa: Perspectives on an ocean world\" in Europa, R. T. Pappalardo, W. B. McKinnon, K. K. Khurana, Eds. (University of Arizona Press, 2009)."},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.284.5420.1631"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1029\/1999JE001126"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1006\/icar.2000.6471"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1029\/2003JE002194"},{"key":"e_1_3_5_14_2","volume-title":"Europa","author":"Zolotov M. Y.","year":"2009","unstructured":"M. Y. Zolotov, J. S. Kargel, \u201cOn the chemical composition of Europa\u2019s icy shell, ocean and underlying rocks\u201d in Europa, R. T. Pappalardo, W. B. McKinnon, K. K. Khurana, Eds. (University of Arizona Press, 2009)."},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2011.0666"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11214-010-9646-y"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1002\/2016GL068547"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2016.1600"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2009.0386"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.1029\/2020GL090077"},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature14262"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1029\/2019GL085885"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1029\/2021GL094143"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.283.5410.2062"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1086\/344307"},{"key":"e_1_3_5_26_2","volume-title":"Jupiter: The Planet, Satellites and Magnetosphere","author":"Johnson R. E.","year":"2004","unstructured":"R. E. Johnson , \u201cRadiation effects on the surfaces of the Gallilean satellite surfaces\u201d in Jupiter: The Planet, Satellites and Magnetosphere, F. Beganal, T. E. Dowling, W. B. McKinnon, Eds. (Cambridge University Press, 2004)."},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2007.0156"},{"key":"e_1_3_5_28_2","volume-title":"Europa","author":"Carlson R. W.","year":"2009","unstructured":"R. W. Carlson , \u201cEuropa\u2019s surface composition\u201d in Europa, R. T. Pappalardo, W. B. McKinnon, K. K. Khurana, Eds. (University of Arizona Press, 2009)."},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41550-021-01393-1"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.98.3.801"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.icarus.2007.02.002"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.3847\/PSJ\/aca275"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.adf3955"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.1089\/153110703322736105"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.icarus.2003.11.026"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.2475\/03.2020.01"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1029\/1999JE900005"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1038\/27394"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1029\/2002JE001966"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1029\/2000JE001413"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.1089\/153110703322736150"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.1088\/0004-6256\/145\/4\/110"},{"key":"e_1_3_5_43_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-023-05987-9"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2201388119"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.1093\/mnras\/stz2280"},{"key":"e_1_3_5_46_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.icarus.2020.114248"},{"key":"e_1_3_5_47_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2007.0075"},{"key":"e_1_3_5_48_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.270.5235.450"},{"key":"e_1_3_5_49_2","doi-asserted-by":"publisher","DOI":"10.2138\/rmg.2013.75.18"},{"key":"e_1_3_5_50_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2017.111"},{"key":"e_1_3_5_51_2","doi-asserted-by":"crossref","unstructured":"M. C. Cook J. G. Blank S. Suzuki K. H. Nealson P. L. Morrill Microbial metabolism at three terrestrial sites of serpentinization: The Tablelands (NL CAN) The Cedars (CA USA) and Aqua de Ney (CA USA). JGR Biogeosci. 126 e2019JG005542 (2021).","DOI":"10.1029\/2019JG005542"},{"key":"e_1_3_5_52_2","doi-asserted-by":"publisher","DOI":"10.1128\/mSystems.00300-21"},{"key":"e_1_3_5_53_2","doi-asserted-by":"publisher","DOI":"10.2475\/03.2011.01"},{"key":"e_1_3_5_54_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2015.227"},{"key":"e_1_3_5_55_2","doi-asserted-by":"publisher","DOI":"10.1021\/acsearthspacechem.9b00016"},{"key":"e_1_3_5_56_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.epsl.2012.12.008"},{"key":"e_1_3_5_57_2","doi-asserted-by":"publisher","DOI":"10.1089\/ast.2011.0776"},{"key":"e_1_3_5_58_2","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jpcc.9b10127"},{"key":"e_1_3_5_59_2","first-page":"175","article-title":"Adaptive response to oxidative stress: Bacteria, fungi, plants, and animals","volume":"153","author":"Luschak V. I.","year":"2011","unstructured":"V. I. Luschak, Adaptive response to oxidative stress: Bacteria, fungi, plants, and animals. Compar. Biochem. Physiol. C 153, 175\u2013190 (2011).","journal-title":"Compar. Biochem. Physiol. C"},{"key":"e_1_3_5_60_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro.2017.26"},{"key":"e_1_3_5_61_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.14445"},{"key":"e_1_3_5_62_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2014.00215"},{"key":"e_1_3_5_63_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0213807"},{"key":"e_1_3_5_64_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01194-07"},{"key":"e_1_3_5_65_2","doi-asserted-by":"publisher","DOI":"10.4319\/lo.2011.56.4.1386"},{"key":"e_1_3_5_66_2","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.000205"},{"key":"e_1_3_5_67_2","doi-asserted-by":"publisher","DOI":"10.3389\/feart.2019.00180"},{"key":"e_1_3_5_68_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1921042117"},{"key":"e_1_3_5_69_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1472-4669.2005.00045.x"},{"key":"e_1_3_5_70_2","first-page":"522","article-title":"Relationships between the cell volume and the carbon content of bacteria","volume":"50","author":"Romanova N. D.","year":"2010","unstructured":"N. D. Romanova, A. F. Sazhin, Relationships between the cell volume and the carbon content of bacteria. Oceanography 50, 522\u2013530 (2010).","journal-title":"Oceanography"},{"key":"e_1_3_5_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0016-7037(97)00241-X"},{"key":"e_1_3_5_72_2","doi-asserted-by":"publisher","DOI":"10.1029\/2018JG004679"},{"key":"e_1_3_5_73_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jhydrol.2013.08.007"},{"key":"e_1_3_5_74_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02919-14"},{"key":"e_1_3_5_75_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2016.03.004"},{"key":"e_1_3_5_76_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.watres.2021.117739"},{"key":"e_1_3_5_77_2","unstructured":"T. J. Wolery USDOE EQ3\/6 A software package for geochemical modeling. Computer software. https:\/\/www.osti.gov\/\/servlets\/purl\/1231666. USDOE. 13 December 2010. 10.11578\/dc.20210416.44."},{"key":"e_1_3_5_78_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.gca.2011.01.020"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2316452121","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,22]],"date-time":"2024-04-22T16:18:30Z","timestamp":1713802710000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2316452121"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,15]]},"references-count":78,"journal-issue":{"issue":"17","published-print":{"date-parts":[[2024,4,23]]}},"alternative-id":["10.1073\/pnas.2316452121"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2316452121","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,15]]},"assertion":[{"value":"2023-09-21","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-03-11","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-04-15","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2316452121"}}