in

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

  • 1.

    Arndt S, Jørgensen BB, LaRowe DE, Middelburg J, Pancost R, Regnier P. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth Sci Rev. 2013;123:53–86.

    CAS  Article  Google Scholar 

  • 2.

    Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, et al. Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta. 1979;43:1075–90.

    CAS  Article  Google Scholar 

  • 3.

    Calvert S. Oceanographic controls on the accumulation of organic matter in marine sediments. Geol Soc Spec Publ. 1987;26:137–51.

    Article  Google Scholar 

  • 4.

    De Leeuw J, Largeau C. A review of macromolecular organic compounds that comprise living organisms and their role in kerogen, coal, and petroleum formation. Org Geochem. 1993;11:23–72.

  • 5.

    Mackenzie FT, Lerman A, Andersson AJ. Past and present of sediment and carbon biogeochemical cycling models. Biogeosciences. 2004;1:11–32.

    CAS  Article  Google Scholar 

  • 6.

    Oni OE, Miyatake T, Kasten S, Richter-Heitmann T, Fischer D, Wagenknecht L, et al. Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland Mud Area, North Sea. Front Microbiol. 2015;6:365.

    PubMed Central  PubMed  Google Scholar 

  • 7.

    Egger M, Hagens M, Sapart CJ, Dijkstra N, van Helmond NA, Mogollón JM, et al. Iron oxide reduction in methane-rich deep Baltic Sea sediments. Geochim Cosmochim Acta. 2017;207:256–76.

    CAS  Article  Google Scholar 

  • 8.

    Riedinger N, Pfeifer K, Kasten S, Garming JFL, Vogt C, Hensen C. Diagenetic alteration of magnetic signals by anaerobic oxidation of methane related to a change in sedimentation rate. Geochim Cosmoch Acta. 2005;69:4117–26.

    CAS  Article  Google Scholar 

  • 9.

    Riedinger N, Formolo MJ, Lyons TW, Henkel S, Beck A, Kasten S. An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments. Geobiology. 2014;12:172–81.

    CAS  Article  Google Scholar 

  • 10.

    März C, Hoffmann J, Bleil U, De Lange G, Kasten S. Diagenetic changes of magnetic and geochemical signals by anaerobic methane oxidation in sediments of the Zambezi deep-sea fan (SW Indian Ocean). Mar Geol. 2008;255:118–30.

    Article  CAS  Google Scholar 

  • 11.

    Hensen C, Zabel M, Pfeifer K, Schwenk T, Kasten S, Riedinger N, et al. Control of sulfate pore-water profiles by sedimentary events and the significance of anaerobic oxidation of methane for the burial of sulfur in marine sediments. Geochim Cosmochim Acta. 2003;67:2631–47.

    CAS  Article  Google Scholar 

  • 12.

    Flood RD, Piper DJW, Klaus A, Party SS. Initial Reports. Proc. Ocean Drill. Progam. 1995;155. https://doi.org/10.2973/odp.proc.ir.155.1995.

  • 13.

    Kasten S, Freudenthal T, Gingele FX, Schulz HD. Simultaneous formation of iron-rich layers at different redox boundaries in sediments of the Amazon deep-sea fan. Geochim Cosmochim Acta. 1998;62:2253–64.

    CAS  Article  Google Scholar 

  • 14.

    Meyers SR. Production and preservation of organic matter: the significance of iron. Paleoceanography. 2007;22:PA4211.

  • 15.

    Barber A, Brandes J, Leri A, Lalonde K, Balind K, Wirick S, et al. Preservation of organic matter in marine sediments by inner-sphere interactions with reactive iron. Sci Rep. 2017;7:1–10.

    CAS  Article  Google Scholar 

  • 16.

    Lalonde K, Mucci A, Ouellet A, Gélinas Y. Preservation of organic matter in sediments promoted by iron. Nature. 2012;483:198–200.

    CAS  Article  Google Scholar 

  • 17.

    Middelburg JJ. A simple rate model for organic matter decomposition in marine sediments. Geochim Cosmochim Acta. 1989;53:1577–81.

    CAS  Article  Google Scholar 

  • 18.

    Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, et al. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA. 2006;103:3846–51.

    CAS  Article  Google Scholar 

  • 19.

    Aromokeye DA, Kulkarni AC, Elvert M, Wegener G, Henkel S, Coffinet S, et al. Rates and microbial players of iron-driven anaerobic oxidation of methane in methanic marine sediments. Front Microbiol. 2020;10:3041.

    PubMed Central  Article  PubMed  Google Scholar 

  • 20.

    Lovley DR, Phillips EJ. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol. 1986;51:683–9.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 21.

    Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJ, Woodward JC. Humic substances as electron acceptors for microbial respiration. Nature. 1996;382:445–8.

    CAS  Article  Google Scholar 

  • 22.

    Lovley D. Dissimilatory Fe (III)-and Mn (IV)-reducing prokaryotes, In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes. Springer: Berlin Heidelberg; 2006, Vol. 2, p. 635–58.

  • 23.

    Lovley DR, Phillips EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol. 1988;54:1472–80.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 24.

    Kato S, Hashimoto K, Watanabe K. Methanogenesis facilitated by electric syntrophy via (semi) conductive iron‐oxide minerals. Environ Microbiol. 2012;14:1646–54.

    CAS  Article  Google Scholar 

  • 25.

    Jiang S, Park S, Yoon Y, Lee J-H, Wu W-M, Phuoc Dan N, et al. Methanogenesis facilitated by geobiochemical iron cycle in a novel syntrophic methanogenic microbial community. Environ Sci Technol. 2013;47:10078–84.

    CAS  Article  Google Scholar 

  • 26.

    Aromokeye DA, Richter-Heitmann T, Oni O, Emmanuel, Kulkarni A, Yin X, et al. Temperature controls crystalline iron oxide utilization by microbial communities in methanic ferruginous marine sediment incubations. Front Microbiol. 2018;9:2574.

    PubMed Central  Article  PubMed  Google Scholar 

  • 27.

    Zhuang L, Tang J, Wang Y, Hu M, Zhou S. Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. J Hazard Mater. 2015;293:37–45.

    CAS  Article  Google Scholar 

  • 28.

    Hebbeln D, Scheurle C, Lamy F. Depositional history of the Helgoland Mud Area, German Bight, North Sea. Geo Mar Lett. 2003;23:81–90.

    Article  Google Scholar 

  • 29.

    Oni OE, Schmidt F, Miyatake T, Kasten S, Witt M, Hinrichs K-U, et al. Microbial communities and organic matter composition in surface and subsurface sediments of the Helgoland Mud Area, North Sea. Front Microbiol. 2015;6:1290.

    PubMed Central  PubMed  Google Scholar 

  • 30.

    Gan S, Schmidt F, Heuer VB, Goldhammer T, Witt M, Hinrichs K-U. Impacts of redox conditions on dissolved organic matter (DOM) quality in marine sediments off the River Rhône, Western Mediterranean Sea. Geochim Cosmochim Acta. 2020;276:151–69.

    CAS  Article  Google Scholar 

  • 31.

    Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF, Valderrama JA, et al. Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev. 2009;73:71–133.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 32.

    Fuchs G, Boll M, Heider J. Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol. 2011;9:803–16.

    CAS  Article  Google Scholar 

  • 33.

    Gibson J, Harwood SC. Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu Rev Microbiol. 2002;56:345–69.

    CAS  Article  Google Scholar 

  • 34.

    Hopkins BT, McInerney MJ, Warikoo V. Evidence for anaerobic syntrophic benzoate degradation threshold and isolation of the syntrophic benzoate degrader. Appl Environ Microbiol. 1995;61:526.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 35.

    Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev. 1997;61:262–80.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 36.

    Schöcke L, Schink B. Energetics of methanogenic benzoate degradation by Syntrophus gentianae in syntrophic coculture. Microbiology. 1997;143:2345–51.

    Article  Google Scholar 

  • 37.

    Widdel F, Kohring G-W, Mayer F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids III. Characterization of the filamentous gliding Desulfonema limicola gen. nov. sp. nov., and Desulfonema magnum sp. nov. Arch Microbiol. 1983;134:286–94.

    CAS  Article  Google Scholar 

  • 38.

    Widdel F. Anaerober Abbau von Fettsäuren und Benzoesäure durch neu isolierte Arten sulfat-reduzierender Bakterien [PhD Thesis]. Göttingen, Germany: Georg-August-Universität zu Göttingen; 1980.

  • 39.

    Widdel F, Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Arch Microbiol. 1981;129:395–400.

    CAS  Article  Google Scholar 

  • 40.

    Viollier E, Inglett P, Hunter K, Roychoudhury A, Van, Cappellen P. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem. 2000;15:785–90.

    CAS  Article  Google Scholar 

  • 41.

    Heuer VB, Pohlman JW, Torres ME, Elvert M, Hinrichs K-U. The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia Margin. Geochim Cosmochim Acta. 2009;73:3323–36.

    CAS  Article  Google Scholar 

  • 42.

    Lin Y-S, Heuer VB, Goldhammer T, Kellermann MY, Zabel M, Hinrichs K-U. Towards constraining H2 concentration in subseafloor sediment: a proposal for combined analysis by two distinct approaches. Geochim Cosmochim Acta. 2012;77:186–201.

    CAS  Article  Google Scholar 

  • 43.

    Lueders T, Manefield M, Friedrich MW. Enhanced sensitivity of DNA‐and rRNA‐based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol. 2004;6:73–8.

    CAS  Article  Google Scholar 

  • 44.

    Amann R, Fuchs BM, Behrens S. The identification of microorganisms by fluorescence in situ hybridisation. Curr Opin Biotechnol. 2001;12:231–6.

    CAS  Article  Google Scholar 

  • 45.

    Poulton SW, Krom MD, Raiswell R. A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide. Geochim Cosmochim Acta. 2004;68:3703–15.

    CAS  Article  Google Scholar 

  • 46.

    Herndon EM, Yang Z, Bargar J, Janot N, Regier TZ, Graham DE, et al. Geochemical drivers of organic matter decomposition in arctic tundra soils. Biogeochemistry. 2015;126:397–414.

    CAS  Article  Google Scholar 

  • 47.

    Yang Z, Wullschleger SD, Liang L, Graham DE, Gu B. Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil. Soil Biol Biochem. 2016;95:202–11.

    CAS  Article  Google Scholar 

  • 48.

    Yang Z, Shi X, Wang C, Wang L, Guo R. Magnetite nanoparticles facilitate methane production from ethanol via acting as electron acceptors. Sci Rep. 2015;5;16118. https://doi.org/10.1038/srep16118.

  • 49.

    McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJ, Schink B, et al. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci. 2008;1125:58–72.

    CAS  Article  Google Scholar 

  • 50.

    Sieber J, McInerney M, Plugge C, Schink B, Gunsalus R. Methanogenesis: syntrophic metabolism. In: Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology. Springer: Berlin, Heidelberg; 2010. p. 337–55.

  • 51.

    Vandieken V, Mußmann M, Niemann H, Jørgensen BB. Desulfuromonas svalbardensis sp. nov. and Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe(III)-reducing bacteria isolated from Arctic sediments, Svalbard. Int J Syst Evol Microbiol. 2006;56:1133–9.

    CAS  Article  Google Scholar 

  • 52.

    Jones DL, Edwards AC. Influence of sorption on the biological utilization of two simple carbon substrates. Soil Biol Biochem. 1998;30:1895–902.

    CAS  Article  Google Scholar 

  • 53.

    Bray MS, Wu J, Reed BC, Kretz CB, Belli KM, Simister RL, et al. Shifting microbial communities sustain multiyear iron reduction and methanogenesis in ferruginous sediment incubations. Geobiology. 2017;15:678–89.

    CAS  Article  Google Scholar 

  • 54.

    Dolfing J, Tiedje JM. Acetate inhibition of methanogenic, syntrophic benzoate degradation. Appl Environ Microbiol. 1988;54:1871–3.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 55.

    Warikoo V, McInerney MJ, Robinson JA, Suflita JM. Interspecies acetate transfer influences the extent of anaerobic benzoate degradation by syntrophic consortia. Appl Environ Microbiol. 1996;62:26–32.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 56.

    Elshahed MS, McInerney MJ. Benzoate Fermentation by the anaerobic bacterium Syntrophus aciditrophicus in the absence of hydrogen-using microorganisms. Appl Environ Microbiol. 2001;67:5520–5.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 57.

    Watanabe M, Kojima H, Fukui M. Review of Desulfotomaculum species and proposal of the genera Desulfallas gen. nov., Desulfofundulus gen. nov., Desulfofarcimen gen. nov. and Desulfohalotomaculum gen. nov. Int J Syst Evol Microbiol. 2018;68:2891–9.

    CAS  Article  Google Scholar 

  • 58.

    Harwood CS, Burchhardt G, Herrmann H, Fuchs G. Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol Rev. 1998;22:439–58.

    CAS  Article  Google Scholar 

  • 59.

    Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, et al. Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol. 2016;26:5–28.

    CAS  Google Scholar 

  • 60.

    Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV, et al. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ Microbiol. 2013;15:1759–71.

    CAS  Article  Google Scholar 

  • 61.

    Kadnikov VV, Mardanov AV, Podosokorskaya OA, Gavrilov SN, Kublanov IV, Beletsky AV, et al. Genomic analysis of Melioribacter roseus, facultatively anaerobic organotrophic bacterium representing a novel deep lineage within Bacteriodetes/Chlorobi group. PLoS ONE 8:e53047. https://doi.org/10.1371/journal.pone.0053047.

  • 62.

    Zavarzina DG, Sokolova TG, Tourova TP, Chernyh NA, Kostrikina NA, Bonch-Osmolovskaya EA. Thermincola ferriacetica sp. nov., a new anaerobic, thermophilic, facultatively chemolithoautotrophic bacterium capable of dissimilatory Fe(III) reduction. Extremophiles. 2007;11:1–7.

    CAS  Article  Google Scholar 

  • 63.

    Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL, DeSantis TZ, et al. A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J. 2008;2:1146–56.

    CAS  Article  Google Scholar 

  • 64.

    Byrne-Bailey KG, Wrighton KC, Melnyk RA, Agbo P, Hazen TC, Coates JD. Complete genome sequence of the electricity-producing “Thermincola potens” strain JR. J Bacteriol. 2010;192:4078–9.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 65.

    Wrighton KC. Following electron flow: from a gram-positive community to mechanisms of electron transfer. Berkeley, CA, USA: UC Berkeley; 2010.

  • 66.

    Poser A, Lohmayer R, Vogt C, Knoeller K, Planer-Friedrich B, Sorokin D, et al. Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes. Extremophiles. 2013;17:1003–12.

    CAS  Article  Google Scholar 

  • 67.

    Sorokin DY, Tourova TP, Mußmann M, Muyzer G. Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles. 2008;12:431–9.

    CAS  Article  Google Scholar 

  • 68.

    Zhuang L, Tang Z, Ma J, Yu Z, Wang Y, Tang J. Enhanced anaerobic biodegradation of benzoate under sulfate-reducing conditions with conductive iron-oxides in sediment of Pearl River Estuary. Front Microbiol. 2019;10:374.

    PubMed Central  Article  PubMed  Google Scholar 

  • 69.

    Kamagata Y, Kitagawa N, Tasaki M, Nakamura K, Mikami E. Degradation of benzoate by an anaerobic consortium and some properties of a hydrogenotrophic methanogen and sulfate-reducing bacterium in the consortium. J Ferment Bioeng. 1992;73:213–8.

    CAS  Article  Google Scholar 

  • 70.

    Junghare M, Schink B. Desulfoprunum benzoelyticum gen. nov., sp. nov., a gram-negative benzoate-degrading sulfate-reducing bacterium isolated from the wastewater treatment plant. Int J Syst Evol Microbiol. 2015;65:77–84.

    CAS  Article  Google Scholar 

  • 71.

    Oren A. The order Halanaerobiales, and the families Halanaerobiaceae and Halobacteroidaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: firmicutes and tenericutes. Berlin, Heidelberg: Springer Berlin Heidelberg; 2014. p. 153–77.

  • 72.

    Hatamoto M, Imachi H, Yashiro Y, Ohashi A, Harada H. Detection of active butyrate-degrading microorganisms in methanogenic sludges by RNA-based stable isotope probing. Appl Environ Microbiol. 2008;74:3610–4.

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  • 73.

    Nobu MK, Narihiro T, Liu M, Kuroda K, Mei R, Liu WT. Thermodynamically diverse syntrophic aromatic compound catabolism. Environ Microbiol. 2017;19:4576–86.

    CAS  Article  Google Scholar 

  • 74.

    Lentini CJ, Wankel SD, Hansel CM. Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol. 2012;3:404.

    PubMed Central  Article  PubMed  Google Scholar 

  • 75.

    Newsome L, Lopez Adams R, Downie HF, Moore KL, Lloyd JR. NanoSIMS imaging of extracellular electron transport processes during microbial iron(III) reduction. FEMS Microbiol Ecol. 2018;94:fiy104.

  • 76.

    Wang H, Byrne JM, Liu P, Liu J, Dong X, Lu Y. Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei. Environ Microbiol Rep. 2020;12:97–109.

    CAS  Article  Google Scholar 

  • 77.

    Dodsworth JA, Blainey PC, Murugapiran SK, Swingley WD, Ross CA, Tringe SG, et al. Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage. Nat Commun. 2013;4:1854.

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • 78.

    Nobu MK, Dodsworth JA, Murugapiran SK, Rinke C, Gies EA, Webster G, et al. Phylogeny and physiology of candidate phylum ‘Atribacteria’(OP9/JS1) inferred from cultivation-independent genomics. ISME J. 2016;10:273–86.

    CAS  Article  Google Scholar 

  • 79.

    Algora C, Vasileiadis S, Wasmund K, Trevisan M, Krüger M, Puglisi E, et al. Manganese and iron as structuring parameters of microbial communities in Arctic marine sediments from the Baffin Bay. FEMS Microbiol Ecol. 2015;91:fiv056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 80.

    Lehours A-C, Rabiet M, Morel-Desrosiers N, Morel J-P, Jouve L, Arbeille B, et al. Ferric iron reduction by fermentative strain BS2 isolated from an iron-rich anoxic environment (Lake Pavin, France). Geomicrobiol J. 2010;27:714–22.

    CAS  Article  Google Scholar 

  • 81.

    Liu D, Wang H, Dong H, Qiu X, Dong X, Cravotta CA. Mineral transformations associated with goethite reduction by Methanosarcina barkeri. Chem Geol. 2011;288:53–60.

    CAS  Article  Google Scholar 

  • 82.

    Sivan O, Shusta S, Valentine D. Methanogens rapidly transition from methane production to iron reduction. Geobiology. 2016;14:190–203.

    CAS  Article  Google Scholar 

  • 83.

    Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Nat Acad Sci USA. 1998;95:6578–83.

    CAS  Article  Google Scholar 

  • 84.

    Aromokeye AD. Iron oxide driven methanogenesis and methanotrophy in methanic sediments of Helgoland Mud Area, North Sea. Bremen, Germany: Universität Bremen; 2018.


  • Source: Ecology - nature.com

    Reanalysis of putative ovarian follicles suggests that Early Cretaceous birds were feeding not breeding

    Increased mosquito abundance and species richness in Connecticut, United States 2001–2019