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Iron is not everything: unexpected complex metabolic responses between iron-cycling microorganisms

  • 1.

    Ponomarova O, Patil KR. Metabolic interactions in microbial communities: untangling the Gordian knot. Curr Opin Microbiol. 2015;27:37–44.

    PubMed  Google Scholar 

  • 2.

    D’Souza G, Shitut S, Preussger D, Yousif G, Waschina S, Kost C. Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat Prod Rep. 2018;35:455–88.

    PubMed  Google Scholar 

  • 3.

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 4.

    Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA. 2008;105:7052–7.

    CAS  PubMed  Google Scholar 

  • 5.

    Men Y, Feil H, Verberkmoes NC, Shah MB, Johnson DR, Lee PKH, et al. Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses. ISME J. 2012;6:410–21.

    CAS  PubMed  Google Scholar 

  • 6.

    Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci USA. 2015;112:6449–54.

    CAS  PubMed  Google Scholar 

  • 7.

    Marchal M, Goldschmidt F, Derksen-Müller SN, Panke S, Ackermann M, Johnson DR. A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations. BMC Evol Biol. 2017;17:106.

    PubMed  PubMed Central  Google Scholar 

  • 8.

    Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science. 2012;337:1546–50.

    CAS  PubMed  Google Scholar 

  • 9.

    Zengler K, Palsson BO. A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol. 2012;10:366–72.

    CAS  PubMed  Google Scholar 

  • 10.

    Sachs JL, Hollowell AC. The origins of cooperative bacterial communities. MBio. 2012;3:1–3.

  • 11.

    Johnson DR, Goldschmidt F, Lilja EE, Ackermann M. Metabolic specialization and the assembly of microbial communities. ISME J. 2012;6:1985–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 12.

    Bull JJ, Rice WR. Distinguishing mechanisms for the evolution of co-operation. J Theor Biol. 1991;149:63–74.

    CAS  PubMed  Google Scholar 

  • 13.

    Foster KR, Wenseleers T. A general model for the evolution of mutualisms. J Evol Biol. 2006;19:1283–93.

    CAS  PubMed  Google Scholar 

  • 14.

    Weber KA, Achenbach LA, Coates JD. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol. 2006;4:752–64.

    CAS  PubMed  Google Scholar 

  • 15.

    Lüdecke C, Reiche M, Eusterhues K, Nietzsche S, Küsel K. Acid-tolerant microaerophilic Fe(II)-oxidizing bacteria promote Fe(III)-accumulation in a fen. Environ Microbiol. 2010;12:2814–25.

    PubMed  Google Scholar 

  • 16.

    Emerson D, Fleming EJ, McBeth JM. Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol. 2010;64:561–83.

    CAS  PubMed  Google Scholar 

  • 17.

    Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L, Munk C, et al. Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol. 2013;4:254.

    PubMed  PubMed Central  Google Scholar 

  • 18.

    Fabisch M, Beulig F, Akob DM, Küsel K. Surprising abundance of Gallionella-related iron oxidizers in creek sediments at pH 4.4 or at high heavy metal concentrations. Front Microbiol. 2013;4:390.

    PubMed  PubMed Central  Google Scholar 

  • 19.

    Fleming EJ, Cetinić I, Chan CS, Whitney King D, Emerson D. Ecological succession among iron-oxidizing bacteria. ISME J. 2014;8:804–15.

    CAS  PubMed  Google Scholar 

  • 20.

    Byrne JM, van der Laan G, Figueroa AI, Qafoku O, Wang C, Pearce CI, et al. Size dependent microbial oxidation and reduction of magnetite nano- and micro-particles. Sci Rep. 2016;6:1–13.

    Google Scholar 

  • 21.

    Byrne JM, Klueglein N, Pearce C, Rosso KM, Appel E, Kappler A. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science. 2015;347:1473–6.

  • 22.

    Braunschweig J, Bosch J, Meckenstock RU. Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation. N. Biotechnol. 2013;30:793–802.

    CAS  PubMed  Google Scholar 

  • 23.

    Bosch J, Heister K, Hofmann T, Meckenstock RU. Nanosized iron oxide colloids strongly enhance microbial iron reduction. Appl Environ Microbiol. 2010;76:184–9.

    CAS  PubMed  Google Scholar 

  • 24.

    Küsel K, Blöthe M, Schulz D, Reiche M, Drake HL. Microbial reduction of iron and porewater biogeochemistry in acidic peatlands. Biogeosci Discuss. 2008;5:2165–96.

    Google Scholar 

  • 25.

    Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA. 2008;105:3968–73.

    CAS  PubMed  Google Scholar 

  • 26.

    Royer RA, Burgos WD, Fisher AS, Unz RF, Dempsey BA. Enhancement of biological reduction of hematite by electron shuttling and Fe(II) complexation. Environ Sci Technol. 2002;36:1939–46.

    CAS  PubMed  Google Scholar 

  • 27.

    Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN, Richardson DJ, et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front Microbiol. 2015;6:332.

    PubMed  PubMed Central  Google Scholar 

  • 28.

    Hartshorne RS, Reardon CL, Ross D, Nuester J, Clarke TA, Gates AJ, et al. Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA. 2009;106:22169–74.

    CAS  PubMed  Google Scholar 

  • 29.

    White GF, Shi Z, Shi L, Wang Z, Dohnalkova AC, Marshall MJ, et al. Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals. Proc Natl Acad Sci USA. 2013;110:6346–51.

    CAS  PubMed  Google Scholar 

  • 30.

    Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, et al. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol. 1999;49:705–24.

    CAS  PubMed  Google Scholar 

  • 31.

    Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science. 1988;240:1319–21.

    CAS  PubMed  Google Scholar 

  • 32.

    Myers CR, Nealson KH. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciensMR-1. J Bacteriol. 1990;172:6232–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 33.

    McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D. Neutrophilic iron-oxidizing ‘Zetaproteobacteria’ and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol. 2011;77:1405–12.

    CAS  PubMed  Google Scholar 

  • 34.

    Mori JF, Ueberschaar N, Lu S, Cooper RE, Pohnert G, Küsel K. Sticking together: inter-species aggregation of bacteria isolated from iron snow is controlled by chemical signaling. ISME J. 2017;11:1075–86.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 35.

    Tamura H, Goto K, Yotsuyanagi T, Nagayama M. Spectrophotometric determination of iron(II) with 1,10-phenanthroline in the presence of large amounts of iron(III). Talanta. 1974;21:314–8.

    CAS  PubMed  Google Scholar 

  • 36.

    Cooper RE, Wegner C-E, McAllister SM, Shevchenko O, Chan CS, Küsel K. Draft genome sequence of Sideroxydanssp. Strain CL21, an Fe(II)-oxidizing bacterium. Microbiol Resour Announc. 2020;9:1–2.

  • 37.

    Wegner C-E, Gaspar M, Geesink P, Herrmann M, Marz M, Küsel K. Biogeochemical regimes in shallow aquifers reflect the metabolic coupling of the elements nitrogen, sulfur, and carbon. Appl Environ Microbiol. 2019;8:1–19.

  • 38.

    Andrews S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc..40.

  • 39.

    Bushnell B. BBMap short read aligner. https://www.sourceforge.net/projects/bbmap/..41.

  • 40.

    Kopylova E, Noé L, Touzet H, Noe L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.

    CAS  PubMed  Google Scholar 

  • 41.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.

    CAS  PubMed  Google Scholar 

  • 42.

    Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, et al. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res. 2013;41:D226–32.

    CAS  PubMed  Google Scholar 

  • 43.

    Heidelberg JF, Paulsen IT, Nelson KE, Gaidos EJ, Nelson WC, Read TD, et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol. 2002;20:1118–23.

    CAS  PubMed  Google Scholar 

  • 44.

    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAM tools. Bioinformatics. 2009;25:2078–9.

    PubMed  PubMed Central  Google Scholar 

  • 45.

    Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41:e108.

    PubMed  PubMed Central  Google Scholar 

  • 46.

    Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–30.

    CAS  Google Scholar 

  • 47.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018.

  • 48.

    Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.

    CAS  Google Scholar 

  • 49.

    Tautenhahn R, Patti GJ, Rinehart D, Siuzdak G. XCMS Online: a web-based platform to process untargeted metabolomic data. Anal Chem. 2012;84:5035–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 50.

    Stettin D, Poulin RX, Pohnert G. Metabolomics benefits fom orbitrap GC-MS—Comparison of low- and high-resolution GC-MS. Metabolites. 2020;10:1–16.

    Google Scholar 

  • 51.

    Chong J, Yamamoto M, Xia J. MetaboAnalystR 2.0: from raw spectra to biological insights. Metabolites. 2019;9:1–10.

  • 52.

    Hummel J, Strehmel N, Bölling C, Schmidt S, Walther D, Kopka J. Mass Spectral search and analysis using the golm metabolome database. In: Weckwerth W, Kahl G (eds). The handbook of plant metabolomics. 2013. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, p. 321–43.

  • 53.

    Lueder U, Druschel G, Emerson D, Kappler A, Schmidt C. Quantitative analysis of O2 and Fe2+ profiles in gradient tubes for cultivation of microaerophilic Iron(II)-oxidizing bacteria. FEMS Microbiol Ecol. 2018;94:1–15.

  • 54.

    Lefevre E, Bossa N, Wiesner MR, Gunsch CK. A review of the environmental implications of in situ remediation by nanoscale zero valent iron (nZVI): behavior, transport and impacts on microbial communities. Sci Total Environ. 2016;565:889–901.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 55.

    Kirschling TL, Gregory KB, Minkley EG Jr, Lowry GV, Tilton RD. Impact of nanoscale zero valent iron on geochemistry and microbial populations in trichloroethylene contaminated aquifer materials. Environ Sci Technol. 2010;44:3474–80.

    CAS  PubMed  Google Scholar 

  • 56.

    Wu S, Cajthaml T, Semerád J, Filipová A, Klementová M, Skála R, et al. Nano zero-valent iron aging interacts with the soil microbial community: a microcosm study. Environ Sci: Nano. 2019;6:1189–206.

    CAS  Google Scholar 

  • 57.

    Auffan M, Rose J, Wiesner MR, Bottero J-Y. Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ Pollut. 2009;157:1127–33.

    CAS  Google Scholar 

  • 58.

    Anza M, Salazar O, Epelde L, Alkorta I, Garbisu C. The application of nanoscale zero-valent iron promotes soil remediation while negatively affecting soil microbial biomass and activity. Front Environ Sci. 2019;7:1–6.

    Google Scholar 

  • 59.

    Friedrich B, Magasanik B. Enzymes of agmatine degradation and the control of their synthesis in Klebsiella aerogenes. J Bacteriol. 1979;137:1127–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 60.

    Kurihara S, Oda S, Kato K, Kim HG, Koyanagi T, Kumagai H, et al. A novel putrescine utilization pathway involves gamma-glutamylated intermediates of Escherichia coli K-12. J Biol Chem. 2005;280:4602–8.

    CAS  PubMed  Google Scholar 

  • 61.

    Hädrich A, Taillefert M, Akob DM, Cooper RE, Litzba U, Wagner FE, et al. Microbial Fe(II) oxidation by Sideroxydans lithotrophicus ES-1 in the presence of Schlöppnerbrunnen fen-derived humic acids. FEMS Microbiol Ecol. 2019;95:1–19.

  • 62.

    Cooper RE, Eusterhues K, Wegner C-E, Totsche KU, Küsel K. Ferrihydrite-associated organic matter (OM) stimulates reduction by Shewanella oneidensis MR-1 and a complex microbial consortia. Biogeosciences. 2017;14:5171–88.

    CAS  Google Scholar 

  • 63.

    Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C, Kennedy DW, et al. Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol. 2012;3:37.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 64.

    DiChristina TJ, Moore CM, Haller CA. Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol. 2002;184:142–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 65.

    Meshulam-Simon G, Behrens S, Choo AD, Spormann AM. Hydrogen metabolism in Shewanella oneidensis MR-1. Appl Environ Microbiol. 2007;73:1153–65.

    CAS  PubMed  Google Scholar 

  • 66.

    Shi L, Belchik SM, Plymale AE, Heald S, Dohnalkova AC, Sybirna K, et al. Purification and characterization of the [NiFe]-hydrogenase of Shewanella oneidensis MR-1. Appl Environ Microbiol. 2011;77:5584–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 67.

    Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev. 2001;25:455–501.

    CAS  PubMed  Google Scholar 

  • 68.

    Reiche M, Torburg G, Küsel K. Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol Ecol. 2008;65:88–101.

    CAS  PubMed  Google Scholar 

  • 69.

    Reiche M, Haedrich A, Lischeid G, Kuesel K, Hädrich A, Lischeid G, et al. Impact of manipulated drought and heavy rainfall events on peat mineralization processes and source-sink functions of an acidic fen. J Geophys Res-Biogeosci. 2009;114:1–13.

    Google Scholar 

  • 70.

    Hädrich A, Heuer VB, Herrmann M, Hinrichs K-U, Küsel K. Origin and fate of acetate in an acidic fen. FEMS Microbiol Ecol. 2012;81:339–54.

    PubMed  Google Scholar 

  • 71.

    Hamberger A, Horn MA, Dumont MG, Murrell JC, Drake HL. Anaerobic consumers of monosaccharides in a moderately acidic fen. Appl Environ Microbiol. 2008;74:3112–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 72.

    Wüst PK, Horn MA, Drake HL. Trophic links between fermenters and methanogens in a moderately acidic fen soil. Environ Microbiol. 2009;11:1395–409.

    PubMed  Google Scholar 

  • 73.

    Tabor CW, Tabor H. Polyamines. Annu Rev Biochem. 1984;53:749–90.

    CAS  PubMed  Google Scholar 

  • 74.

    Karatan E, Watnick P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev. 2009;73:310–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 75.

    Bachrach U, Heimer YM. The physiology of polyamines. 1989. CRC Press Taylor and Francis Group, Boca Raton, FL, USA.

  • 76.

    Karatan E, Duncan TR, Watnick PI. NspS, a predicted polyamine sensor, mediates activation of Vibrio cholerae biofilm formation by norspermidine. J Bacteriol. 2005;187:7434–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 77.

    Cockerell SR, Rutkovsky AC, Zayner JP, Cooper RE, Porter LR, Pendergraft SS, et al. Vibrio cholerae NspS, a homologue of ABC-type periplasmic solute binding proteins, facilitates transduction of polyamine signals independent of their transport. Microbiology. 2014;160:832–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 78.

    Matthysse AG, Yarnall HA, Young N. Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J Bacteriol. 1996;178:5302–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 79.

    Sauer K, Camper AK. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol. 2001;183:6579–89.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 80.

    Patel CN, Wortham BW, Lines JL, Fetherston JD, Perry RD, Oliveira MA. Polyamines are essential for the formation of plague biofilm. J Bacteriol. 2006;188:2355–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 81.

    Capdevila DA, Wang J, Giedroc DP. Bacterial strategies to maintain zinc metallostasis at the host–pathogen interface. J Biol Chem. 2016;291:20858–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 82.

    Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W. The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life. Sci Rep. 2012;2:263.

    PubMed  PubMed Central  Google Scholar 

  • 83.

    Reda T, Plugge CM, Abram NJ, Hirst J. Reversible interconversion of carbon dioxide and formate by an electroactive enzyme. Proc Natl Acad Sci USA. 2008;105:10654–8.

    CAS  PubMed  Google Scholar 

  • 84.

    Hartmann T, Schwanhold N, Leimkühler S. Assembly and catalysis of molybdenum or tungsten-containing formate dehydrogenases from bacteria. Biochim Biophys Acta. 2015;1854:1090–1100.

    CAS  PubMed  Google Scholar 

  • 85.

    Ilbert M, Bonnefoy V. Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta. 2013;1827:161–75.

    CAS  PubMed  Google Scholar 

  • 86.

    Lovley DR, Holmes DE, Nevin KP. Dissimilatory Fe(III) and Mn(IV) reduction. Adv Micro Physiol. 2004;49:219–86.

    CAS  Google Scholar 

  • 87.

    Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat Rev Microbiol. 2014;12:797–808.

    CAS  PubMed  Google Scholar 

  • 88.

    Maisch M, Lueder U, Laufer K, Scholze C, Kappler A, Schmidt C. Contribution of microaerophilic Iron(II)-oxidizers to Iron(III) mineral formation. Environ Sci Technol. 2019;53:8197–204.

    CAS  PubMed  Google Scholar 

  • 89.

    Hong Y, Wu J, Wilson S, Song B. Vertical stratification of sediment microbial communities along geochemical gradients of a subterranean estuary located at the Gloucester Beach of Virginia, United States. Front Microbiol. 2018;9:3343.

    PubMed  Google Scholar 

  • 90.

    Liptzin D, Silver WL. Spatial patterns in oxygen and redox sensitive biogeochemistry in tropical forest soils. Ecosphere. 2015;6:art211.

    Google Scholar 

  • 91.

    Borer B, Tecon R, Or D. Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks. Nat Commun. 2018;9:769.

    PubMed  PubMed Central  Google Scholar 

  • 92.

    Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, et al. Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J. 2016;10:2557–68.

    PubMed  PubMed Central  Google Scholar 

  • 93.

    Frey PA, Reed GH. The ubiquity of iron. ACS Chem Biol. 2012;7:1477–81.

    CAS  PubMed  Google Scholar 

  • 94.

    Edwards KJ, Bach W, McCollom TM, Rogers DR. Neutrophilic iron-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition, rock alteration, and biomass production in the deep-sea. Geomicrobiol J. 2004;21:393–404.

    CAS  Google Scholar 

  • 95.

    Bondici VF, Khan NH, Swerhone GDW, Dynes JJ, Lawrence JR, Yergeau E, et al. Biogeochemical activity of microbial biofilms in the water column overlying uranium mine tailings. J Appl Microbiol. 2014;117:1079–94.

    CAS  PubMed  Google Scholar 

  • 96.

    Lee AK, Newman DK. Microbial iron respiration: impacts on corrosion processes. Appl Microbiol Biotechnol. 2003;62:134–9.

    CAS  PubMed  Google Scholar 

  • 97.

    Glasser NR, Saunders SH, Newman DK. The colorful world of extracellular electron shuttles. Annu Rev Microbiol. 2017;71:731–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 98.

    Philips J, Verbeeck K, Rabaey K, Arends JBA. Electron transfer mechanisms in biofilms. In: Scott K, Yu EH (eds). Microbial electrochemical and fuel cells. 2016. Woodhead Publishing, Sawston, Cambridge, United Kingdom, p. 67–113.

  • 99.

    Gao L, Lu X, Liu H, Li J, Li W, Song R, et al. Mediation of extracellular polymeric substances in microbial reduction of hematite by Shewanella oneidensis MR-1. Front Microbiol. 2019;10:575.

    PubMed  PubMed Central  Google Scholar 

  • 100.

    Roden EE, McBeth JM, Blöthe M, Percak-Dennett EM, Fleming EJ, Holyoke RR, et al. The microbial ferrous wheel in a neutral pH groundwater seep. Front Microbiol. 2012;3:172.

    PubMed  PubMed Central  Google Scholar 


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