Dual Role of Humic Substances As Electron Donor and Shuttle for Dissimilatory Iron Reduction

Stern, Noah; Mejia, Jacqueline; He, Shaomei; Yang, Yu; Ginder-Vogel, Matthew; Roden, Eric E.

doi:10.1021/acs.est.7b06574

Dual Role of Humic Substances As Electron Donor and Shuttle for Dissimilatory Iron Reduction

Journal Article · Mon Apr 16 00:00:00 EDT 2018 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.7b06574· OSTI ID:1469803

Stern, Noah ^[1]; Mejia, Jacqueline ^[2]; He, Shaomei ^[3]; Yang, Yu ^[4]; ^[2]; ^[5]

Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering, Environmental Chemistry and Technology Program; Unniversity of Wisconsin Department of Geoscience
Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering, Environmental Chemistry and Technology Program
Univ. of Wisconsin, Madison, WI (United States). Dept. of Geoscience, Dept. of Bacteriology
Univ. of Nevada, Reno, NV (United States). Dept. of Civil and Environmental Engineering
Univ. of Wisconsin, Madison, WI (United States). Dept. of Geoscience

Dissimilatory iron-reducing bacteria (DIRB) are known to use humic substances (HS) as electron shuttles for dissimilatory iron reduction (DIR) by transferring electrons to HS-quinone moieties, which in turn rapidly reduce Fe(III) oxides. However, the potential for HS to serve as a source of organic carbon (OC) that can donate electrons for DIR is unknown. We studied whether humic acids (HA) and humins (HM) recovered from peat soil by sodium pyrophosphate extraction could serve as both electron shuttles and electron donors for DIR by freshwater sediment microorganisms. Both HA and HM served as electron shuttles in cultures amended with glucose. However, only HA served as an electron donor for DIR. Metagenomes from HA-containing cultures had an overrepresentation of genes involved in polysaccharide and to a lesser extent aromatic compound degradation, suggesting complex OC metabolism. Genomic searches for the porin-cytochrome complex involved in DIR resulted in matches to Ignavibacterium/Melioribacter, DIRB capable of polymeric OC metabolism. These results indicate that such taxa may have played a role in both DIR and decomposition of complex OC. Our results suggest that decomposition of HS coupled to DIR and other anaerobic pathways could play an important role in soil and sediment OC metabolism.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0016217

OSTI ID:: 1469803

Alternate ID(s):: OSTI ID: 1480447

Journal Information:: Environmental Science and Technology, Journal Name: Environmental Science and Technology Journal Issue: 10 Vol. 52; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (67)

Mechanisms regulating bioavailability of phenanthrene sorbed on a peat soil-origin humic substance Yang, Yu; Shu, Liang; Wang, Xilong Environmental Toxicology and Chemistry, Vol. 31, Issue 7 https://doi.org/10.1002/etc.1844	journal	May 2012
Association of organic matter with iron and aluminum across a range of soils determined via selective dissolution techniques coupled with dissolved nitrogen analysis Wagai, Rota; Mayer, Lawrence M.; Kitayama, Kanehiro Biogeochemistry, Vol. 112, Issue 1-3 https://doi.org/10.1007/s10533-011-9652-5	journal	September 2011
Review on iron availability in soil: interaction of Fe minerals, plants, and microbes Colombo, Claudio; Palumbo, Giuseppe; He, Ji-Zheng Journal of Soils and Sediments, Vol. 14, Issue 3 https://doi.org/10.1007/s11368-013-0814-z	journal	November 2013
Biodegradation of soil-derived dissolved organic matter as related to its properties Kalbitz, K.; Schmerwitz, J.; Schwesig, D. Geoderma, Vol. 113, Issue 3-4 https://doi.org/10.1016/S0016-7061(02)00365-8	journal	May 2003
Dissimilatory Fe(III) and Mn(IV) Reduction Lovley, Derek R.; Holmes, Dawn E.; Nevin, Kelly P. Advances in Microbial Physiology https://doi.org/10.1016/S0065-2911(04)49005-5	book	January 2004
Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment Kappler, Andreas; Benz, Marcus; Schink, Bernhard FEMS Microbiology Ecology, Vol. 47, Issue 1 https://doi.org/10.1016/S0168-6496(03)00245-9	journal	January 2004
Asynchronous reductive release of iron and organic carbon from hematite–humic acid complexes Adhikari, Dinesh; Poulson, Simon R.; Sumaila, Samira Chemical Geology, Vol. 430 https://doi.org/10.1016/j.chemgeo.2016.03.013	journal	July 2016
Coupled dynamics of iron and iron-bound organic carbon in forest soils during anaerobic reduction Zhao, Qian; Adhikari, Dinesh; Huang, Rixiang Chemical Geology, Vol. 464 https://doi.org/10.1016/j.chemgeo.2016.12.014	journal	August 2017
The role of carbon starvation in the induction of enzymes that degrade plant-derived carbohydrates in Aspergillus niger van Munster, Jolanda M.; Daly, Paul; Delmas, Stéphane Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.04.006	journal	November 2014
Sorptive stabilization of organic matter in soils by hydrous iron oxides Wagai, Rota; Mayer, Lawrence M. Geochimica et Cosmochimica Acta, Vol. 71, Issue 1 https://doi.org/10.1016/j.gca.2006.08.047	journal	January 2007
Dynamics of ferrihydrite-bound organic carbon during microbial Fe reduction Adhikari, Dinesh; Zhao, Qian; Das, Kamol Geochimica et Cosmochimica Acta, Vol. 212 https://doi.org/10.1016/j.gca.2017.06.017	journal	September 2017
Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules Lorenz, Klaus; Lal, Rattan; Preston, Caroline M. Geoderma, Vol. 142, Issue 1-2 https://doi.org/10.1016/j.geoderma.2007.07.013	journal	November 2007
Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest Nemergut, Diana R.; Cleveland, Cory C.; Wieder, William R. Soil Biology and Biochemistry, Vol. 42, Issue 12 https://doi.org/10.1016/j.soilbio.2010.08.011	journal	December 2010
Ferrozine---a new spectrophotometric reagent for iron Stookey, Lawrence L. Analytical Chemistry, Vol. 42, Issue 7, p. 779-781 https://doi.org/10.1021/ac60289a016	journal	June 1970
Sorption Mechanisms of Phenanthrene, Lindane, and Atrazine with Various Humic Acid Fractions from a Single Soil Sample Wang, Xilong; Guo, Xiaoying; Yang, Yu Environmental Science & Technology, Vol. 45, Issue 6 https://doi.org/10.1021/es102468z	journal	March 2011
Impact of De-Ashing Humic Acid and Humin on Organic Matter Structural Properties and Sorption Mechanisms of Phenanthrene Yang, Yu; Shu, Liang; Wang, Xilong Environmental Science & Technology, Vol. 45, Issue 9 https://doi.org/10.1021/es2003149	journal	May 2011
Kinetics of Microbial and Chemical Reduction of Humic Substances: Implications for Electron Shuttling Jiang, Jie; Kappler, Andreas Environmental Science & Technology, Vol. 42, Issue 10 https://doi.org/10.1021/es7023803	journal	May 2008
Quinone Moieties Act as Electron Acceptors in the Reduction of Humic Substances by Humics-Reducing Microorganisms Scott, Durelle T.; McKnight, Diane M.; Blunt-Harris, Elizabeth L. Environmental Science & Technology, Vol. 32, Issue 19 https://doi.org/10.1021/es980272q	journal	October 1998
Oxidation of aromatic contaminants coupled to microbial iron reduction Lovley, Derek R.; Baedecker, Mary Jo; Lonergan, Debra J. Nature, Vol. 339, Issue 6222 https://doi.org/10.1038/339297a0	journal	May 1989
Humic substances as electron acceptors for microbial respiration Lovley, Derek R.; Coates, John D.; Blunt-Harris, Elizabeth L. Nature, Vol. 382, Issue 6590 https://doi.org/10.1038/382445a0	journal	August 1996
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite Warnecke, Falk; Luginbühl, Peter; Ivanova, Natalia Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06269	journal	November 2007
Preservation of organic matter in sediments promoted by iron Lalonde, Karine; Mucci, Alfonso; Ouellet, Alexandre Nature, Vol. 483, Issue 7388 https://doi.org/10.1038/nature10855	journal	March 2012
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Humic substances as fully regenerable electron acceptors in recurrently anoxic environments Klüpfel, Laura; Piepenbrock, Annette; Kappler, Andreas Nature Geoscience, Vol. 7, Issue 3 https://doi.org/10.1038/ngeo2084	journal	February 2014
Extracellular electron transfer through microbial reduction of solid-phase humic substances Roden, Eric E.; Kappler, Andreas; Bauer, Iris Nature Geoscience, Vol. 3, Issue 6 https://doi.org/10.1038/ngeo870	journal	May 2010
The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle Melton, Emily D.; Swanner, Elizabeth D.; Behrens, Sebastian Nature Reviews Microbiology, Vol. 12, Issue 12 https://doi.org/10.1038/nrmicro3347	journal	October 2014
Anaerobic decomposition of humic substances by Clostridium from the deep subsurface Ueno, Akio; Shimizu, Satoru; Tamamura, Shuji Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep18990	journal	January 2016
What is recalcitrant soil organic matter? Kleber, Markus Environmental Chemistry, Vol. 7, Issue 4 https://doi.org/10.1071/EN10006	journal	January 2010
Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens Reardon, Patrick N.; Mueller, Karl T. Journal of Biological Chemistry, Vol. 288, Issue 41 https://doi.org/10.1074/jbc.M113.498527	journal	August 2013
The GH130 Family of Mannoside Phosphorylases Contains Glycoside Hydrolases That Target β-1,2-Mannosidic Linkages in Candida Mannan Cuskin, Fiona; Baslé, Arnaud; Ladevèze, Simon Journal of Biological Chemistry, Vol. 290, Issue 41 https://doi.org/10.1074/jbc.M115.681460	journal	August 2015
Influence of Biogenic Fe(II) on Bacterial Crystalline Fe(III) Oxide Reduction Roden, Eric E.; Urrutia, Matilde M. Geomicrobiology Journal, Vol. 19, Issue 2 https://doi.org/10.1080/01490450252864280	journal	March 2002
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
PRED-TMBB: a web server for predicting the topology of -barrel outer membrane proteins Bagos, P. G.; Liakopoulos, T. D.; Spyropoulos, I. C. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh417	journal	July 2004
PROMALS3D: a tool for multiple protein sequence and structure alignments Pei, Jimin; Kim, Bong-Hyun; Grishin, Nick V. Nucleic Acids Research, Vol. 36, Issue 7 https://doi.org/10.1093/nar/gkn072	journal	February 2008
IMG: the integrated microbial genomes database and comparative analysis system Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1044	journal	December 2011
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
KEGG: new perspectives on genomes, pathways, diseases and drugs Kanehisa, Minoru; Furumichi, Miho; Tanabe, Mao Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1092	journal	November 2016
Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer Coates, J. D.; Ellis, D. J.; Gaw, C. V. International Journal of Systematic Bacteriology, Vol. 49, Issue 4 https://doi.org/10.1099/00207713-49-4-1615	journal	October 1999
Ignavibacterium album gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from microbial mats at a terrestrial hot spring and proposal of Ignavibacteria classis nov., for a novel lineage at the periphery of green sulfur bacteria Iino, T.; Mori, K.; Uchino, Y. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 6 https://doi.org/10.1099/ijs.0.012484-0	journal	August 2009
Integrative analysis of environmental sequences using MEGAN4 Huson, D. H.; Mitra, S.; Ruscheweyh, H. -J. Genome Research, Vol. 21, Issue 9 https://doi.org/10.1101/gr.120618.111	journal	June 2011
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
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 I gnavibacteriae Podosokorskaya, Olga A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12067	journal	January 2013
A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by G eobacter sulfurreducens PCA : A trans-outer membrane electron transfer complex Liu, Yimo; Wang, Zheming; Liu, Juan Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12204	journal	September 2014
Microbial Fe(III) oxide reduction potential in Chocolate Pots hot spring, Yellowstone National Park Fortney, N. W.; He, S.; Converse, B. J. Geobiology, Vol. 14, Issue 3 https://doi.org/10.1111/gbi.12173	journal	January 2016
Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen: Metabolic response of soil cellulose degraders Schellenberger, Stefanie; Kolb, Steffen; Drake, Harold L. Environmental Microbiology, Vol. 12, Issue 4 https://doi.org/10.1111/j.1462-2920.2009.02128.x	journal	December 2009
Bioavailability of soil organic matter and microbial community dynamics upon permafrost thaw: Bioavailability of permafrost organic matter Coolen, Marco J. L.; van de Giessen, Jeroen; Zhu, Elizabeth Y. Environmental Microbiology, Vol. 13, Issue 8 https://doi.org/10.1111/j.1462-2920.2011.02489.x	journal	May 2011
The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer Shi, Liang; Richardson, David J.; Wang, Zheming Environmental Microbiology Reports, Vol. 1, Issue 4 https://doi.org/10.1111/j.1758-2229.2009.00035.x	journal	August 2009
Microbial Metabolic Potential for Carbon Degradation and Nutrient (Nitrogen and Phosphorus) Acquisition in an Ombrotrophic Peatland Lin, Xueju; Tfaily, Malak M.; Green, Stefan J. Applied and Environmental Microbiology, Vol. 80, Issue 11 https://doi.org/10.1128/AEM.00206-14	journal	March 2014
Requirement for a Microbial Consortium To Completely Oxidize Glucose in Fe(III)-Reducing Sediments Lovley, Derek R.; Phillips, Elizabeth J. P. Applied and Environmental Microbiology, Vol. 55, Issue 12 https://doi.org/10.1128/AEM.55.12.3234-3236.1989	journal	January 1989
Anaerobic Oxidation of Toluene, Phenol, and p-Cresol by the Dissimilatory Iron-Reducing Organism, GS-15 Lovley, Derek R.; Lonergan, Debra J. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/AEM.56.6.1858-1864.1990	journal	January 1990
Recovery of Humic-Reducing Bacteria from a Diversity of Environments Coates, John D.; Ellis, Debra J.; Blunt-Harris, Elizabeth L. Applied and Environmental Microbiology, Vol. 64, Issue 4 https://doi.org/10.1128/AEM.64.4.1504-1509.1998	journal	April 1998
Diversion of Electron Flow from Methanogenesis to Crystalline Fe(III) Oxide Reduction in Carbon-Limited Cultures of Wetland Sediment Microorganisms Roden, Eric E. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5702-5706.2003	journal	September 2003
Possible Nonconductive Role of Geobacter sulfurreducens Pilus Nanowires in Biofilm Formation Reguera, G.; Pollina, R. B.; Nicoll, J. S. Journal of Bacteriology, Vol. 189, Issue 5, p. 2125-2127 https://doi.org/10.1128/JB.01284-06	journal	December 2006
A new Generation of Homology Search Tools Based on Probabilistic Inference Eddy, Sean R. Proceedings of the 20th International Conference, Genome Informatics 2009 https://doi.org/10.1142/9781848165632_0019	conference	March 2012
MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm Wu, Yu-Wei; Tang, Yung-Hsu; Tringe, Susannah G. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-26	journal	August 2014
Genomic characterization of plant cell wall degrading enzymes and in silico analysis of xylanses and polygalacturonases of Fusarium virguliforme Chang, Hao-Xun; Yendrek, Craig R.; Caetano-Anolles, Gustavo BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0761-0	journal	July 2016
Comparative analysis of sugarcane bagasse metagenome reveals unique and conserved biomass-degrading enzymes among lignocellulolytic microbial communities Mhuantong, Wuttichai; Charoensawan, Varodom; Kanokratana, Pattanop Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0200-8	journal	January 2015
Metagenomic analysis of microbial consortia enriched from compost: new insights into the role of Actinobacteria in lignocellulose decomposition Wang, Cheng; Dong, Da; Wang, Haoshu Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0440-2	journal	January 2016
Comparative Metagenomic and Metatranscriptomic Analysis of Hindgut Paunch Microbiota in Wood- and Dung-Feeding Higher Termites He, Shaomei; Ivanova, Natalia; Kirton, Edward PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061126	journal	April 2013
Metagenomic Insights into Metabolic Capacities of the Gut Microbiota in a Fungus-Cultivating Termite (Odontotermes yunnanensis) Liu, Ning; Zhang, Lei; Zhou, Haokui PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069184	journal	July 2013
Comparative Analysis of Carbohydrate Active Enzymes in Clostridium termitidis CT1112 Reveals Complex Carbohydrate Degradation Ability Munir, Riffat I.; Schellenberg, John; Henrissat, Bernard PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104260	journal	August 2014
Identification of the Core Set of Carbon-Associated Genes in a Bioenergy Grassland Soil Howe, Adina; Yang, Fan; Williams, Ryan J. PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0166578	journal	November 2016
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014

Cited By (3)

Dissimilatory reduction of Fe(III) by a novel Serratia marcescens strain with special insight into the influence of prodigiosin Castillo-Zacarías, Carlos; Cantú-Cárdenas, María Elena; López-Chuken, Ulrico Javier International Microbiology, Vol. 23, Issue 2 https://doi.org/10.1007/s10123-019-00088-y	journal	July 2019
Iron and nitrogen cycling, bacterioplankton community composition and mineral transformations involving phosphorus stabilisation in the ferruginous hypolimnion of a post-mining lake Petrash, Daniel A.; Jan, Jiří; Sirová, Dagmara Environmental Science: Processes & Impacts, Vol. 20, Issue 10 https://doi.org/10.1039/c8em00328a	journal	January 2018
Role of Humic Acid Chemical Structure Derived from Different Biomass Feedstocks on Fe(III) Bioreduction Activity: Implication for Sustainable Use of Bioresources Wei, Yuquan; Wei, Zimin; Zhang, Fang Catalysts, Vol. 9, Issue 5 https://doi.org/10.3390/catal9050450	journal	May 2019

Similar Records

Stability of Ferrihydrite–Humic Acid Coprecipitates under Iron-Reducing Conditions

Journal Article · Thu Oct 25 00:00:00 EDT 2018 · Environmental Science and Technology · OSTI ID:1812867

Role of clay-associated humic substances in catalyzing bioreduction of structural Fe(III) in nontronite by Shewanella putrefaciens CN32

Journal Article · Fri Jun 19 00:00:00 EDT 2020 · Science of the Total Environment · OSTI ID:1646332

Related Subjects

54 ENVIRONMENTAL SCIENCES

Dual Role of Humic Substances As Electron Donor and Shuttle for Dissimilatory Iron Reduction

Citation Formats

References (67)

Cited By (3)

Similar Records

Related Subjects